3.1. INTRODUCTION

Insects are the most diverse and abundant animal group, representing more than 70% of all known animal species. They display a range of sophisticated and adaptive behaviors based on the perception of a multitude of stimuli. Within the incoming stream of multimodal sensory information, olfactory signals often serve as key stimuli or releasers for the initiation of behaviors such as orientation toward mating partners, localization of appropriate sites for oviposition, and foraging. The vitally important role of olfaction is a general phenomenon across the animal kingdom.

Insects are valuable model systems in neuroscience due to the balance between the moderate complexity of their nervous systems, a rich behavioral repertoire, and the low cost of maintenance as experimental animals. Insect brains contain on the order of 10⁵ to 10⁶ neurons, thus they range slightly above Aplysia in this measure, but below Octopus (>10⁸), which is comparable to small mammals (mouse: ca. 5 × 10⁷). For comparison, the human brain contains on the order of 10¹¹ neurons. The concept of individually identifiable neurons and small networks as functional units have been vital for understanding insect brains, whose main properties are processing speed, relative simplicity, and elegant design principles.

Moreover, insects are well suited for multidisciplinary studies in brain research involving a combined approach at various levels, from molecules to single neurons to neural networks, behavior, and modeling. These preparations are amenable to a wide variety of methodological approaches, in particular genetic engineering, neuroanatomy, electrophysiology, and functional imaging. The similarity in the construction principles of central olfactory processing areas between insects and vertebrates and the common structural units of olfactory processing, called glomeruli, have made insects valuable model systems for investigating general mechanisms of olfactory information processing (Hildebrand and Shepherd 1997; Rössler et al. 2002). The striking similarity in the design of olfactory systems suggests that there are optimized solutions to deal with this kind of stimulus space, whose relevant metrics are still poorly understood. Odor-induced behaviors and their plasticity in insects have also led to important advances in the understanding of learning and memory (Menzel 2001). Even on shorter timescales of odor-induced orientation, flexibility and reliability are features that characterize insect behavior. In particular, moths have been a model system with a long-standing tradition being able to localize a female or pheromone source over long distances in natural environments despite (or because of?) the intermittent stimulus characteristics caused by turbulent flows.

In the present context, we cover, without claiming an exhaustive review of the vast literature, the current state of knowledge concerning moth olfactory behaviors, their plasticity, and the underlying neural mechanisms. These encompass the structure and function of olfactory sensory organs, the molecular mechanisms of olfactory transduction, and the anatomical and physiological properties of olfactory neurons and circuits in the brain, which deliver outputs for the control of behavior.

While there is also a large body of work on the development of the olfactory system in moths that is important for our understanding of the generation of the structural characteristics of olfactory systems, we refer the reader to available reviews covering this topic (Keil 1992; Oland and Tolbert 1996; Salecker and Malun 1999; Tolbert et al. 2004).

3.2. OLFACTORY BEHAVIOR

Insects are well known for their rich repertoire of olfactory behaviors (Hartlieb and Anderson 1999). Odorants important for moth behavior may be classified as either species-specific pheromones or so-called general odors that are not involved in intraspecific communication. In broad terms, olfactory-induced behaviors in moths can be associated with the contexts of reproduction or foraging and feeding. While olfaction is the dominant modality in reproductive behaviors, visual cues can take precedence in foraging when approaching flowers (Balkenius et al. 2006; Goyret et al. 2007). A factor that must always be considered is that under natural conditions, olfactory stimuli have peculiar properties: they are discontinuous in time at a fixed spatial location, in the form of odor plumes (Murlis et al. 1992).

3.2.1. Pheromone-Related Behaviors

Sex pheromones released by female moths represent a special class of odors because their signals are processed by conspicuous sexually dimorphic structures in the male moth nervous system (see Section 3.5.1.1). Males are attracted to substances produced by females. In some cases, as in Bombyx mori (Butenandt et al. 1959; Kramer 1975), a single component from the mixture released can be behaviorally effective, while in others, such as Manduca sexta (Tumlinson et al. 1989), a particular mixture of components, a blend, is necessary (Roelofs 1995). Besides sex pheromones, oviposition pheromones have been found in larval feces, acting as deterrents (Anderson et al. 1993).

Male moths use specific strategies for localizing pheromone sources. Flying moths display a characteristic orientation behavior toward pheromone sources that is supported by optomotor anemotaxis (Kennedy and Marsh 1974), a topic that has been a major focus of research in moth olfactory studies (Baker 1986; Arbas 1997; Baker and Vickers 1997; Cardé and Mafra-Neto 1997; Willis and Arbas 1997; Witzgall 1997). Upon exposure to pheromones, moths take flight upwind in a zigzagging pattern of straight segments at small angles with respect to the wind direction (so-called surge) and counterturns that change into crossing the wind at large angles with little or no net progression (so-called casting) upon odor loss (Kennedy 1983; Figure 3.1A through C). The properties of the behavior are species-specific and also depend on pheromone (blend) concentration (Cardé and Hagaman 1979; Kuenen and Baker 1982; Willis and Arbas 1991; Mafra-Neto and Cardé 1995; Justus and Cardé 2002). Some evidence, however, has led to the postulation of an intrinsic wind-independent turn-generating mechanism (Kennedy et al. 1980; Baker and Kuenen 1982; Kuenen and Baker 1983; Baker et al. 1984). Pheromone orientation should be evaluated in the context of realistic stimulus conditions (Vickers 2000, 2006; Cardé and Willis 2008) and indeed, efficient pheromone source localization depends on temporally fluctuating pheromone concentrations encountered by a moth (Kennedy et al. 1980; Willis and Baker 1984; Baker et al. 1985), with counterturn rates decreasing with increasing pulse frequency, inducing straighter upwind flight paths (Mafra-Neto and Cardé 1994; Vickers and Baker 1994; Figure 3.1A through C). These results support the idea that the flight pattern may consist of two basic elements, surges and casts, internally generated following the first interception of the pheromone stimulus. It should be noted that intermittency of the stimulation also appears to be necessary for the suppression of casting. The combination of surges and casts, the involvement of opto-motor anemotaxis, as well as the temporal pheromone stimulation pattern, is thought to result in the behaviors observed. Essentially, this view corresponds to Baker’s (1990) model in which surges are initiated by the encounter with strands of pheromone, and casting is initiated upon the encounter of pockets of clean air of sufficient duration in the plume (see also Figure 3.1C). Kaissling and Kramer (1990) also put forward similar concept. However, some moths show regular turning spontaneously without an olfactory stimulus, and their behavior suggests that odor source localization is an actively generated and continuously modulated ongoing pattern of upwind surges and counterturns matched for sampling sensory information (Willis and Arbas 1997, 1998). As a result, the detailed mechanisms of the generation of pheromone orientation behavior are still a matter of debate (Vickers 2006). After a male moth has located a female, various cues, including male pheromones, are involved in courtship prior to copulation (Krasnoff et al. 1987; Charlton and Cardé 1989).

FIGURE 3.1

Orientation of male moths to pheromone stimulation. (A) Cadra cautella male orienting in a wind tunnel in response to a pheromone plume pulsed at low frequency. (B) as (A) but with higher pheromone stimulus pulse frequency. (C) Flight track of a Heliothis (more...)

The fightless male B. mori has been particularly useful to investigate pheromone orientation, as there are hardly any other behaviors that the males engage in and movements are restricted to two dimensions in this species (Kanzaki 1997). Despite the similarities with fying moths and the proposal of a unified model (Kramer 1997), the mechanisms are not necessarily identical: for instance, in response to pheromones, fying Grapholita molesta show counterturning while they orient in rather straight upwind paths when walking (Willis and Baker 1987). The locomotor pattern of B. mori in pheromone orientation depends on the temporal structure of the stimulation (Kramer 1975, 1986, 1992; Kanzaki et al. 1992). With naturalistic pulsed stimulation, a characteristic zigzag upwind walking pattern is observed (Figure 3.1D), which can also be supported by wing-beat induced displacement after leg ablation (Kanzaki 1998). As in fying moths, there is evidence for an internal turn generator (Kanzaki et al. 1992). The elementary sequence of pheromone-induced programmed behavior in response to a single pulse is thought to consist of a short straight surge, followed by turning and counterturning, and finally by cycloids (looping). Over some frequency range, zigzag walking is induced, but paths become straighter with increasing frequency. The locomotor pattern is associated with abdominal bending, neck turning, antennal posture, and wing posture responses (Olberg 1983; Kanzaki 1998; Mishima and Kanzaki 1998; Figure 3.1D).

3.3. PERIPHERAL OLFACTORY PROCESSING

At the base of mechanisms generating olfactory behavior are the neural substrates detecting and processing olfactory information. This sequence of events starts with the reception of odorant molecules by sensory organs. The insect cuticle is covered by specializations of numerous morphological types for sensing chemical, thermal, and mechanical stimuli, sensory organs known as sensilla (Altner and Prillinger 1980). Among the body appendages, antennae assume a special role as compound multimodal sensory organs with a large number of olfactory sensilla. In moths, the most common type of olfactory sensillum has the shape of a hair characterized by the presence of numerous minute pores on its surface. Each sensillum contains multiple olfactory receptor neurons (ORNs), whose dendrites extend into the sensillar lumen. Odorant signals detected at the dendritic membrane are transduced into electric signals and transmitted to the brain. In this section, we summarize olfactory processing occurring at the peripheral level with an emphasis on the recent progress in the understanding of the molecular mechanism of pheromone reception.

3.3.1. Structure of Olfactory Sensilla

Insect ORNs are bipolar and housed in cuticular specializations characterized by multiple pores (Figure 3.2) (reviewed in Keil 1999; Steinbrecht 1999). The size of the pores is in the range of 10–100 nm, which is suited to allow the passage of odorants while preventing dessication of the sensillum. The number of ORNs in a single sensillum is two to four in many cases. Three types of auxiliary cells surround the cell bodies and inner dendrites of ORNs: the tormogen, trichogen, and thecogen cells (Figure 3.2C). Transport processes in the auxiliary cells and septate junctions between them and tight contacts of the tormogen cell with the adjacent cuticle give rise to a lymph space surrounding the outer dendrites of the ORNs that is isolated from the hemolymph. Differences in chemical composition of the sensillum lymph and the hemolymph bring about a standing electrical potential difference, the transepithelial potential (TEP) (see Morita and Shiraishi 1985; Kijima et al. 1995). Odorant stimulation generates a receptor potential in the outer dendritic membrane, which can induce the generation of action potentials in a more proximally located spike-generating zone. Olfactory sensilla are categorized into several types by their outer shape (s. trichodea, s. basiconica, s. coeloconica, s. placodea, etc.), while the basic structure is conserved among them.

FIGURE 3.2

Main olfactory sensory organs of the silk moth, Bombyx mori. (A) A male silk moth with its prominent antennae optimized for odorant detection. (B) Scanning electron micrograph of the antenna, displaying the external morphology of sensilla trichodea. Scale (more...)

3.3.4. Molecular Mechanism of Odorant Reception

Moth antennae, especially in males, are often carefully tuned systems to optimize odorant catch (Adam and Delbrück 1968; Kaissling and Priesner 1970; Koehl 2006). Once odorants are absorbed on the cuticular surface, they can diffuse inside the sensilla through sensillar pores. When odorants enter the sensillum lymph surrounding the dendritic membrane of ORNs, two kinds of processes occur. At frst, perireceptor events (Getchell et al. 1984) take place in proximity of the ORNs and determine the residence time of odorants in the sensillum lymph, as well as the efficiency of odorant transfer to the ORN membrane. After these processes, receptor events occur by the spe-cific interaction of odorants with olfactory receptor proteins (ORs), which lead to the activation of the chemoelectric transduction machinery in the ORN. Although recent evidence has accumulated pointing toward the specific interaction of odorants with ORs as the critical step for the detection and discrimination of odors (de Bruyne and Baker 2008), the understanding of perireceptor events is also vital.

3.3.4.1. Perireceptor Events

3.3.4.1.1. Odorant-Binding Proteins

Due to the hydrophobic nature of volatile odorants, the aqueous sensillum lymph represents a hydrophilic barrier impeding the diffusion of odorants toward the dendritic membrane of ORNs. This problem has been resolved by the expression of small (about 15 kDa) soluble proteins, termed odorant-binding proteins (OBP), which are extremely abundant in the sensillum lymph and thought to bind and transfer odorants to the ORNs (Pelosi et al. 2006). The first OBP described was discovered in the sensillum lymph of Antheraea polyphemus (Vogt and Riddiford 1981). OBPs have since been found in many insects, including numerous moth species (Pelosi et al. 2006). In moths, OBPs are grouped into four classes based on their amino acid sequence similarity: pheromone-binding proteins (PBPs), two types of general odorant-binding proteins (GOBP1 and GOBP2), and the antennal binding protein X (ABPX; Vogt et al. 1991, 1999). These proteins are synthesized by tormogen and trichogen cells, which secrete them into the sensillum lymph (Laue and Steinbrecht 1997). Their expression pattern and close relationship with particular sensillum types indicate a functional differentiation of the OBPs. In general, PBPs are predominantly expressed in the male antennae and are localized in the sensillum lymph of pheromone-sensitive s. trichodea, while other OBPs are expressed at a similar level in both the male and female antennae in s. basiconica (Steinbrecht et al. 1995), which are believed to respond to plant-derived odorants.

OBPs are thought to function as passive carriers for odorants. For instance, PBP undergoes a conformational change when the pH becomes more acidic, as would be expected to occur by virtue of the fxed negative charges on the cell membrane. This conformational change might result in the release of the bound pheromone onto the dendritic membrane of the ORN (Wojtasek and Leal 1999). This hypothesis has been supported by subsequent structural analyses showing that conformational changes at acidic pH lead to the release of bound bombykol in B. mori PBP (Tegoni et al. 2004). Besides their function as odorant carriers, OBPs have been suggested to be involved in odorant discrimination by functioning as a molecular flter for odorants to cross the sensillum lymph, and may also have a role in the activation of ORs (Kaissling 2001; Pophof 2004). While the specificity of ORs could be enhanced by OBPs (Große-Wilde et al. 2006), the latter are not essential for the activation of ORs and specific responses of ORNs, since heterologous expression of ORs in the absence of OBPs results in responses to odorants as selective as in in vivo ORNs (Wetzel et al. 2001; Sakurai et al. 2004; Nakagawa et al. 2005; Große-Wilde et al. 2006).

3.3.4.1.2. Odorant Degrading Enzymes

For efficient orientation of male moths toward females, the capability of following an intermittent pheromone trail comprising pockets of pheromone-free air is paramount. This requires sufficiently high temporal resolution of the male sensory apparatus. In fact, electrophysiological recordings under pulsed pheromone stimulation revealed that the temporal resolution of male antennae is in the range 5–33 Hz (Rumbo and Kaissling 1989; Marion-Poll and Tobin 1992; Bau et al. 2002, 2005). Thus, after activating ORs, odorants must be inactivated and eliminated rapidly to maintain high sensitivity to incoming stimuli. To accomplish such a rapid inactivation of odorants, the sensillum lymph contains odorant degrading enzymes (ODE) that enzymatically modify odorants into inactive substances. Two types of ODEs for pheromones (PDE: pheromone degrading enzyme) have been characterized in sen-sillum lymph; a sensillar esterase in A. polyphemus (Vogt et al. 1981, 1985) and an aldehyde oxidase in M. sexta (Rybczynski et al. 1989). Based on the kinetics of these enzymes, the half-life of pheromone molecules in sensillum lymph was estimated to be 15 and 0.6 ms in A. polyphemus and M. sexta, respectively (Vogt et al. 1985; Rybczynski et al. 1989). Recently, a gene encoding a sensillar esterase with properties similar to that previously isolated was identified from A. polyphemus male antennae, and named ApolPDE (Ishida and Leal 2005). The enzymatic efficiency of purified ApolPDE is about fortyfold higher than that of partially purified PDE by Vogt et al. (1985). The properties of ApolPDE are sufficient to explain the temporal resolution observed in physiology and behavior. Furthermore, the authors showed that the kinetics of pheromone degradation by ApolPDE were slowed at acidic pH, which may prevent degrading pheromones released from PBPs in close proximity to the dendritic membrane (Ishida and Leal 2005). In contrast to PDE, little research has been concerned with ODEs for general odorants, which have, so far, not been reported in moths.

3.3.4.2. Olfactory Receptors (ORs) in Moths

Odorants delivered by OBPs are bound by ORs in the dendritic membrane of ORNs. ORs in insects were first identified in Drosophila melanogaster through genome surveys of 7-transmembrane receptors (Clyne et al. 1999; Vosshall et al. 1999). In moths, ORs have been identified in several species (Krieger et al. 2002, 2004; Sakurai et al. 2004; Nakagawa et al. 2005; Wanner et al. 2007; Mitsuno et al. 2008). Although insect ORs are predicted to be 7-transmembrane proteins like vertebrate G-protein-coupled ORs (Firestein 2001; see also Chapter 7), there is no relationship in their amino acid sequences with vertebrate ORs or any known G-protein-coupled receptors (GPCRs) (Clyne et al. 1999; Vosshall et al. 1999). The B. mori genome project provided almost the entire genome sequence and 64 candidate OR genes were predicted (Xiang et al. 2009). In D. melano-gaster, it has been shown that each ORN expresses a single or a few ORs, and ORNs expressing the same OR(s) convergently project into a single glomerulus to create a topographic map of odor information in the Antennal Lobe (AL) (Vosshall et al. 2000; Gao et al. 2000; Fishilevich and Vosshall 2005; Couto et al. 2005). Such principles may be applicable in the moth olfactory system, as the number of candidate OR genes is well correlated with that of the glomeruli in the AL of B. mori (Kazawa et al. 2009; see also Section 3.5.3). Although the ligands for most of the moth candidate ORs are still unknown, ORs tuned to detect behaviorally relevant odorants, including pheromones and plant odorants, have been described.

In B. mori, two male antenna-specific OR genes, BmOR1 and BmOR3, have been identified as sex pheromone receptor genes. BmOR1 and BmOR3 are mutually exclusively expressed in pairs of pheromone receptor neurons in long s. trichodea, being fine-tuned to bombykol and bombykal, respectively (Sakurai et al. 2004; Nakagawa et al. 2005). These observations are consistent with physiological studies in which one of a pair of pheromone receptor neurons in long s. trichodea was activated by bombykol and the other responded to bombykal (Kaissling et al. 1978), and provide evidence that highly selective discrimination of pheromone components is accomplished by ligand selectivity of the ORs.

More recently, sex pheromone receptors in H. virescens (Große-Wilde et al. 2007), Plutella xylo-stella, Mythimna separata, and Diaphania indica (Mitsuno et al. 2008) have been functionally identified. Phylogenetic analyses of insect ORs indicate that these genes form a subfamily within the insect OR gene family, suggesting that sex pheromone receptors have evolved from a common ancestral OR gene (Mitsuno et al. 2008).

The function of ORs for general odorants has been less well studied compared to pheromone ORs and, currently, only three ORs (BmOR19, BmOR45, and BmOR47, in B. mori) have been characterized to be involved in the detection of plant odorants in moths (Anderson et al. 2009). These ORs are predominantly or exclusively expressed in the female antennae. BmOR19 responds to linalool, which has been reported to elicit characteristic wing futtering behavior in female moths (Priesner 1979), while the other two ORs respond most strongly to benzoic acid and moderately to several benzyl moiety-containing odorants. BmOR19 expressing ORNs are colocalized with BmOR45 and/or BmOR47 expressing ORNs within the same sensilla (Anderson et al. 2009). These sensilla are likely to be long s. trichodea, because two ORNs in long s. trichodea of female silk moths are known to respond to either linalool or benzoic acid (Heinbockel and Kaissling 1996).

3.3.4.3. Signal Transduction Following Odorant Reception

In ORNs, odorant signals are converted into electric activity by a chemoelectric transduction mechanism (Figure 3.3). Transduction was supposed to be mediated by a second messenger cascade triggered by the activation of a heterotrimeric G-protein by ORs with a bound ligand. In this model, odorant-evoked OR activation leads to a conformational change of a heterotrimeric G-protein comprising Gq α subunits. Thereafter, Gq induces phospholipase C (PLC) activation that results in the hydrolysis of phosphatidyl inositol 4,5-bisphosphate (PIP₂) into inositol (1,4,5)-trisphosphate (IP₃) and diacylglycerol (DAG). Subsequent opening of IP₃-gated Ca²⁺ channels induces Ca²⁺ influx, which, in turn, opens Ca²⁺-dependent cation channels to generate the receptor potential (Stengl 1994; Krieger and Breer 1999; Jacquin-Joly and Merlin 2004; Jacquin-Joly and Lucas 2005; Figure 3.3A).

FIGURE 3.3

Proposed signal transduction cascades following odorant reception. (A) A conventional model of olfactory transduction that involves a G-protein-mediated PLC-IP₃ pathway. (B) Alternative model in which the odorant receptor (OR) forms a heteromeric odorant-gated (more...)

Recently, this view was challenged by the finding that insect ORs either form a ligand (odorant)-gated nonselective cation channel with an atypical OR, named Or83b family protein (Sato et al. 2008; Figure 3.3B), or that insect ORs directly activate Or83b to function as a nonselective cation channel (Wicher et al. 2008; Figure 3.3C). In these models, the Or83b family protein plays a central role in signal transduction. Or83b was initially isolated from D. melanogaster as a member of the OR gene family (Vosshall et al. 2000), but it has the following two characteristic features that distinguish it from conventional ORs: (1) Or83b is expressed in almost all ORNs, while conventional ORs are expressed in restricted subsets of the ORN population. (2) Or83b family genes are highly conserved among different species including moths (Krieger et al. 2003; Jones et al. 2005), whereas conventional ORs show an extreme diversity in amino acid sequences. In fact, Or83b is not directly involved in odor detection, but supports translocation of coexpressed ORs to the dendritic membranes where it forms a heteromeric complex with ORs (Larsson et al. 2004; Neuhaus et al. 2004). Sato et al. coexpressed BmOR1 with BmOR2, a B. mori Or83b orthologue, and other combinations of members of the Or83b family with ORs in heterologous expression systems. Examination of the electrophysiological properties of an Or83b/OR complex revealed that it acts as an odorant-gated nonselective cation channel (Figure 3.3B) (Sato et al. 2008). Interestingly, there was no evidence for an elevation of second messenger levels upon stimulation with ligands appropriate for the expressed ORs, implying that there was no involvement of a G-protein-mediated cascade in the activation of Or83b/OR complexes. Wicher et al. (2008) found that fast transient and slow prolonged ionic currents occur in cultured cells coexpressing Or83b and D. melanogaster ORs upon stimulation with appropriate ligands. They proposed that the fast currents result from direct activation of Or83b by ORs, and that the slow currents result from G-protein-mediated activation of Or83b (Figure 3.3C). The atypical insect OR family Or83b represents the first identified 7-transmembrane ion channels so far. In this regard, insect ORs have a reversed topology relative to conventional GPCRs with their N-terminus on the cytoplasmic side and the C-terminus on the extracellular side (Benton et al. 2006).

3.4. MOTH BRAIN STRUCTURE

After detection by the peripheral processes, olfactory information is relayed to the central nervous system (CNS) to generate behavioral reactions. A short overview of the structure of moth brains is provided here as an introduction (Figure 3.4). Moth brains, as all insect brains, can be divided into four large regions: protocerebrum (PC), deutocerebrum (DC), tritocerebrum (TC), and subesophageal ganglion (SOG), which are fused in moths. The first three form the supraesophageal ganglion. The PC, which includes the optic lobes (OL), belongs to the ocular segment, whereas the DC and TC are associated with the antennal and labral ancestral segments, respectively. The SOG is composed of three neuromeres representing ancestral segments: mandibular, maxillary, and labial. From the SOG, the neck connective carries ascending and descending information from and to the ventral nerve cord. The overall structure of insect brains and the architecture of some areas important in olfaction have been reviewed in some detail previously (Bullock and Horridge 1965; Strausfeld 1976; Mobbs 1985; Homberg et al. 1989; Hansson and Anton 2000; Fahrbach 2006).

FIGURE 3.4

Anatomy of a moth (Manduca sexta) brain with emphasis on the olfactory neuropils. (A) View from dorsal (horizontal orientation with respect to body axis). (B) View from frontal (transversal orientation with respect to body axis). AL: antennal lobe; AMMC: (more...)

ORNs of the antenna project to the primary olfactory neuropil of the DC, the AL (see Section 3.5). In the AL, a segregation of pheromone and general odor information has been well documented in male moths, which possess a sex-specific macroglomerular complex (MGC) processing pheromone information (see Section 3.5.1). Odor information is relayed to the PC via AL projection neurons (PNs) that project to the mushroom body (MB) and the lateral protocerebrum (LPC), namely to the lateral horn (LH; see Section 3.6). The superior median PC (SMPC) is possibly involved in subsequent olfactory information processing (see Section 3.6.2). The lateral accessory lobe (LAL) represents the major output area of the brain, carrying olfactory signals to more posterior ganglia (see Section 3.6.2). The antennal system also contains mechanoreceptive and gustatory sensory cells, which project to the antennal mechanosensory and motor center (AMMC) and the SOG (Jørgensen et al. 2006). This deutocerebral area is additionally involved in the motor control of the antenna (Kloppenburg et al. 1997).

The optic ganglia receive visual inputs from the retinae of the compound eyes. This information is relayed through the lamina ganglionaris and the medulla, lobula (Lo), and Lo plate, mostly to the PC, but also to the AMMC as well as to the thoracic ganglia through descending PC neurons. The MBs of moths probably also receive visual information along with other modalities. Further visual and multimodal areas are the anterior optic tubercle (AOTu) and the central complex (CC). So far, these PC areas and the ocellar pathway have not been studied in great detail in moths. The TC and SOG have also received little attention in moths so far. The SOG contains at least circuitry related to the sensory and motor function of the mouth parts and the neck (Kvello et al. 2006; Mishima and Kanzaki 1998). There are olfactory projections from the labial pit organ, bearing CO₂-sensitive sensilla to the AL (Bogner et al. 1986; Kent et al. 1986). Whether projections in the TC and the SOG seen in these studies are olfactory remains to be investigated.

In moths, as in other insects, the major excitatory neurotransmitter in the CNS is acetylcholine, which is also the candidate neurotransmitter of ORNs (Homberg and Müller 1999). Glutamate is thought to function as a CNS neurotransmitter (Sinakevitch et al. 2008). In the brain, inhibition is conveyed by GABAergic neurons (Homberg et al. 1987; Iwano and Kanzaki 2005; Seki and Kanzaki 2008). Nitric oxide is also implicated in signaling (Nighorn et al. 1998; Seki et al. 2005). Furthermore, the biogenic amines, octopamine, tyramine, dopamine, serotonin, and histamine, as well as neuropeptides have been detected in moth brains (Homberg et al. 1987, 1990, 1991; Homberg and Hildebrand 1989, 1991; Iwano and Kanzaki 2005; Dacks et al. 2005; Sjöholm et al. 2006; Berg et al. 2007; Sinakevitch et al. 2008).

3.5. INFORMATION PROCESSING IN THE ANTENNAL LOBE

3.5.1. Glomeruli and Neuronal Components in the Moth Antennal Lobe

3.5.1.1. Glomerular Organization and Projections of Identified Olfactory Receptor Neurons (ORNs)

Olfactory information from the antennae is conveyed by the central projections of ORN axons to the AL, the main primary olfactory neuropil in the insect brain. The AL is composed of dense compartments of synaptic neuropil, termed glomeruli (Strausfeld 1976; Hildebrand and Shepherd 1997). Detailed morphological maps of the ALs are available for a number of moth species (Rospars and Chambille 1981; Rospars 1983; Rospars and Hildebrand 1992; Berg et al. 2002; Sadek et al. 2002; Greiner et al. 2004; Huetteroth et al. 2005; Masante-Roca et al. 2005; Skiri et al. 2005b; Kazawa et al. 2009). The AL of male moths is divided into two subregions: the MGC, which is an assembly of large glomeruli near the base of the AN, receiving the axons of pheromone-sensitive ORNs (Boeckh and Boeckh 1979; Matsumoto and Hildebrand 1981; Kanzaki and Shibuya 1986; Koontz and Schneider 1987), and the ordinary glomeruli, which are an array of small glomeruli present in both sexes, receiving input from the axons of ORNs tuned to general odors (Hansson 1995). The ordinary glomeruli also comprise glomeruli that process nonolfactory modalities (Guerenstein et al. 2004; Han et al. 2005).

Early imaging studies have revealed that odor stimulation elicits an activity pattern in a specific combination of glomeruli, supporting the concept that the individual glomerulus is the functional unit for olfactory processing (Rodrigues and Buchner 1984). This is in line with the fact that axonal branches of individual ORNs are restricted to single glomeruli. ORNs tuned to particular pheromone components project to particular subdivisions of the MGC, forming a topographic map of pheromone component information in the MGC (Hansson et al. 1992; Hansson 1995; Figure 3.5). The female AL contains two sexually dimorphic glomeruli, the large female glomeruli, in lieu of the MGC in M. sexta (Rössler et al. 1998) and H. virescens (Berg et al. 2002). The large female glomeruli are innervated by ORNs of short s. trichodea that respond to host-plant odors in M. sexta (Shields and Hildebrand 2001), but by ORNs tuned to the species-specific pheromone or linalool in H. virescens (Hillier et al. 2006).

FIGURE 3.5

Axonal projections of functionally identified pheromone receptor neurons in the male turnip moth, Agrotis segetum. (A) AL structure of male A. segetum. The MGC is situated at the entrance of the AL, and MGC subdivisions are indicated by A, B, and C. A (more...)

In addition to the ORN-glomerulus relationship, the innervation pattern of individual pheromone receptor neurons within the MGC can be correlated with the position of the corresponding sensilla on the antennae (Christensen et al. 1995; Ai and Kanzaki 2004). For example, ORNs from the medial and lateral sides of the antennae branched in medial and lateral regions, respectively, in the MGC of B. mori (Ai and Kanzaki 2004; see Section 3.5.2.3).

3.5.1.2. Neuron Types in the Antennal Lobe (AL)

Moth ALs contain two major types of neurons besides the axonal projections of ORNs. PNs are principal cells of the AL and transmit olfactory information from the AL to the PC (Figure 3.6). Homberg et al. (1988) have first systematically classified PNs in the AL of M. sexta. PNs were classified by morphological characteristics, such as the number of glomeruli that are innervated, the position of the soma, and the tracts in which their axons project (called the antenno-cerebral tracts, ACTs) and later, this classification scheme was applied to other moth species. Uniglomerular PNs have dendritic arborizations restricted to single glomeruli. The majority of the PNs in the moth AL are of the uniglomerular type. Multiglomerular PNs have dendritic ramifications in multiple glomeruli and are less well understood, although several studies have investigated this type of PN in moths (Kanzaki and Shibuya 1986; Homberg et al. 1988; Kanzaki et al. 1989; Rø et al. 2007).

FIGURE 3.6

Morphology and physiology of MGC-PNs of the silk moth. (A–C) Confocal images of PNs innervating cumulus (A), toroid (B), and both glomeruli (C). The axons of uniglomerular PNs run in the IACT and send blebby projections to the MBCa and the lateral (more...)

Local interneurons (LNs) are intrinsic cells of the AL and connect individual glomeruli, indicating that LNs have an important role in interglomerular interaction (Figure 3.7). Moth LNs described so far are all spiking neurons, most of them GABAergic, exerting inhibition on both PNs and other LNs identified by anatomical and electrophysiological methods (Waldrop et al. 1987; Christensen et al. 1993, 1998). The AL contains LN populations quite heterogeneous in dendritic morphology and immunohistochemical staining properties (Iwano and Kanzaki 2005; Seki and Kanzaki 2008). LNs are classified into several types according to their morphological characteristics (Figure 3.7), but their functional significance in moths remains to be investigated. In addition to PNs and LNs, moth ALs contain several types of extrinsic neurons (Kent et al. 1987; Homberg and Hildebrand 1989; Sun et al. 1993; Hill et al. 2002; Dacks et al. 2005, 2006; see also Section 3.5.5). They normally have several processes covering wide areas of the brain.

FIGURE 3.7

Various types of LNs in (A) male Agrotis segetum, (B) female Spodoptera littoralis, (C) female Manduca sexta, and (D) male Bombyx mori. ([A] From Hansson, B. S., Anton, S., and Christensen, T. A. J. Comp. Physiol. A, 175, 547–62, 1994. With permission. (more...)

3.5.3. General Odor Processing in the Ordinary Glomeruli

3.5.3.1. Combinatorial Olfactory Representation

The ordinary glomeruli are an assembly of ca. 60 glomeruli in the moth AL (Anton and Homberg 1999; Schachtner et al. 2005) and process information from ORNs tuned to general odorants. As in the MGC, PNs innervating the same glomeruli generally have similar olfactory response profiles (Reisenman et al. 2005; Namiki and Kanzaki 2008; D. melanogaster:Wilson et al. 2004; Bhandawat et al. 2007; but see Sadek et al. 2002). One major hypothesis is that odor identity is encoded by the combination of active glomeruli.

Odor stimulation evokes spatiotemporal activity patterns in the PN population (Figure 3.8). Optical imaging in vivo has been widely used in the investigation of the moth AL (Okada et al. 1996; Galizia et al. 2000; Carlsson et al. 2002, 2005; Hansson et al. 2003; Meijerink et al. 2003; Skiri et al. 2004; Figure 3.8A). Calcium imaging has revealed a detailed chemotopic representation in the AL (Hansson et al. 2003; Carlsson et al. 2005). While aromatics activated different subregions of the AL as compared to terpenes, compounds in the same class elicited similar activation patterns, a finding that has been confirmed by multiunit recording (Lei et al. 2004; Figure 3.8B). These studies also showed that the spatial representations of odors are dynamic. Using a different approach, the combination of a digital AL atlas and single-cell electrophysiological and anatomical identification, Namiki and Kanzaki (2008) reconstructed the odor-evoked spatiotemporal activity of a PN population in the silk moth (Figure 3.8C). Different odors were shown to elicit distinct spatiotemporal patterns.

FIGURE 3.8

Spatiotemporal organization of odor-evoked activity in the moth AL. (A) Olfaction activation pattern in the AL of Spodoptera littoralis revealed by calcium imaging. (B) Ensemble olfactory response in the AL of Manduca sexta revealed by tetrode recording. (more...)

3.5.3.2. Synchronized Activity

The AL may encode sensory information at multiple timescales. When one monitors the odor-evoked firing rate change in a low frequency band (~1–20 Hz), PNs show various temporal activation patterns (Christensen et al. 2000; Stopfer et al. 2003; Daly et al. 2004; Lei et al. 2004; Namiki and Kanzaki 2008; Figure 3.8). At higher frequencies (~20–50 Hz), odor-evoked responses in PNs exhibit synchronized activity (Laurent and Naraghi 1994; Heinbockel et al. 1998), which is thought to possess several computational roles such as improving olfactory discrimination and involvement in short-term memory in olfactory processing (Stopfer et al. 1997; Stopfer and Laurent 1999; Laurent 2002).

Christensen et al. (2000) have shown that a PN population can exhibit synchronized firing in response to odor stimulation. Using trains of brief stimulus pulses mimicking natural stimulus conditions, they have characterized several aspects of odor-evoked population activity in the moth AL (Christensen et al. 2003). First, odor presentation evokes a local field potential in the AL as well as in the MB, and these are not coherent. Second, the odor-evoked field potential is not globally coherent within the AL. Such spatial heterogeneity of synchronized activity has also been observed in the bumblebee AL (Okada et al. 2001).

3.5.5. Neuromodulation and Plasticity in the Antennal Lobe

Physiological experiments have shown that neural responses to pheromone and electrical stimuli in the moth AL are enhanced by serotonin (Kloppenburg and Hildebrand 1995; Kloppenburg et al. 1999; Hill et al. 2003; Figure 3.9). Serotonin also has effects on field potential oscillations (Kloppenburg and Heinbockel 2000) and is thus likely to affect olfactory information encoding. In PNs and possibly other AL neurons, the basis of such changes is the reduction of potassium currents upon exposure to serotonin application (Mercer et al. 1995; Kloppenburg et al. 1999). At AL circuit level, 5-hydroxytryptamine (5HT) increases sensitivity and improves ensemble discrimination of odors (Dacks et al. 2008). The ALs of B. mori and M. sexta contain a bilaterally symmetrical serotonergic neuron that innervates all glomeruli (Kent et al. 1987; Hill et al. 2002), mostly making output synapses (Sun et al. 1993). This neuron, similar to 5HT neurons with overall glomerular innervation patterns in other insects (Schürmann and Klemm 1984; Rehder et al. 1987; Breidbach 1990; Salecker and Distler 1990; Dacks et al. 2006), is the likely natural source for modulation by 5HT in the AL reflected in behaviorally determined sensitivity changes (see Section 3.2.3.2). It displays no odorant-specific response and shows slow, regular activity (Hill et al. 2002). It is a possible neural substrate for short-term and circadian modulation of olfactory sensitivity, but also for long-term structural changes (Kloppenburg and Mercer 2008). Juvenile hormone-dependent maturation of the AL also occurs at a longer timescale, increasing the sensitivity of AL neurons (Anton and Gadenne 1999). Interestingly, the age-dependent increase of sensitivity is specific to pheromone-responsive neurons (Greiner et al. 2002). At the timescale of ongoing olfactory processing, nitric oxide is involved in shaping AL responses (Wilson et al. 2007). While other neuroactive substances have been identified in the AL of M. sexta (Homberg and Müller 1999; Dacks et al. 2005), B. mori (Iwano and Kanzaki 2005), and H. virescens (Berg et al. 2007), their roles in the modulation of information fow through the AL have, so far, not been investigated. Octopamine possibly plays a similar role in learning as in the honeybee because a neuron similar to the bee’s putatively octo-paminergic VUMmx1 (Hammer 1993; Schröter et al. 2007) has been found in H. virescens (Rø et al. 2007).

FIGURE 3.9

Modulation of pheromone-induced responses in AL projection neurons of male Manduca sexta by 5HT. (A) Whole cell recording of an MGC projection neuron under current clamp (hyperpolarizing current injection). Responses to antennal pheromone stimulation (more...)

In AL neurons of male moths, different forms of central nonassociative plasticity have been demonstrated. Responses to pheromone are decreased for a brief period after mating, reflecting similar changes in behavior (Gadenne et al. 2001; see Section 3.2.3.3). On the other hand, brief pre-exposure to pheromone was shown to enhance sensitivity at behavioral and AL physiological level (Anderson et al. 2007). Pavlovian conditioning, the pairing of an odor with a gustatory reward stimulus, is also capable of altering information processing in the AL. Notably, the number of neurons responsive to the conditioned odor stimulus increases as a result of learning (Daly et al. 2004).

3.6. PROTOCEREBRAL OLFACTORY CIRCUITS

The outputs of the AL, the PNs, project to different PC targets. A wide target area of PNs is the LPC (Homberg et al. 1988; Kanzaki et al. 1989, 2003; Rø et al. 2007). Each PN has a single axon that innervates one of the ACTs. In M. sexta, five ACTs have been identified: the inner (IACT), outer (OACT), middle (MACT), dorsal (DACT), and dorso-median (DMACT) ACTs (Homberg et al. 1988; Kanzaki et al. 1989). Depending on the species, not all of these were found in other moths (Kanzaki et al. 2003; Rø et al. 2007). Some OACT projections have been found to the contralateral PC (Homberg et al. 1988; Wu et al. 1996).

Most PNs with axons in the IACT appear to have uniglomerular dendritic arborizations in the AL of moths (Christensen and Hildebrand 1987; Homberg et al. 1988; Kanzaki et al. 1989; Christensen et al. 1991; Anton and Homberg 1999; Rø et al. 2007; Anton and Hansson 1994, 1995), but some multiglomerular PNs running through the IACT exist (Hansson et al. 1991; Heinbockel et al. 2004). Uniglomerular PNs have also been found in the OACT and DMACTs (Anton and Homberg 1999; Homberg et al. 1988; Kanzaki et al. 2003). Putatively GABAergic PNs with multiglomerular dendritic arborizations and somata in the lateral cell cluster (LC) of the AL project in the MACT (Hoskins et al. 1986; Anton and Homberg 1999; Iwano and Kanzaki 2005). Some PNs of the LC projecting into the MACT are immunoreactive for FMRFamide (Iwano and Kanzaki 2005). In the silk moth, the somata of uniglomerular MGC PNs are located in the medial cell cluster (MC) and their axons innervate the IACT, whereas the somata of multiglomerular MGC PNs are located in the LC and their axons run through the MACT or OACT (Kanzaki et al. 2003).

The segregation of the pheromone and general odor systems is maintained in the LPC as PNs from the ordinary glomeruli project to the LH, while PNs from the MGC project to a separate area in the ILPC (Homberg et al. 1988; Kanzaki et al. 1989). In B. mori, MGC PNs specifically innervated a circumscribed pyramidally shaped projection area between the LH and the MB calyx (MBCa), called the delta area of the inferolateral protocerebrum (δILPC), in which the projections representing the blend components occupy partially overlapping regions (Seki et al. 2005; Figure 3.10). PNs also project to the MBCa, where projections cover a substantial area of the calyx with wide axonal arbors. Projections from the MGC toroid subdivision, responsive to the major pheromone blend component, only project to a restricted area of the MBCa (Kanzaki et al. 2003; Seki et al. 2005). The segregation of general odor and pheromone systems may be a general feature in insects (Jefferis et al. 2007).

FIGURE 3.10

Innervation of MGC PNs in the LPC. (A) Anti-cGMP immunostaining in the LPC, showing axonal projections of PNs that define the δILPC. (B) Three-dimensional reconstruction of the data shown in (A) with the ACTs. (C) Anti-cGMP immunostaining in the (more...)

The nature of information processing by PC neurons remains largely obscure. One particular problem is the fact that besides some easily recognizable structures, a sizable portion of the PC lacks clear compartments. High blend specificity and sophisticated multimodal response properties have been found in PC neurons (Kanzaki et al. 1991a, 1991b; Light 1986). However, complex response properties, in particular blend-specific responses, may be less common than expected and temporal resolution rather declines compared to AL PN neurons (Lei et al. 2001). Systematic work has so far only been done in two protocerebral areas, the MB and the LAL.

3.6.2. Lateral Accessory Lobe

Based on the fact that descending neurons (DNs) show pheromone responses, the LAL of the PC and adjacent areas of the ventral protocerebrum (VPC) could be identified as important olfactory neuropils in which the output of the brain in response to olfactory stimuli is generated (Olberg 1983; Kanzaki et al. 1994). In several insect species, DN responses to stimuli of different modalities and their role in the control of various behaviors have been investigated (see Okada et al. 2003). DNs in moths have so far chiefly been investigated with pheromone and visual stimuli, since these are important for odor source localization behaviors.

DNs showing phasic excitation, phasic inhibition, or long-lasting excitatory or inhibitory aftereffects following pheromone stimulation have been found in M. sexta and B. mori (Kanzaki and Shibuya 1986; Kanzaki et al. 1991b; Mishima and Kanzaki 1999; Wada and Kanzaki 2005). While M. sexta DNs without projections in the LAL showed only phasic pheromone responses, state-dependent activity and tonic modulation by light intensity was observed in pheromonesensitive LAL DNs (Kanzaki et al. 1991b). DNs with state-dependent activity found in B. mori, show conspicuous fipfop activity, switching between low and high firing rates upon subsequent pheromone stimuli, reminiscent of a toggle flipfop circuit (Figure 3.11; Olberg 1983; Kanzaki et al. 1994; Mishima and Kanzaki 1999; Wada and Kanzaki 2005). There are two classes of flipfop DNs on each side of the neck connective, firing in antiphase relative to the same class on the contralateral side and to the other class on the ipsilateral side (Kanzaki et al. 1994; Kanzaki and Mishima 1996). The flipfop DNs belong to two soma clusters containing pheromone-sensitive DNs (Kanzaki et al. 1994; Mishima and Kanzaki 1999; Wada and Kanzaki 2005), one located near the anterior border between DC and PC (Group I, three neurons with bilateral projections, one capable of flipfop responses) and another located anterodorsally just medial of the AL (Group II, 10–15 unilaterally confined cells of three morphological types, two of which can show flipfop responses). DNs are often multimodal. In Lymantria dispar DNs, synergistic effects between responses to moving patterns and pheromone, as well as responses only occurring in combined stimulation, were shown (Olberg and Willis 1990). Such responses are possible substrates of optomotor responses involved in upwind fight. In B. mori, flipfopping could be induced by light intensity changes or modulated by absolute light intensity as well as pheromone concentration, and some flipfop DNs also responded with graded responses to mechanical and moving visual stimuli (Olberg 1983; Kanzaki et al. 1994). One target of at least some flipfop DNs are motor neurons of the SOG controlling head movements that are correlated with turns in locomotion (Kanzaki and Mishima 1996; Mishima and Kanzaki 1998, 1999; Wada and Kanzaki 2005). The flipfop DNs have been implicated to represent command neurons controlling walking direction, thus being the neural substrates of zigzag walking, the main element of pheromone orientation behavior in B. mori.

FIGURE 3.11

Flipflopping descending neurons in the silk moth brain. (A) Distribution of DN somata in the brain of Bombyx mori labeled by backfilling through the neck connective. (B) Physiological responses to bombykol pulses (lower trace) and morphology of a Group-I (more...)

Besides DNs, the LAL/VPC region also contains LNs that are unilaterally confined and bilateral neurons (BNs), identified both in B. mori and M. sexta (Figure 3.12; Kanzaki et al. 1991a; Kanzaki and Shibuya 1992; Mori et al. 1999; Iwano et al. 2009). These neurons showed transient excitation or excitatory after-effects to ipsilateral pheromone stimulation and multimodal properties. The BNs, in particular, are thought to be important in the generation of fipfop activity by providing contralateral inhibition (Kanzaki et al. 1994) and some of them have been shown to be GABA-immunoreactive (Iwano et al. 2009).

FIGURE 3.12

Morphology of LAL interneurons in the silk moth brain. (A) Morphology of a LAL bilateral interneuron. The neuron has smooth processes in the ipsilateral LAL and varicose process in the contralateral LAL, and responds to bombykol with lasting excitatory (more...)

A third, broadly defined class, are mostly unilateral interneurons linking the LAL and adjacent VPC neuropil with other protocerebral areas. A few neurons that establish direct connections between δILPC and LAL have been identified in M. sexta and A. segetum (Kanzaki et al. 1991a; Lei et al. 2001). Preliminary results from our laboratory taken together with the results of Lei et al. (2001) imply that pheromone information is largely relayed though an area in the superior median protocerebrum (SPMC). Other interneurons connect the LAL with the MB and show features similar to MB extrinsic cells in other insects, including after-effects (Kanzaki et al. 1991a).

3.7. OUTLOOK

Research in moth olfaction has come a long way since the isolation of the first sex pheromone (Butenandt et al. 1959) and the discovery of the electroantennogram (EAG; Schneider 1957), still the most widely used technique to assess ORN responses in insects. EAGs are now being used to create highly specific sensors for odorants (Park et al. 2002), and the fact that insect odorant receptors are capable of direct transduction into electrical signals (see Section 3.3.4.3) has great potential for use as odorant sensors in measurement apparatus. Learning in moths and other insects is employed to use insects for locating odor sources of interest at various spatial scales (Rains et al. 2008). Pheromone research and host-plant-induced behaviors remain highly active fields in moth olfaction not least because of the economic importance of a number of moth species as agricultural pests in still widely used large-scale monocultures. However, pheromone-induced responses are also a tool in basic research with applications in engineering, for instance in autonomous systems, because they are one of the most accessible approaches to study mechanisms of reliable, robust odor source localization, while allowing precise control over perturbations due to the high specificity of pheromone-induced behavioral programs. The first implementations have started to appear in the area of odor source localization as hybrid robots, coupling biological information processing to artificial effectors (Emoto et al. 2007; Kanzaki et al. 2008).

In this field, the elucidation of protocerebral mechanisms generating the steering control outputs relayed by DNs is currently a major challenge. The relatively small size of moth brains and a large body of identified neuron data are now being used to attempt rebuilding behaviorally relevant circuits of the moth brain by means of realistic biophysical simulations. Genetic manipulations have become feasible and the silk moth (B. mori) in particular, being fightless and showing locomotion only in response to stimulation, is a very convenient and safe system in which the full array of these techniques may be applied (Yamagata et al. 2008).

The general odor detection system of moths also holds promises for the future. It will be a valuable tool in understanding odorant information encoding in the CNS, especially in conjunction with learning paradigms that have recently been developed, allowing direct evaluation of neural activity through behavioral performance. Outside the more reductionist laboratory setting, research in moth olfaction is increasingly linking field conditions with their multimodal stimulus conditions to behavior and neurobiology, leading to a better understanding of how mechanisms evolved as adaptations to environmental constraints.

ACKNOWLEDGMENTS

We would like to thank Sylvia Anton, Uwe Homberg, Sid Simon, and our colleagues in the laboratory, in particular, Douglas Bakkum and Ryota Fukushima, for their help in improving the manuscript.

ABBREVIATIONS

5HT:

5-hydroxytryptamine (serotonin)

A:

anterior

ABPX:

antennal binding protein X

ACT:

antenno-cerebral tract

AL:

antennal lobe

AMMC:

antennal mechanosensory and motor center

AN:

antennal nerve

AOTu:

anterior optic tubercle

BN:

PC bilateral neuron

CC:

central complex

AILPC:

delta area of the inferolateral protocerebrum

D:

dorsal

DACT:

dorsal antenno-cerebral tract

DC:

deutocerebrum

DMACT:

dorso-median antenno-cerebral tract

DN:

descending neuron

EAG:

electroantennogram

FF:

flipflop neuron

GABA:

γ-aminobutyric acid

GOBP:

general odorant-binding protein

GPCR:

G-protein-coupled receptor

IACT:

inner antenno-cerebral tract

IP₃:

inositol-(1,4,5) trisphosphate

KC:

Kenyon cell

L:

lateral

LAL:

lateral accessory lobe

LbN:

labial nerves

LC:

lateral cell cluster of the AL

LH:

lateral horn

LN:

AL local interneuron

Lo:

lobula

lobl:

MB lobelet

LPC:

lateral protocerebrum

M:

medial

MACT:

middle antenno-cerebral tract

MB:

mushroom body

MBCa:

MB calyx

MBL:

MB lobes

MBPe:

MB pedunculus

MBYT:

MB Y-tract

MC:

medial cell cluster of the AL

MGC:

macroglomerular complex

mL:

MB medial lobe

OACT:

outer antenno-cerebral tract

OBP:

odorant-binding protein

ODE:

odorant degrading enzyme

Oe:

esophagus (esophageal foramen)

OL:

optic lobe

OR:

olfactory receptor (protein)

ORN:

olfactory receptor neuron

P:

posterior

PBP:

pheromone-binding protein

PC:

protocerebrum

PDE:

pheromone degrading enzyme

PER:

proboscis extension response

PIP₂:

phosphatidyl inositol 4,5-bisphosphate

PN:

AL projection neuron

s.:

sensillum/sensilla

SMPC:

superior median protocerebrum

SOG:

subesophageal ganglion

TC:

tritocerebrum

V:

ventral

vL:

MB vertical lobe

VPC:

ventral protocerebrum

REFERENCES

• Adam G., Delbrück M. Reduction of dimensionality in biological diffusion processes. In: Rich A., Davidson N., editors. Structural Chemistry and Molecular Biology. San Francisco, CA: WH Freeman; 1968. pp. 198–215.
• Ai H., Kanzaki R. Modular organization of the silk moth antennal lobe macroglomerular complex revealed by voltage-sensitive dye imaging. J. Exp. Biol. 2004;207:633–44. [PubMed: 14718506]
• Akhtar Y., Isman M.B. Larval exposure to oviposition deterrents alters subsequent oviposition behavior in generalist, Trichoplusia ni, and specialist, Plutella xylostella, moths. J. Chem. Ecol. 2003;29:1853–70. [PubMed: 12956511]
• Altner H., Prillinger L. Ultrastructure of invertebrate chemo-, thermo-, and hygroreceptors and its functional significance. Int. Rev. Cytol. 1980;67:69–139.
• Anderson A.R., Wanner K.W., Trowell S.C. et al. Molecular basis of female-specific odorant responses in Bombyx mori. Insect Biochem. Molec. Biol. 2009 doi: 10.1016/j.ibmb 2008.11.002. [PubMed: 19100833]
• Anderson P., Hilker M., Hansson B.S. et al. Oviposition deterring components in larval frass of Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae): A behavioral and electrophysiological evaluation. J. Insect Physiol. 1993;39:129–37.
• Anderson P., Hansson B.S., Nilsson U. et al. Increased behavioral and neuronal sensitivity to sex pheromone after brief odor experience in a moth. Chem. Senses. 2007;32:483–91. [PubMed: 17510089]
• Anderson P., Zadek M.M., Hansson B.S. Pre-exposure modulates attraction to sex pheromone in a moth. Chem. Senses. 2003;28:285–91. [PubMed: 12771015]
• Anton S., Gadenne C. Proc. Natl. Acad. Sci. USA. Vol. 96. 1999. Effect of juvenile hormone on the central nervous processing of sex pheromone in an insect; pp. 5764–67. [PMC free article: PMC21934] [PubMed: 10318958]
• Anton S., Hansson B.S. Central processing of sex pheromone, host odor, and oviposition deterrent information by interneurons in the antennal lobe of female Spodoptera littoralis (Lepidoptera: Noctuidae). J. Comp. Neurol. 1994;350:199–214. [PubMed: 7884038]
• Anton S., Hansson B.S. Sex pheromone and plant-associated odor processing in antennal lobe interneurons of male Spodoptera littoralis (Lepidoptera: Noctuidae). J. Comp. Physiol. A. 1995;176:773–89.
• Anton S., Hansson B.S. Physiological mismatching between neurons innervating olfactory glomeruli in a moth. Proc. R. Soc. B. 1999;266:1813–20.
• Anton S., Homberg U. Antennal lobe structure. In: Hansson B.S., editor. Insect Olfaction. Berlin: Springer; 1999. pp. 97–124.
• Arbas E.A. Neuroethological study of pheromone-modulated responses. In: Cardé R.T., Minks A.K., editors. Insect Pheromone Research: New Directions. New York: Chapman & Hall; 1997. pp. 320–29.
• Balkenius A., Rosén W.Q., Kelber A. The relative importance of olfaction and vision in a diurnal and a nocturnal hawkmoth. J. Comp. Physiol. A. 2006;192:431–37. [PubMed: 16380841]
• Baker T.C. Pheromone-modulated movements of flying moths. In: Payne T.L., Birch M.C., Kennedy D.E.J., editors. Mechanisms in Insect Olfaction. Oxford: Oxford University Press; 1986. pp. 39–48.
• Baker T.C. Upwind flight and casting flight: Complimentary phasic and tonic systems used for location of sex pheromone sources by male moths. In: Døving K.B., editor. Proceedings of the Tenth International Symposium on Olfaction and Taste. Oslo: GCS A/S; 1990. pp. 18–25.
• Baker T.C., Cossé A.A., Todd J.L. Behavioral antagonism in the moth Helicoverpa zea in response to pheromone blends of three sympatric heliothine moth species is explained by one type of antennal neuron. Ann. N. Y. Acad. Sci. 1998;855:511–13. [PubMed: 10049230]
• Baker T.C., Kuehnen L.P.S. Pheromone source location by flying moths: A supplementary nondemocratic mechanism. Science. 1982;216:424–27. [PubMed: 17745868]
• Baker T.C., Vickers N.J. Pheromone-mediated flight in moths. In: Cardé R.T., Minks A.K., editors. Insect Pheromone Research: New Directions. New York: Chapman & Hall; 1997. pp. 238–64.
• Baker T.C., Willis M.A., Haynes K.F., Phelan P.L. A pulsed cloud of sex pheromone elicits upwind flight in male moths. Physiol. Entomol. 1985;10:257–65.
• Baker T.C., Willis M.A., Phelan P.L. Optomotor anemotaxis polarizes self-steered zigzagging in flying moths. Physiol. Entomol. 1984;9:257–65.
• Bartell R.J., Roelofs W.L. Inhibition of sexual response in males of the moth Argyroteania velutinana by brief exposures to synthetic pheromone or its geometrical isomer. J. Insect Physiol. 1973;19:655–61.
• Bau J., Justus K.A., Cardé R.T. Antennal resolution of pulsed pheromone plumes in three moth species. J. Insect Physiol. 2002;48:433–42. [PubMed: 12770092]
• Bau J., Justus K.A., Loudon C., Cardé R.T. Electroantennographic resolution of pulsed pheromone plumes in two species of moths with bipectinate antennae. Chem. Senses. 2005;30:771–80. [PubMed: 16267163]
• Benton R., Sachse S., Michnick S.W., Vosshall L.B. Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol. 2006;4(2):e20. [PMC free article: PMC1334387] [PubMed: 16402857]
• Berg B.G., Galizia C.G., Brandt R., Mustaparta H. Digital atlases of the antennal lobe in two species of tobacco budworm moths, the Oriental Helicoverpa assulta (male) and the American Heliothis virescens (male and female). J. Comp. Neurol. 2002;446:123–34. [PubMed: 11932931]
• Berg B.G., Schachtner J., Utz S., Homberg U. Distribution of neuropeptides in the primary olfactory center of the heliothine moth Heliothis virescens. Cell Tissue Res. 2007;327:385–98. [PubMed: 17013588]
• Bhandawat V., Olsen S.R., Gouwens N.W., Schlief M.L., Wilson R.I. Sensory processing in the Drosophila antennal lobe increases reliability and separability of ensemble odor representations. Nat. Neurosci. 2007;10:1474–82. [PMC free article: PMC2838615] [PubMed: 17922008]
• Boeckh J., Boeckh V. Threshold and odor specificity of pheromone-sensitive neurons in the deutocerebrum of Antheraea pernyi and A. polyphemus (Saturniidae). J. Comp. Physiol. A. 1979;132:235–42.
• Bogner F., Boppré M., Ernst K.-D., Boeckh J. CO2 sensitive receptors on labial palps of Rhodogastria moths (Lepidoptera: Arctiidae): Physiology, fine structure and central projection. J. Comp. Physiol. A. 1986;158:741–49. [PubMed: 3090241]
• Breidbach O. Serotonin-immunoreactive brain interneurons persist during metamorphosis of an insect, a developmental study of Tenebrio molitor, L. (Coleoptera). Cell Tissue Res. 1990;259:345–60.
• Bullock T.H., Horridge G.A. Structure and Function in the Nervous System of Invertebrates. Vol. 2. San Francisco, CA: Freeman; 1965.
• Butenandt A., Beckermann R., Stamm D., Hecker E. Über den Sexuallockstoff des Seidenspinners Bombyx mori. Reindarstellung und Konstitution. Z. Naturforsch. 1959;14b:283–84.
• Cardé R.T., Comeau A., Baker T.C., Roelofs W.L. Moth mating periodicity: Temperature regulates the circadian gate. Experientia. 1975;31:46–48. [PubMed: 1112321]
• Cardé R.T., Hagaman T.E. Behavioral responses of the gypsy moth in a wind tunnel to airborne enantiomers of disparlure. Environ. Entomol. 1979;8:475–84.
• Cardé R.T., Mafra-Neto A. Mechanisms of flight of male moths to pheromone. In: Cardé R.T., Minks A.K., editors. Insect Pheromone Research: New Directions. New York: Chapman & Hall; 1997. pp. 275–90.
• Cardé R.T., Willis M.A. Navigational strategies used by insects to find distant, wind-borne sources of odor. J. Chem. Ecol. 2008;34:854–66. [PubMed: 18581182]
• Carlsson M.A., Galizia C.G., Hansson B.S. Spatial representation of odors in the antennal lobe of the moth Spodoptera littoralis (Lepidoptera: Noctuidae). Chem. Senses. 2002;27:231–44. [PubMed: 11923186]
• Carlsson M.A., Knüsel P., Verschure P.F.M.J., Hansson B.S. Spatio-temporal Ca2 + dynamics of moth olfactory projection neurones. Eur. J. Neurosci. 2005;22:647–57. [PubMed: 16101746]
• Charlton R.E., Cardé R.T. Factors mediating copulatory behavior and close-range mate recognition in the male gypsy moth, Lymantria dispar (L.). Can. J. Zool. 1989;68:1995–2004.
• Christensen T.A., D’Alessandro G., Lega J., Hildebrand J.G. Morphometric modeling of olfactory circuits in the insect antennal lobe: I. Simulations of spiking local interneurons. Biosystems. 2001;61:143–53. [PMC free article: PMC2773206] [PubMed: 11716974]
• Christensen T.A., Harrow I.D., Cuzzocrea C., Randolph P.W., Hildebrand J.G. Distinct projections of two populations of olfactory receptor axons in the antennal lobe of the sphinx moth Manduca sexta. Chem. Senses. 1995a;20:313–23. [PubMed: 7552040]
• Christensen T.A., Hildebrand J.G. Coincident stimulation with pheromone components improves temporal pattern resolution in central olfactory neurons. J. Neurophysiol. 1997;77:775–81. [PubMed: 9065849]
• Christensen T.A., Hildebrand J.G. Male-specific, sex pheromone-selective projection neurons in the antennal lobes of the moth Manduca sexta. J. Comp. Physiol. A. 1987;160:553–69. [PubMed: 3612589]
• Christensen T.A., Lei H., Hildebrand J.G. Coordination of central odor representations through transient, non-oscillatory synchronization of glomerular output neurons. Proc. Natl. Acad. Sci. USA. 2003;100:11076–81. [PMC free article: PMC196929] [PubMed: 12960372]
• Christensen T.A., Mustaparta H., Hildebrand J.G. Chemical communication in heliothine moths II. Central processing of intraand interspecific olfactory messages in the male corn earworm moth Helicoverpa zea. J. Comp. Physiol. A. 1991;169:259–74.
• Christensen T.A., Mustaparta H., Hildebrand J.G. Chemical communication in heliothine moths VI. Parallel pathways for information processing in the macroglomerular complex of the male tobacco budworm moth Heliothis virescens. J. Comp. Physiol. A. 1995b;177:545–57.
• Christensen T.A., Pawlowski V.M., Lei H., Hildebrand J.G. Multi-unit recordings reveal context-dependent modulation of synchrony in odor-specific neural ensembles. Nat. Neurosci. 2000;3:927–31. [PubMed: 10966624]
• Christensen T.A., Waldrop B.R., Harrow I.D., Hildebrand J.G. Local interneurons and information processing in the olfactory glomeruli of the moth Manduca sexta. J. Comp. Physiol. A. 1993;173:385–99. [PubMed: 8254565]
• Christensen T.A., Waldrop B.R., Hildebrand J.G. Multitasking on the olfactory system: Context-dependent in single olfactory projection neurons. J. Neurosci. 1998;18:5999–6008. [PMC free article: PMC6793051] [PubMed: 9671685]
• Clyne P.J., Warr C.G., Freeman M.R. et al. A novel family of divergent seven-transmembrane proteins: Candidate odorant receptors in Drosophila. Neuron. 1999;22:327–38. [PubMed: 10069338]
• Coracini M., Bengtsson M., Cichon L., Witzgall P. Codling moth males do not discriminate between pheromone and a pheromone/antagonist blend during upwind flight. Naturwissenschaften. 2003;90:419–23. [PubMed: 14504786]
• Couto A., Alenius M., Dickson B.J. Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr. Biol. 2005;15:1535–47. [PubMed: 16139208]
• Cunningham J.P., Moore C.J., Zalucki M.P., West S.A. Learning, odor preference and flower foraging in moths. J. Exp. Biol. 2004;207:87–94. [PubMed: 14638836]
• Dacks A.M., Christensen T.A., Agricola H.-J., Wollweber L., Hildebrand J.G. Octopamineimmunoreactive neurons in the brain and subesophageal ganglion of the hawkmoth Manduca sexta. J. Comp. Neurol. 2005;488:255–68. [PMC free article: PMC1363738] [PubMed: 15952164]
• Dacks A.M., Christensen T.A., Hildebrand J.G. Phylogeny of a serotonin-immunoreactive neuron in the primary olfactory center of the insect brain. J. Comp. Neurol. 2006;498:727–46. [PubMed: 16927264]
• Dacks A.M., Christensen T.A., Hildebrand J.G. Modulation of olfactory information processing in the antennal lobe of Manduca sexta by serotonin. J. Neurophysiol. 2008;99:2077–85. [PubMed: 18322001]
• Daly K.C., Carrell L.A., Mwilaria E. Characterizing psychophysical measures of discrimination thresholds and the effects of concentration on discrimination learning in the moth Manduca sexta. Chem. Senses. 2008;33:95–106. [PubMed: 17928636]
• Daly K.C., Chandra S., Durtschi M.L., Smith B.H. The generalization of an olfactory-based conditioned response reveals unique but overlapping odor representations in the moth Manduca sexta. J. Exp. Biol. 2001a;204:3085–95. [PubMed: 11551996]
• Daly K.C., Christensen T.A., Lei H., Smith B.H., Hildebrand J.G. Learning modulates the ensemble representations for odors in primary olfactory networks. Proc. Natl. Acad. Sci. USA. 2004a;101:10476–81. [PMC free article: PMC478594] [PubMed: 15232007]
• Daly K.C., Durtschi M.L., Smith B.H. Olfactory-based discrimination learning in the moth, Manduca sexta. J. Insect Physiol. 2001b;47:375–84. [PubMed: 11166302]
• Daly K.C., Smith B.H. Associative learning in the moth Manduca sexta. J. Exp. Biol. 2000;203:2025–38. [PubMed: 10851119]
• Daly K.C., Wright G.A., Smith B.H. Molecular features of odorants systematically influence slow temporal responses across clusters of coordinated antennal lobe units in the moth Manduca sexta. J. Neurophysiol. 2004b;92:236–54. [PubMed: 14985411]
• de Bruyne M., Baker T.C. Odor detection in insects: Volatile codes. J. Chem. Ecol. 2008;34:882–97. [PubMed: 18535862]
• de Bruyne M., Clyne P.J., Carlson J.R. Odor coding in a model olfactory organ: Drosophila maxillary palp. J. Neurosci. 1999;19:4520–32. [PMC free article: PMC6782632] [PubMed: 10341252]
• Den Otter C.J., Schuil H.A., Sander-van Oosten A. Reception of host-plant odors and female sex pheromone in Adoxophyes orana (Lepidoptera: Tortricidae): Electrophysiology and morphology. Ent. Exp. Appl. 1978;24:370–78.
• Dolzer J., Krannich S., Fischer K., Stengl M. Oscillations of the transepithelial potential of moth olfactory sensilla are influenced by octopamine and serotonin. J. Exp. Biol. 2001;204:2781–94. [PubMed: 11683434]
• Emoto S., Ando N., Takahashi K., Kanzaki R. Insect-controlled robot – evaluation of adaptability. J. Robotics Mechatron. 2007;19:436–43.
• Fahrbach S.E. Structure of the mushroom bodies of the insect brain. Annu. Rev. Entomol. 2006;51:209–32. [PubMed: 16332210]
• Fan R.-J., Anderson P., Hansson B.S. Behavioral analysis of olfactory conditioning in the moth Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae). J. Exp. Biol. 1997;200:2969–76. [PubMed: 9359884]
• Fan R.-J., Hansson B.S. Olfactory discrimination conditioning in the moth Spodoptera littoralis. Physiol. Behav. 2001;72:159–65. [PubMed: 11239993]
• Farris S.M. Evolution of insect mushroom bodies: Old clues, new insights. Arthropod Struct. Dev. 2005;34:211–34.
• Flecke C., Dolzer J., Krannich S., Stengl M. Perfusion with cGMP analogue adapts the action potential response of pheromone-sensitive sensilla trichodea of the hawkmoth Manduca sexta in a daytime-dependent manner. J. Exp. Biol. 2006;209:3898–3912. [PubMed: 16985206]
• Firestein S. How the olfactory system makes sense of scents. Nature. 2001;413:211–18. [PubMed: 11557990]
• Fishilevich E., Vosshall L.B. Genetic and functional subdivision of the Drosophila antennal lobe. Curr. Biol. 2005;15:1548–53. [PubMed: 16139209]
• Fukushima R., Kanzaki R. Modular subdivision of mushroom bodies by Kenyon cells in the silk moth. J Comp. Neurol. 2009;513:315–330. [PubMed: 19148932]
• Gadenne C., Dufour M.-C., Anton S. Transient post-mating inhibition of behavioral and central nervous responses to sex pheromone in an insect. Proc. Biol. Sci. 2001;268:1631–35. [PMC free article: PMC1088787] [PubMed: 11487411]
• Galizia C.G., Sachse S., Mustaparta H. Calcium responses to pheromones and plant odors in the antennal lobe of the male and female moth Heliothis virescens. J. Comp. Physiol. A. 2000;186:1049–63. [PubMed: 11195281]
• Gao Q., Yuan B., Chess A. Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe. Nat. Neurosci. 2000;3:780–85. [PubMed: 10903570]
• Gatellier L., Nakao T., Kanzaki R. Serotonin modifies the sensitivity of the male silk moth to pheromone. J. Exp. Biol. 2004;207:2487–96. [PubMed: 15184520]
• Getchell T.V., Margolis J.L., Getchell M.L. Perireceptor and receptor events in vertebrate olfaction. Prog. Neurobiol. 1984;23:317–45. [PubMed: 6398455]
• Goyret J., Markwell P.M., Raguso R.A. The effect of decoupling olfactory and visual stimuli on the foraging behavior of Manduca sexta. J. Exp. Biol. 2007;210:1398–1405. [PubMed: 17401122]
• Greiner B., Gadenne C., Anton S. Central processing of plant volatiles in Agrotis ipsilon males is age-independent in contrast to sex pheromone processing. Chem. Senses. 2002;27:45–48. [PubMed: 11751467]
• Greiner B., Gadenne C., Anton S. Three-dimensional antennal lobe atlas of the male moth, Agrotis ipsilon: A tool to study structure-function correlation. J. Comp. Neurol. 2004;475:202–10. [PubMed: 15211461]
• Große-Wilde E., Gohl T., Bouché E., Breer H., Krieger J. Candidate pheromone receptors provide the basis for the response of distinct antennal neurons to pheromonal compounds. Eur. J. Neurosci. 2007;25:2364–73. [PubMed: 17445234]
• Große-Wilde E., Svatos A., Krieger J. A pheromone binding protein mediates the bombykol-induced activation of a pheromone receptor in vitro. Chem. Senses. 2006;31:547–55. [PubMed: 16679489]
• Grosmaitre X., Marion-Poll F., Renou M. Biogenic amines modulate olfactory receptor neurons firing activity in Mamestra brassicae. Chem. Senses. 2001;26:653–61. [PubMed: 11473931]
• Guerenstein P.G., Christensen T.A., Hildebrand J.G. Sensory processing of ambient CO2 information in the brain of the moth Manduca sexta. J. Comp. Physiol. A. 2004;190:707–25. [PubMed: 15235811]
• Hammer M. An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature. 1993;366:59–63. [PubMed: 24308080]
• Han Q., Hansson B., Anton S. Interactions of mechanical stimuli and sex pheromone information in antennal lobe neurons of a male moth, Spodoptera littoralis. J. Comp. Physiol. A. 2005;191:521–28. [PubMed: 15856257]
• Hansson B.S. Antennal lobe projection patterns of pheromone-specific olfactory receptor neurons in moths. In: Cardé R.T., Minks A.K., editors. Insect Pheromone Research: New Directions. New York: Chapman & Hall; 1997. pp. 164–83.
• Hansson B.S., Anton S. Function and morphology of the antennal lobe: New developments. Annu. Rev. Entomol. 2000;45:203–31. [PubMed: 10761576]
• Hansson B.S., Anton S., Christensen T.A. Structure and function of antennal lobe neurons in the male turnip moth, Agrotis segetum (Lepidoptera, Noctuidae). J. Comp. Physiol. A. 1994;175:547–62.
• Hansson B.S., Carlsson M.A., Kalinovà B. Olfactory activation patterns in the antennal lobe of the sphinx moth, Manduca sexta. J. Comp. Physiol. A. 2003;189:301–8. [PubMed: 12743734]
• Hansson B.S., Christensen T.A., Hildebrand J.G. Functionally distinct subdivisions of the macroglomerular complex in the antennal lobe of the male sphinx moth Manduca sexta. J. Comp. Neurol. 1991;312:264–78. [PubMed: 1748732]
• Hansson B.S., Ljungberg H., Hallberg E., Lofstedt C. Functional specialization of olfactory glomeruli in a moth. Science. 1992;256:1313–15. [PubMed: 1598574]
• Hansson B.S., Van der Pers J.N.C., Löfqvist J. Comparison of male and female olfactory cell response to pheromone compounds and plant volatiles in the turnip moth, Agrotis segetum. Physiol. Entomol. 1989;14:147–55.
• Hartlieb E. Olfactory conditioning in the moth Heliothis virescens. Naturwissenschaften. 1996;83:87–88.
• Hartlieb E., Anderson P. Olfactory-released behaviors. In: Hansson B.S., editor. Insect Olfaction. Berlin: Springer; 1999. pp. 315–49.
• Hartlieb E., Anderson P., Hansson B.S. Appetitive learning of odors with different behavioral meaning in moths. Physiol. Behav. 1999;67:671–77. [PubMed: 10604836]
• Haynes K.F., Zhao J.Z., Latif A. Identification of floral compounds from Abelia grandiflora that stimulate upwind flight in cabbage looper moths. J.Chem. Ecol. 1991;17:637–46. [PubMed: 24258812]
• Heath R.R., Manukian A. Development and evaluation of systems to collect volatile semiochemicals from insects and plants using a charcoal-infused medium for air purification. J. Chem. Ecol. 1992;18:1209–26. [PubMed: 24254160]
• Heinbockel T., Christensen T.A., Hildebrand J.G. Temporal tuning of odor responses in pheromone-responsive projection neurons in the brain of the sphinx moth Manduca sexta. J. Comp. Neurol. 1999;409:1–12. [PubMed: 10363707]
• Heinbockel T., Christensen T.A., Hildebrand J.G. Representation of binary pheromone blends by glomerulus-specific olfactory projection neurons. J. Comp. Physiol. A. 2004;190:1023–37. [PubMed: 15378331]
• Heinbockel T., Hildebrand J.G. Antennal receptive fields of pheromone-responsive projection neurons in the antennal lobes of the male sphinx moth Manduca sexta. J. Comp. Physiol. A. 1998;183:121–33. [PubMed: 9693989]
• Heinbockel T., Kaissling K.-E. Variability of olfactory receptor neuron responses of female silkworms (Bombyx mori L.) to benzoic acid and (±)-linalool. J. Insect Physiol. 1996;42:565–78.
• Heinbockel T., Kloppenburg P., Hildebrand J.G. Pheromone-evoked potentials and oscillations in the antennal lobes of the sphinx moth Manduca sexta. J. Comp. Physiol. A. 1998;182:703–14. [PubMed: 9631552]
• Heisenberg M. Mushroom body memoir: From maps to models. Nat. Rev. Neurosci. 2003;4:266–75. [PubMed: 12671643]
• Hildebrand J.G., Shepherd G.M. Mechanisms of olfactory discrimination: Converging evidence for common principles across phyla. Annu. Rev. Neurosci. 1997;20:595–631. [PubMed: 9056726]
• Hill E.S., Iwano M., Gatellier L., Kanzaki R. Morphology and physiology of the serotoninimmunoreactive putative antennal lobe feedback neuron in the male silk moth Bombyx mori. Chem. Senses. 2002;27:475–83. [PubMed: 12052784]
• Hill E.S., Okada K., Kanzaki R. Visualization of modulatory effects of serotonin in the silk moth antennal lobe. J. Exp. Biol. 2003;206:345–52. [PubMed: 12477903]
• Hillier N.K., Kleineidam C., Vickers N.J. Physiology and glomerular projections of olfactory receptor neurons on the antenna of female Heliothis virescens (Lepidoptera: Noctuidae) responsive to behaviorally relevant odors. J. Comp. Physiol. A. 2006;192:199–219. [PubMed: 16249880]
• Homberg U., Christensen T.A., Hildebrand J.G. Structure and function of the deutocerebrum in insects. Annu. Rev. Entomol. 1989;34:477–501. [PubMed: 2648971]
• Homberg U., Davis N.T., Hildebrand J.G. Peptide-immunocytochemistry of neurosecretory cells in the brain and retrocerebral complex of the sphinx moth Manduca sexta. J. Comp. Neurol. 1991;303:a35–52. [PubMed: 1706364]
• Homberg U., Hildebrand J.G. Serotonin-immunoreactive neurons in the median protocerebrum and subesophageal ganglion of the sphinx moth Manduca sexta. Cell Tissue Res. 1989;258:1–24. [PubMed: 2680097]
• Homberg U., Hildebrand J.G. Histamine-immunoreactive neurons in the midbrain and suboesophageal ganglion of the sphinx moth Manduca sexta. J. Comp. Neurol. 1991;307:647–57. [PubMed: 1869635]
• Homberg U., Kingan T.G., Hildebrand J.G. Immunocytochemistry of GABA in the brain and suboesophageal ganglion of Manduca sexta. Cell Tissue Res. 1987;248:1–24. [PubMed: 3552234]
• Homberg U., Kingan T.G., Hildebrand J.G. Distribution of FMRFamide-like immunoreactivity in the brain and suboesophageal ganglion of the sphinx moth Manduca sexta and colocalization with SCPB-, BPP-, and GABA-like immunoreactivity. Cell Tissue Res. 1990;259:401–19. [PubMed: 2180574]
• Homberg U., Montague R.A., Hildebrand J.G. Anatomy of antenno-cerebral pathways in the brain of the sphinx moth Manduca sexta. Cell Tissue Res. 1988;254:255–81. [PubMed: 3197087]
• Homberg U., Müller U. Neuroactive substances in the antennal lobe. In: Hansson B.S., editor. Insect Olfaction. Berlin: Springer; 1999. pp. 181–206.
• Honda K. Chemical basis of differential oviposition by lepidopterous insects. Arch. Insect Biochem. Physiol. 1995;30:1–23.
• Hoskins S.G., Homberg U., Kingan T.G., Christensen T.A., Hildebrand J.G. Immunocytochemistry of GABA in the antennal lobes of the sphinx moth Manduca sexta. Cell Tissue Res. 1986;244:243–52. [PubMed: 3521878]
• Huetteroth W., Schachtner J. Standard three-dimensional glomeruli of the Manduca sexta antennal lobe: A tool to study both developmental and adult neuronal plasticity. Cell Tissue Res. 2005;319:513–24. [PubMed: 15672266]
• Ishida Y., Leal W.S. Rapid inactivation of a moth pheromone. Proc. Natl. Acad. Sci. USA. 2005;102:14075–79. [PMC free article: PMC1216831] [PubMed: 16172410]
• Ito I., Ong R.C., Raman B., Stopfer M. Sparse odor representation and olfactory learning. Nat. Neurosci. 2008;11:1177–84. [PMC free article: PMC3124899] [PubMed: 18794840]
• Iwano M., Hill E.S., Mori A., Mishima T., Mishima T., Ito K., Kanzaki R. Neurons associated with the flip-flop activity in the lateral accessory lobe and ventral protocerebrum of the silkworm moth brain. J. Comp. Neurol. 2009 [PubMed: 19950256]
• Iwano M., Kanzaki R. Immunocytochemical identification of neuroactive substances in the antennal lobe of the male silkworm moth Bombyx mori. Zool. Sci. 2005;22:199–211. [PubMed: 15738640]
• Jacquin-Joly E., Lucas P. Pheromone reception and transduction: Mammals and insects illustrate converging mechanisms across phyla. Curr. Top. Neurochem. 2005;4:75–105.
• Jacquin-Joly E., Merlin C. Insect olfactory receptors: Contributions of molecular biology to chemical ecology. J. Chem. Ecol. 2004;30:2359–97. [PubMed: 15724962]
• Jefferis G.S., Potter C.J., Chan A.M. et al. Comprehensive maps of Drosophila higher olfactory centers: Spatially segregated fruit and pheromone representation. Cell. 2007;128:1187–1203. [PMC free article: PMC1885945] [PubMed: 17382886]
• Jones W.D., Nguyen T.T., Kloss B., Lee K.J., Vosshall L.B. Functional conservation of an insect odorant receptor gene across 250 million years of evolution. Curr. Biol. 2005;15:R119–8211. [PubMed: 15723778]
• Jørgensen K., Kvello P., Almaas T.J., Mustaparta H. Two closely located areas in the suboesophageal ganglion and the tritocerebrum receive projections of gustatory receptor neurons located on the antennae and the proboscis in the moth Heliothis virescens. J. Comp. Neurol. 2006;496:121–34. [PubMed: 16528726]
• Jørgensen K., Stranden M., Sandoz J.C., Menzel R., Mustaparta H. Effects of two bitter substances on olfactory conditioning in the moth Heliothis virescens. J. Exp. Biol. 2007;210:2563–73. [PubMed: 17601960]
• Judd G.J.R., Gardiner M.G.T., DeLury N.C., Karg G. Reduced antennal sensitivity, behavioral response, and attraction of male codling moths, Cydia pomonella, to their pheromone (E,E)-8,10-dodecadien-1-ol following various pre-exposure regimes. Entomol. Exp. Appl. 2005;114:65–78.
• Justus K.A., Cardé R.T. Flight behavior of males of two moths, Cadra cautella and Pectinophora gossypiella, in homogeneous clouds of pheromone. Physiol. Entomol. 2002;27:67–75.
• Kárpáti Z., Dekker T., Hansson B.S. Reversed functional topology in the antennal lobe of the male European corn borer. J. Exp. Biol. 2008;211:2841–48. [PubMed: 18723543]
• Kaissling K.-E. R. H. Wright Lectures on Insect Olfaction. Burnaby, BC, Canada: Simon Fraser University; 1987.
• Kaissling K.-E. Olfactory perireceptor and receptor events in moths: A kinetic model. Chem. Senses. 2001;26:125–50. [PubMed: 11238244]
• Kaissling K.-E., Kasang G., Bestmann H.J., Stransky W., Vostrowsky O. A new pheromone of the silkworm moth Bombyx mori. Sensory pathway and behavioral effect. Naturwissenschaften. 1978;65:382–84.
• Kaissling K.-E., Kramer E. Sensory basis of pheromone mediated orientation in moths. Verh. Dtsch. Zool. Ges. 1990;83:109–31.
• Kaissling K.-E., Priesner E. Die Riechschwelle des Seidenspinners. Naturwissenschaften. 1970;57:23–28. [PubMed: 5417282]
• Kanzaki R. Pheromone processing in the lateral accessory lobe of the moth brain: Flip-flopping signals related to zigzagging upwind walking. In: Cardé R.T., Minks A.K., editors. Insect Pheromone Research: New Directions. New York: Chapman & Hall; 1997. pp. 291–303.
• Kanzaki R. Coordination of wing motion and walking suggests common control of zigzag motor program in a male silkworm moth. J. Comp. Physiol. A. 1998;182:267–76.
• Kanzaki R., Ando N., Sakurai T., Kazawa T. Understanding and reconstruction of the mobiligence of insects employing multiscale biological approaches and robotics. Adv. Robotics. 2008;22:1605–28.
• Kanzaki R., Arbas E.A., Hildebrand J.G. Physiology and morphology of protocerebral olfactory neurons in the male moth Manduca sexta. J. Comp Physiol. A. 1991a;168:281–98. [PubMed: 2066906]
• Kanzaki R., Arbas E.A., Hildebrand J.G. Physiology and morphology of descending neurons in pheromone-processing olfactory pathways in the male moth Manduca sexta. J. Comp Physiol. A. 1991b;169:1–14. [PubMed: 1941713]
• Kanzaki R., Arbas E.A., Strausfeld N.J., Hildebrand J.G. Physiology and morphology of projection neurons in the antennal lobe of the male moth Manduca sexta. J. Comp. Physiol. A. 1989;165:427–53. [PubMed: 2769606]
• Kanzaki R., Ikeda A., Shibuya T. Morphological and physiological properties of pheromone-triggered flipflopping descending interneurons of the male silkworm moth, Bombyx mori. J. Comp. Physiol A. 1994;175:1–14.
• Kanzaki R., Mishima T. Pheromone-triggered “flipflopping” neural signals correlate with activities of neck motor neurons of a male moth, Bombyx mori. Zool. Sci. 1996;13:79–87.
• Kanzaki R., Shibuya T. Olfactory neural pathway and sexual pheromone responses in the deutocerebrum of the male silkworm moth, Bombyx mori (Lepidoptera: Bombycidae). Appl. Entomol. Zool. 1983;18:131–33.
• Kanzaki R., Shibuya T. Identification of the deutocerebral neurons responding to the sexual pheromone in the male silkworm moth brain. Zool. Sci. 1986a;3:409–18.
• Kanzaki R., Shibuya T. Descending protocerebral neurons related to the mating dance of the male silkworm moth. Brain Res. 1986b;377:378–82. [PubMed: 3730870]
• Kanzaki R., Shibuya T. Long-lasting excitation of protocerebral bilateral neurons in the pheromone-processing pathways of the male moth Bombyx mori. Brain Res. 1992;587:211–15. [PubMed: 1525657]
• Kanzaki R., Soo K., Seki Y., Wada S. Projections to higher order olfactory centers from subdivisions of the antennal lobe macroglomerular complex of the male silk moth. Chem. Senses. 2003;28:113–30. [PubMed: 12588734]
• Kanzaki R., Sugi N., Shibuya T. Self-generated zigzag turning of Bombyx mori males during pheromone-mediated upwind walking. Zool. Sci. 1992;9:515–27.
• Kazawa T., Namiki S., Fukushima R. et al. Constancy and variability of glomerular organization in the antennal lobe of the silkmoth Cell Tissue Res. 2009 doi/10.1007/S0041–009–0756–8211. [PubMed: 19225812]
• Keil T.A. Fine structure of a developing insect olfactory organ: Morphogenesis of the silk moth antenna. Microsc. Res. Tech. 1992;22:351–71. [PubMed: 1392065]
• Keil T.A. Morphology and development of the peripheral olfactory organs. In: Hansson B.S., editor. Insect Olfaction. Berlin: Springer; 1999. pp. 5–48.
• Kennedy J.S. Zigzagging and casting as a programmed response to wind-borne odor: A review. Physiol. Entomol. 1983;3:1–98.
• Kennedy J.S., Ludlow A.R., Sanders C.J. Guidance system used in moth sex attraction. Nature. 1980;288:475–77.
• Kennedy J.S., Marsh D. Pheromone-regulated anemotaxis in flying moths. Science. 1974;184:999–1001. [PubMed: 4826172]
• Kent K.S., Harrow I.D., Quartararo P., Hildebrand J.G. An accessory olfactory pathway in Lepidoptera: The labial pit organ and its central projections in Manduca sexta and certain other sphinx moths and silk moths. Cell Tissue Res. 1986;245:237–45. [PubMed: 3742559]
• Kent K.S., Hoskins S.G., Hildebrand J.G. A novel serotonin-immunoreactive neuron in the antennal lobe of the sphinx moth Manduca sexta persists throughout postembryonic life. J. Neurobiol. 1987;18:451–65. [PubMed: 3309187]
• Kijima H., Okada Y., Oiki S. et al. Free ion concentrations in receptor lymph and role of transepithelial voltage in the fly labeler taste receptor. J. Comp. Physiol. A. 1995;177:123–33.
• Kloppenburg P., Camazine S.M., Sun X.J., Randolph P., Hildebrand J.G. Organization of the antennal motor system in the sphinx moth Manduca sexta. Cell Tissue Res. 1997;287:425–33. [PubMed: 8995213]
• Kloppenburg P., Ferns D., Mercer A.R. Serotonin enhances central olfactory neuron responses to female sex pheromone in the male sphinx moth Manduca sexta. J. Neurosci. 1999;19:8172–81. [PMC free article: PMC6783045] [PubMed: 10493719]
• Kloppenburg P., Heinbockel T. 5-hydroxytryptamine modulates pheromone-evoked local field potentials in the macroglomerular complex of the sphinx moth Manduca sexta. J. Exp. Biol. 2000;203:1701–9. [PubMed: 10804160]
• Kloppenburg P., Hildebrand J.G. Neuromodulation by 5-hydroxytryptamine in the antennal lobe of the sphinx moth Manduca sexta. J. Exp. Biol. 1995;198:603–11. [PubMed: 7714450]
• Kloppenburg P., Mercer A.R. Serotonin modulation of moth central olfactory neurons. Annu. Rev. Entomol. 2008;53:179–90. [PubMed: 18067443]
• Koehl M.A. The fluid mechanics of arthropod sniffing in turbulent odor plumes. Chem. Senses. 2006;31:93–105. [PubMed: 16339271]
• Koontz M.A., Schneider D. Sexual dimorphism in neuronal projections from the antennae of silk moths (Bombyx mori, Antheraea polyphemus) and the gypsy moth (Lymantria dispar). Cell Tissue Res. 1987;249:39–50.
• Kramer E. Orientation of the male silk moth to the sex attractant bombykol. In: Denton D.A., Coghlan J., editors. Olfaction and Taste V. New York: Academic Press; 1975. pp. 329–35.
• Kramer E. Turbulent diffusion and pheromone-triggered anemotaxis. In: Payne T.L., Birch M.C., Kennedy D. E. J., editors. Mechanisms in Insect Olfaction. Oxford: Oxford University Press; 1986. pp. 39–48.
• Kramer E. Attractivity of pheromone surpassed by time-patterned application of two nonpheromone compounds. J. Insect Behav. 1992;5:83–97.
• Kramer E. A tentative intercausal nexus and its computer model on insect orientation in windborne pheromone plumes. In: Cardé R.T., Minks A.K., editors. Insect Pheromone Research: New Directions. New York: Chapman & Hall; 1997. pp. 232–47.
• Krasnoff S.B., Bjostad L.B., Roelofs W.L. Quantitative and qualitative variation in male pheromones of Phragmatobia fuliginosa and Pyrrharctia isabella (Lepidoptera: Arctiidae). J. Chem. Ecol. 1987;13:807–22. [PubMed: 24302048]
• Krieger J., Breer H. Olfactory reception in invertebrates. Science. 1999;286:720–23. [PubMed: 10531050]
• Krieger J., Große-Wilde E., Gohl T. et al. Genes encoding pheromone receptors in a moth (Heliothis virescens). Proc. Natl. Acad. Sci. USA. 2004;101:11845–50. [PMC free article: PMC511062] [PubMed: 15289611]
• Krieger J., Klink O., Mohl C., Breer H. A candidate olfactory receptor subtype highly conserved across different insect orders. J. Comp. Physiol. A. 2003;189:519–26. [PubMed: 12827420]
• Krieger J., Raming K., Dewer Y.M.E. et al. A divergent gene family encoding candidate olfactory receptors of the moth Heliothis virescens. Eur. J. Neurosci. 2002;16:619–28. [PubMed: 12270037]
• aKrieger J., von Nickisch-Rosenegk E., Mameli M., Pelosi P., Breer H. Binding proteins from the antennae of Bombyx mori. Insect Biochem. Mol. Biol. 1996;26:297–307. [PubMed: 8900598]
• Kuenen L.P.S., Baker T.C. Habituation versus sensory adaptation as the cause of reduced attraction following pulsed and constant sex pheromone pre-exposure in Trichoplusia ni. J. Insect. Physiol. 1981;27:721–26.
• Kuenen L.P.S., Baker T.C. The effects of pheromone concentration on the flight behavior of the oriental fruit moth, Grapholita molesta. Physiol. Entomol. 1982;7:423–34.
• Kuenen L.P.S., Baker T.C. A non-anemotactic mechanism used in pheromone source location by flying moths. Physiol. Entomol. 1983;8:277–89. [PubMed: 17745868]
• Kvello P., Almaas T.J., Mustaparta H. A confined taste area in a lepidopteran brain. Arthropod Struct. Dev. 2006;35:35–25. [PubMed: 18089056]
• Landolt P.J., Heath R.R., Millar J.G. et al. Effects of host plant, Gossypium hirsutum L., on sexual attraction of cabbage looper moths, Trichoplusia ni (Hübner) (Lepidoptera: Noctuidae). J. Chem. Ecol. 1994;20:2959–74. [PubMed: 24241928]
• Larsson M., Domingos A.I., Jones W.D. et al. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron. 2004;43:703–14. [PubMed: 15339651]
• Laue M., Steinbrecht R.A. Topochemistry of moth olfactory sensilla. Int. J. Insect Morphol. Embryol. 1997;26:217–28.
• Laurent G. Olfactory network dynamics and the coding of multidimensional signals. Nat. Rev. Neurosci. 2002;3:884–95. [PubMed: 12415296]
• Laurent G., Naraghi M. Odorant-induced oscillations in the mushroom bodies of the locust. J. Neurosci. 1994;14:2993–3004. [PMC free article: PMC6577505] [PubMed: 8182454]
• Lei H., Anton S., Hansson B.S. Olfactory protocerebral pathways processing sex pheromone and plant odor information in the male moth Agrotis segetum. J. Comp. Neurol. 2001;432:356–70. [PubMed: 11246213]
• Lei H., Christensen T.A., Hildebrand J.G. Local inhibition modulates odor-evoked synchronization of glomerulus-specific output neurons. Nat. Neurosci. 2002;5:557–65. [PubMed: 12006983]
• Lei H., Christensen T.A., Hildebrand J.G. Spatial and temporal organization of ensemble representations for different odor classes in the moth antennal lobe. J. Neurosci. 2004;24:11108–19. [PMC free article: PMC6730268] [PubMed: 15590927]
• Lei H., Hansson B.S. Central processing of pulsed pheromone signals by antennal lobe neurons in the male moth Agrotis segetum. J. Neurophysiol. 1999;81:1113–22. [PubMed: 10085338]
• Light D.M. Central integration of sensory signals: An exploration of processing of pheromonal and multimodal information in lepidopteran brains. In: Payne T.L.M., Birch M.C., Kennedy D.E.J., editors. Mechanisms in Insect Olfaction. Oxford: Oxford University Press; 1986. pp. 287–301.
• Lingren P.D., Greene G.L., Davis D.R., Baumhover A.H., Henneberry T.J. Nocturnal behavior of four Lepitopteran pests that attack tobacco and other crops. Ann. Entomol. Soc. Am. 1977;70:161–67.
• Linn C.E. Neuroendocrine factors in the photoperiodic control of male moth responsiveness to pheromone. In: Cardé R.T., Minks A.K., editors. Insect Pheromone Research: New Directions. New York: Chapman & Hall; 1997. pp. 232–47.
• Linn C.E., Roelofs W.L. Modulatory effects of octopamine and serotonin on male sensitivity and periodicity of responses to sex pheromone in the cabbage looper moth Trichoplusia ni. Arch. Insect Biochem. Physiol. 1986;3:161–72.
• Linster C., Sachse S., Galizia C.G. Computational modeling suggests that response properties rather than spatial position determine connectivity between olfactory glomeruli. J. Neurophysiol. 2005;93:3410–17. [PubMed: 15673548]
• Liu S.S., Li Y.H., Liu Y.Q., Zalucki M.P. Experience-induced preference for oviposition repellents derived from a non-host plant by a specialist herbivore. Ecol. Lett. 2005;8:722–29.
• Mafra-Neto A., Cardé R.T. Fine-scale structure of pheromone plumes modulates upwind orientation of flying moths. Nature. 1994;369:142–44.
• Mafra-Neto A., Cardé R.T. Influence of plume structure and pheromone concentration on upwind flight of Cadra cautella males. Physiol. Entomol. 1995;20:117–33.
• Marion-Poll F., Tobin T.R. Temporal coding of pheromone pulses and trains in Manduca sexta. J. Comp. Physiol. A. 1992;171:505–12. [PubMed: 1469666]
• Masante-Roca I., Anton S., Delbac L., Dufour M.-C., Gadenne C. Attraction of the grapevine moth to host and non-host plant parts in the wind tunnel: Effects of plant phenology, sex, and mating status. Entomol. Exp. Appl. 2007;122:239–45.
• Masante-Roca I., Gadenne C., Anton S. Three-dimensional antennal lobe atlas of male and female moths, Lobesia botrana (Lepidoptera: Tortricidae) and glomerular representation of plant volatiles in females. J. Exp. Biol. 2005;208:1147–59. [PubMed: 15767314]
• Matsumoto S.G., Hildebrand J.G. Olfactory mechanisms in the moth Manduca sexta: Response characteristics and morphology of central neurons in the antennal lobes. Proc. R. Soc. B. 1981;213:249–77.
• Mechaber W.L., Capaldo C.T., Hildebrand J.G. Behavioral responses of adult female tobacco hornworms, Manduca sexta, to hostplant volatiles change with age and mating status. J. Insect Sci. 2002;2:1–8. [PMC free article: PMC355905] [PubMed: 15455039]
• Meijerink J., Carlsson M.A., Hansson B.S. Spatial representation of odorant structure in the moth antennal lobe: A study of structure-response relationships at low doses. J. Comp. Neurol. 2003;467:11–21. [PubMed: 14574676]
• Menzel R. Searching for the memory trace in a mini-brain, the honeybee. Learn. Mem. 2001;8:53–62. [PubMed: 11274250]
• Mercer A.R., Hayashi J.H., Hildebrand J.G. Modulatory effects of serotonin on voltage-activated currents in cultured antennal lobe neurons of the sphinx moth Manduca sexta. J. Exp. Biol. 1995;198:613–27. [PubMed: 7714451]
• Merlin C., Lucas P., Rochat D. et al. An antennal circadian clock and circadian rhythms in peripheral pheromone reception in the moth Spodoptera littoralis. J. Biol. Rhythms. 2007;22:502–14. [PubMed: 18057325]
• Mishima T., Kanzaki R. Coordination of flipflopping neural signals and head turning during pheromone-mediated walking in a male silkworm moth Bombyx mori. J. Comp. Physiol. A. 1998;183:273–82.
• Mishima T., Kanzaki R. Physiological and morphological characterization of olfactory descending interneurons of the male silkworm moth, Bombyx mori. J. Comp. Physiol. A. 1999;184:143–60.
• Mitsuno H., Sakurai T., Murai M. et al. Identification of receptors of main sex-pheromone components of three Lepidopteran species. Eur. J. Neurosci. 2008;28:893–902. [PubMed: 18691330]
• Mobbs P.G. Brain structure Comprehensive Insect Physiology, Biochemistry, and Pharmacology. In: Kerkut G.A., Gilbert L.I., editors. Nervous System: Structure and Motor Function. Vol. 5. Oxford: Pergamon: 1985. pp. 299–370.
• Mori A., Kumagai T., Kanzaki R. Neural pathways to generate odor-evoked flip-flopping activities in a brain of a male silkworm moth. Soc. Neurosci. Abstr. 1999;25:389.
• Morita H., Shiraishi A. Chemoreception physiology. In: Kerkut G.A., Gilbert L.I., editors. Comprehensive Insect Physiology, Biochemistry and Pharmacology: Nervous System. Vol. 6. Oxford: Pergamon; 1985. pp. 133–70.
• Murlis J., Elikton J.S., Cardé R.T. Odour plumes and how insects use them. Annu. Rev. Entomol. 1992;37:505–32.
• Murlis J., Jones C.D. Fine-scale structure of odor plumes in relation to insect orientation to distant pheromone and other attractant sources. Physiol. Entomol. 1981;6:71–86.
• Murlis J., Willis M.A., Cardé R.T. Spatial and temporal structures of pheromone plumes in fields and forests. Physiol. Entomol. 2000;25:211–22.
• Mustaparta H. Olfactory coding mechanisms for pheromone and interspecific signal information in related species of moths. In: Cardé R.T., Minks A.K., editors. Insect Pheromone Research: New Directions. New York: Chapman & Hall; 1997. pp. 141–63.
• Mwileria E.K., Ghatak C., Daly K.C. Disruption of GABA_A in the insect antennal lobe generally increases odor detection and discrimination thresholds. Chem. Senses. 2008;33:267–81. [PubMed: 18199605]
• Nakagawa T., Sakurai T., Nishioka T., Touhara K. Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science. 2005;307:1638–42. [PubMed: 15692016]
• Namiki S., Iwabuchi S., Kanzaki R. Representation of a mixture of pheromone and host plant odor by antennal lobe projection neurons of the silk moth Bombyx mori. J. Comp. Physiol. A. 2008;194:501–15. [PubMed: 18389256]
• Namiki S., Kanzaki R. Reconstructing the population activity of olfactory output neurons innervating identifiable processing units. Front. Neural Circuits. 2008;2(1) http://frontiersin​.org​/neuralcircuits/paper/10​.3389/neuro.04/001.2008/pdf (accessed on 1 January 2009) [PMC free article: PMC2526276] [PubMed: 18946541]
• Natale D., Mattiacci L., Pasqualini E., Dorn S. Apple and peach fruit volatiles and the apple constituent butyl hexanoate attract female oriental fruit moth, Cydia molesta, in the laboratory. J. Appl. Entomol. 2004;128:22–27.
• Neuhaus E.M., Gisselmann G., Zhang W. et al. Odorant receptor heterodimerization in the olfactory system of Drosophila melanogaster. Nat. Neurosci. 2005;8:15–17. [PubMed: 15592462]
• Nighorn A., Gibson N.J., Rivers D.M., Hildebrand J.G., Morton D.B. The nitric oxide-cGMP pathway may mediate communication between sensory afferents and projection neurons in the antennal lobe of Manduca sexta. J. Neurosci. 1998;18:7244–55. [PMC free article: PMC6793266] [PubMed: 9736646]
• Ochieng S.A., Anderson P., Hansson B.S. Antennal lobe projection patterns of olfactory receptor neurons involved in sex pheromone detection in Spodoptera littoralis (Lepidoptera: Noctuidae). Tissue Cell. 1995;27:221–32. [PubMed: 7539947]
• Ochieng S.A., Park K.C., Baker T.C. Host plant volatiles synergize responses of sex pheromonespecific olfactory receptor neurons in male Helicoverpa zea. J. Comp. Physiol. A. 2002;188:325–33. [PubMed: 12012103]
• Okada K., Kanzaki R. Localization of odor-induced oscillations in the bumblebee antennal lobe. Neurosci. Lett. 2001;316:133–36. [PubMed: 11744220]
• Okada K., Kanzaki R., Kawachi K. High-speed voltage-sensitive dye imaging of an in vivo insect brain. Neurosci. Lett. 1996;209:197–200. [PubMed: 8736644]
• Okada R., Sakura M., Mizunami M. Distribution of dendrites of descending neurons and its implications for the basic organization of the cockroach brain. J. Comp. Neurol. 2003;459:158–74. [PubMed: 12830795]
• Oland L.A., Tolbert L.P. Multiple factors shape development of olfactory glomeruli: Insights from an insect model system. J. Neurobiol. 1996;30:92–109. [PubMed: 8727986]
• Olberg R.M. Pheromone-triggered flip-flopping interneurons in the ventral nerve cord of the silkworm moth, Bombyx mori. J. Comp. Physiol. 1983;A 152:297–307.
• Olberg R.M., Willis M.A. Pheromone-modulated optomotor response in male gypsy moths, Lymantria dispar L.: Directionally selective visual interneurons in the ventral nerve cord. J. Comp. Physiol. A. 1990;167:707–14.
• Olsen S.R., Bhandawat V., Wilson R.I. Excitatory interactions between olfactory processing channels in the Drosophila antennal lobe. Neuron. 2007;54:89–103. [PMC free article: PMC2048819] [PubMed: 17408580]
• Park K.C., Ochieng S.A., Zhu J., Baker T.C. Odor discrimination using insect electroantennogram responses from an insect antennal array. Chem. Senses. 2002;27:343–52. [PubMed: 12006374]
• Pearson L. The corpora pedunculata of Sphinx ligustri L. and other Lepidoptera: An anatomical study. Phil. Trans. R. Soc. Lond. B. 1971;259:477–516.
• Pelosi P., Zhou J.-J., Ban L.P., Calvello M. Soluble proteins in insect chemical communication. Cell. Mol. Life. Sci. 2006;63:1658–76. [PubMed: 16786224]
• Phelan P.L., Baker T.C. An attracticide for control of Amyelois transitella (Lepidoptera: Pyralidae) in almonds. J. Econ. Entomol. 1987;80:779–83.
• Piñero J.C., Dorn S. Response of female oriental fruit moth to volatiles from apple and peach trees at three phenological stages. Entomol. Exp. Appl. 2007;131:67–74.
• Pophof B. Octopamine modulates the sensitivity of silk moth pheromone receptor neurons. J. Comp. Physiol. A. 2000;186:307–13. [PubMed: 10757246]
• Pophof B. Octopamine enhances moth olfactory responses to pheromones, but not those to general odorants. J. Comp. Physiol. A. 2002;188:659–62. [PubMed: 12355242]
• Pophof B. Pheromone-binding proteins contribute to the activation of olfactory receptor neurons in the silk moths Antheraea polyphemus and Bombyx mori. Chem. Senses. 2004;29:117–25. [PubMed: 14977808]
• Priesner E. Progress in the analysis of pheromone receptor systems. Ann. Zool. Ecol. Anim. 1979;11:533–46.
• Raguso R.A., LeClere A.R., Schlumpberger B.O. Sensory flexibility in hawkmoth foraging behavior: Lessons from Manduca sexta and other species. Chem. Senses. 2005;30:i295–8211. [PubMed: 15738165]
• Raguso R.A., Willis M.A. Synergy between visual and olfactory cues in nectar feeding by naive hawkmoths. Anim. Behav. 2002;63:685–95.
• Raguso R.A., Willis M.A. Synergy between visual and olfactory cues in nectar feeding by wild hawkmoths. Manduca sexta. Anim. Behav. 2005;69:407–18.
• Rains G.C., Tomberlin J.K., Kulasiri D. Using insect sniffing devices for detection. Trends Biotechnol. 2008;26:288–94. [PubMed: 18375006]
• Reddy G.V.P., Guerrero A. Interactions of insect pheromones and plant semiochemicals. Trends Plant Sci. 2004;9:253–61. [PubMed: 15130551]
• Rehder V., Bicker G., Hammer M. Serotonin-immunoreactive neurons in the antennal lobes and suboesophageal ganglion of the honeybee. Cell Tissue Res. 1987;247:59–66.
• Reisenman C.E., Christensen T.A., Hildebrand J.G. Chemosensory selectivity of output neurons innervating an identified, sexually isomorphic olfactory glomerulus. J. Neurosci. 2005;25:8017–26. [PMC free article: PMC1351300] [PubMed: 16135759]
• Reisenman C.E., Heinbockel T., Hildebrand J.G. Inhibitory interactions among olfactory glomeruli do not necessarily reflect spatial proximity. J. Neurophysiol. 2008;100:554–64. [PMC free article: PMC2525721] [PubMed: 18417626]
• Renwick J.A.A., Chew F.S. Oviposition behavior in Lepidoptera. Annu. Rev Entomol. 1994;39:377–400.
• Riffell J.A., Alarcón R., Abrell L. et al. Behavioral consequences of innate preferences and olfactory learning in hawkmoth flower interactions. Proc. Natl. Acad. Sci. USA. 2008;105:3404–9. [PMC free article: PMC2265144] [PubMed: 18305169]
• Rø H., Müller D., Mustaparta H. Anatomical organization of antennal lobe projection neurons in the moth Heliothis virescens. J. Comp. Neurol. 2007;500:658–75. [PubMed: 17154270]
• Rodrigues V., Buchner E. [3H]2-deoxyglucose mapping of odor-induced neuronal activity in the antennal lobes of Drosophila melanogaster. Brain Res. 1984;324:374–78. [PubMed: 6442179]
• Roelofs W.L. Chemistry of sex attraction. Proc. Natl. Acad. Sci. USA. 1995;92:44–49. [PMC free article: PMC42814] [PubMed: 7816846]
• Rojas J.C. Electrophysiological and behavioral responses of the cabbage moth to plant volatiles. J. Chem. Ecol. 1999;25:1867–83.
• Rojas J.C., Wyatt T.D. Role of visual cues and interaction with host odor during the host-finding behavior of the cabbage moth. Entomol. Exp. Appl. 1999;91:59–65.
• Rosén W.Q. Endogenous control of circadian rhythms of pheromone production in the turnip moth. Agrotis segetum. Arch. Insect Biochem. Physiol. 2002;50:21–30. [PubMed: 11948972]
• Rosén W.Q., Han G.B., Löfstedt C. The circadian rhythm of the sex-pheromone-mediated behavioral response in the turnip moth, Agrotis segetum, is not controlled at the peripheral level. J. Biol. Rhythms. 2003;18:402–8. [PubMed: 14582856]
• Rospars J.P. Invariance and sex-specific variations of the glomerular organization in the antennal lobes of a moth, Mamestra brassicae, and a butterfly, Pieris brassicae. J. Comp. Neurol. 1983;220:80–96. [PubMed: 6643719]
• Rospars J.P., Chambille I. Deutocerebrum of the cockroach Blaberus craniifer Burm. Quantitative study and automated identification of glomeruli. J. Neurobiol. 1981;12:221–47. [PubMed: 7276924]
• Rospars J.P., Hildebrand J.G. Anatomical identification of glomeruli in the antennal lobes of the male sphinx moth Manduca sexta. Cell Tissue Res. 1992;270:205–27. [PubMed: 1451169]
• Røstelien T., Borg-Karlson A.-K., Fáldt J., Jacobsson U., Mustaparta H. The plant sesquiterpene germacrene D specifically activates a major type of antennal receptor neuron of the tobacco budworm moth. Heliothis virescens. Chem. Senses. 2000a;25:141–48. [PubMed: 10781020]
• Røstelien T., Borg-Karlson A.-K., Mustaparta H. The selective receptor neurone responses to E-beta-ocimene, beta-myrcene, E,E-alpha-farnesene and homo-farnesene in the moth Heliothis virescens, identified by gas chromatography linked to electrophysiology. J. Comp. Physiol. A. 2000b;186:833–47. [PubMed: 11085637]
• Rössler W., Kuduz J., Schürmann F.W., Schild D. Aggregation of F-actin in olfactory glomeruli: A common feature of glomeruli across phyla. Chem. Senses. 2002;27:803–10. [PubMed: 12438205]
• Rössler W., Tolbert L.P., Hildebrand J.G. Early formation of sexually dimorphic glomeruli in the developing olfactory lobe of the brain of the moth. J. Comp. Neurol. 1998;396:415–28. [PubMed: 9651002]
• Rumbo E.R., Kaissling K.-E. Temporal resolution of odor pulses by three types of pheromone receptor cells in Antheraea polyphemus. J. Comp. Physiol. A. 1989;165:281–91.
• Rybczynski R., Reagen J., Lerner M.R. A pheromone-degrading aldehyde oxidase in the antennae of the moth Manduca sexta. J. Neurosci. 1989;9:1341–53. [PMC free article: PMC6569867] [PubMed: 2703880]
• Sadek M.M., Hansson B.S., Rospars J.P., Anton S. Glomerular representation of plant volatiles and sex pheromone components in the antennal lobe of the female Spodoptera littoralis. J. Exp. Biol. 2002;205:1363–76. [PubMed: 11976349]
• Sakurai T., Nakagawa T., Mitsuno H. et al. Identification and functional characterization of a sex pheromone receptor in the silk moth. Bombyx mori. Proc. Natl. Acad. Sci. USA. 2004;101:16653–58. [PMC free article: PMC528734] [PubMed: 15545611]
• Salecker I., Distler P. Serotonin-immunoreactive neurons in the antennal lobes of the American cockroach Periplaneta americana, lightand electron-microscopic observations. Histochemistry. 1990;94:463–73. [PubMed: 2283309]
• Salecker I., Malun D. Development of olfactory glomeruli. In: Hansson B.S., editor. Insect Olfaction. Berlin: Springer; 1999. pp. 208–42.
• Sane S.P., Dieudonné A., Willis M.A., Daniel T.L. Antennal mechanosensors mediate flight control in moths. Science. 2007;315:771–72. [PubMed: 17290001]
• Sasaki M., Riddford L.M. Regulation of reproductive behavior and egg maturation in the tobacco hawk moth, Manduca sexta. Physiol. Entomol. 1984;9:315–27.
• Sato K., Pellegrino M., Nakagawa T. et al. Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature. 2008;452:1002–7. [PubMed: 18408712]
• Schachtner J., Schmidt M., Homberg U. Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea+Hexapoda). Arthropod Struct. Dev. 2005;34:257–99.
• Schneider D. Elektrophysiologische Untersuchungen von Chemound Mechanorezeptoren der Antenne des Seidenspinners Bombyx mori L. Z. Vergl Physiol. 1957;40:8–41.
• Schröter U., Malun D., Menzel R. Innervation pattern of suboesophageal ventral unpaired median neurones in the honeybee brain. Cell Tissue Res. 2007;327:647–67. [PubMed: 17093927]
• Schuckel J., Siwicki K.K., Stengl M. Putative circadian pacemaker cells in the antenna of the hawkmoth Manduca sexta. Cell Tissue Res. 2007;330:271–78. [PubMed: 17786482]
• Schürmann F.W., Klemm N. Serotonin-immunoreactive neurons in the brain of the honeybee. J. Comp. Neurol. 1984;225:570–80. [PubMed: 6376546]
• Seabrook W.D., Linn C.E., Dyer L.J., Shorey H.H. Comparison of electroantennograms from female and male cabbage looper moths (Trichoplusia ni) of different ages and for various pheromone concentrations. J. Chem. Ecol. 1987;13:1443–53. [PubMed: 24302245]
• Seki Y., Aonuma H., Kanzaki R. Pheromone processing center in the protocerebrum of Bombyx mori revealed by nitric oxide-induced anti-cGMP immunocytochemistry. J. Comp. Neurol. 2005;481:340–51. [PubMed: 15593336]
• Seki Y., Kanzaki R. Comprehensive morphological identification and GABA immunocytochemistry of antennal lobe local interneurons in Bombyx mori. J. Comp. Neurol. 2008;506:93–107. [PubMed: 17990273]
• Shang Y., Claridge-Chang A., Sjulson L., Pypaert M., Miesenböck G. Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe. Cell. 2007;128:601–12. [PMC free article: PMC2866183] [PubMed: 17289577]
• Shields V.D.C., Hildebrand J.G. Recent advances in insect olfaction, specifically regarding the morphology and sensory physiology of antennal sensilla of the female sphinx moth Manduca sexta. Microsc. Res. Tech. 2001;55:307–29. [PMC free article: PMC2386875] [PubMed: 11754510]
• Shorey H.H., Gaston L.K. Sex pheromones of noctuid moths. V. Circadian rhythm of pheromone-responsiveness in males of Autographa californica, Heliothis virescens, Spodoptera exigua, and Trichoplusia ni (Lepidoptera: Noctuidae). Ann. Entomol. Soc. Am. 1965;58:597–600. [PubMed: 5834924]
• Silbering A.F., Galizia C.G. Processing of odor mixtures in the Drosophila antennal lobe reveals both global inhibition and glomerulus-specific interactions. J. Neurosci. 2007;27:11966–77. [PMC free article: PMC6673347] [PubMed: 17978037]
• Silvegren G., Löfstedt C., Rosén W.Q. Circadian mating activity and effect of pheromone preexposure on pheromone response rhythms in the moth Spodoptera littoralis. J. Insect Physiol. 2005;51:277–86. [PubMed: 15749110]
• Sinakevitch I., Sjöholm M., Hansson B.S., Strausfeld N.J. Global and local modulatory supply to the mushroom bodies of the moth Spodoptera littoralis. Arthropod Struct. Dev. 2008;37:260–72. [PMC free article: PMC4876857] [PubMed: 18406668]
• Sjöholm M., Sinakevitch I., Ignell R., Strausfeld N.J., Hansson B.S. Organization of Kenyon cells in subdivisions of the mushroom bodies of a lepidopteran insect. J. Comp. Neurol. 2005;491:290–304. [PubMed: 16134139]
• Sjöholm M., Sinakevitch I., Strausfeld N.J., Ignell R., Hansson B.S. Functional division of intrinsic neurons in the mushroom bodies of male Spodoptera littoralis revealed by antibodies against aspartate, taurine, FMRF-amide, Mas-allatotropin and DC0. Arthropod Struct. Dev. 2006;35:153–68. [PubMed: 18089067]
• Skals N., Anderson P., Kanneworff M., Löfstedt C., Surlykke A. Her odors make him deaf: Crossmodal modulation of olfaction and hearing in a male moth. J. Exp. Biol. 2005;208:595–601. [PubMed: 15695752]
• Skiri H.T., Galizia C.G., Mustaparta H. Representation of primary plant odorants in the antennal lobe of the moth Heliothis virescens using calcium imaging. Chem. Senses. 2004;29:253–67. [PubMed: 15047600]
• Skiri H.T., Stranden M., Sandoz J.C., Menzel R., Mustaparta H. Associative learning of plant odorants activating the same or different receptor neurones in the moth Heliothis virescens. J. Exp. Biol. 2005a;208:787–96. [PubMed: 15695769]
• Skiri H.T., Rø H., Berg B.G., Mustaparta H. Consistent organization of glomeruli in the antennal lobes of related species of heliothine moths. J. Comp. Neurol. 2005b;491:367–80. [PubMed: 16175552]
• Steinbrecht R.A. Olfactory receptors Atlas of Arthropod Sensory Receptors – Dynamic Morphology in Relation to Function. In: Eguchi E., Tominaga Y., editors. Tokyo: Springer; 1999. pp. 155–76.
• Steinbrecht R.A., Laue M., Ziegelberger G. Immunolocalization of pheromone-binding protein and general odorant-binding protein in olfactory sensilla of the silk moths Antheraea and Bombyx. Cell Tissue Res. 1995;282:203–17.
• Steinbrecht R.A., Ozaki M., Ziegelberger G. Immunolocalization of pheromone-binding protein in moth antennae. Cell Tissue Res. 1992;270:287–302.
• Stengl M. Inositol-trisphosphate-dependent calcium currents precede cation currents in insect olfactory receptor neurons. J. Comp. Physiol. 1994;A 174:187–94. [PubMed: 7511689]
• Stopfer M., Bhagavan S., Smith B.H., Laurent G. Impaired odor discrimination on desynchronization of odor-encoding neural assemblies. Nature. 1997;390:70–74. [PubMed: 9363891]
• Stopfer M., Jayaraman V., Laurent G. Intensity versus identity coding in an olfactory system. Neuron. 2003;39:991–1004. [PubMed: 12971898]
• Stopfer M., Laurent G. Short-term memory in olfactory network dynamics. Nature. 1999;402:664–68. [PubMed: 10604472]
• Strausfeld N.J. Atlas of an Insect Brain. Heidelberg; Springer: 1976.
• Strausfeld N.J., Hansen L., Li Y., Gomez R.S., Ito K. Evolution, discovery, and interpretations of arthropod mushroom bodies. Learn. Mem. 1998;5:11–37. [PMC free article: PMC311242] [PubMed: 10454370]
• Sun X.J., Tolbert J.P., Hildebrand J.G. Ramification pattern and ultrastructural characteristics of the serotonin-immunoreactive neuron in the antennal lobe of the moth Manduca sexta: A laser scanning confocal and electron microscopic study. J. Comp. Neurol. 1993;338:5–16. [PubMed: 8300899]
• Tasin M., Anfora G., Ioriatti C. et al. Antennal and behavioral responses of grapevine moth Lobesia botrana females to volatiles from grapevine. J. Chem. Ecol. 2005;31:77–87. [PubMed: 15839481]
• Tegoni M., Campanacci V., Cambillau C. Structural aspects of sexual attraction and chemical communication in insects. Trends Biochem. Sci. 2004;29:257–64. [PubMed: 15130562]
• Tichenor L.H., Seigler D.S. Electroantennogram and oviposition responses of Manduca sexta to volatile components of tobacco and tomato. J. Insect Physiol. 1980;26:309–14.
• Tichy H., Loftus R. Hygroreceptors in insects and a spider: Humidity transduction models. Naturwissenschaften. 1996;83:255–63.
• Thom C., Guerenstein P.G., Mechaber W.L., Hildebrand J.G. Floral CO2 reveals flower profitability to moths. J. Chem. Ecol. 2004;30:1285–88. [PubMed: 15303329]
• Todd J.L., Baker T.C. Function of peripheral olfactory organs. In: Cardé R.T., Minks A.K., editors. Insect Pheromone Research: New Directions. New York: Chapman & Hall; 1997. pp. 164–83.
• Tolbert L.P., Oland L.A., Tucker E.S. et al. Bidirectional influences between neurons and glial cells in the developing olfactory system. Prog. Neurobiol. 2004;73:73–105. [PubMed: 15201035]
• Traynier R.M.M. Habituation of the response to sex pheromone in two species of Lepidoptera, with reference to a method of control. Entomol. Exp. Appl. 1970;13:179–87.
• Tumlinson J.H., Brennan M.M., Doolittle R.E. et al. Identification of a pheromone blend attractive to Manduca sexta (L.) males in a wind tunnel. Arch. Insect Biochem. Physiol. 1989;10:255–71.
• Vickers N.J. Mechanisms of animal navigation in odor plumes. Biol. Bull. 2000;198:203–12. [PubMed: 10786941]
• Tumlinson J.H., Brennan M.M., Doolittle R.E. Winging it: Moth flight behavior and responses of olfactory neurons are shaped by pheromone plume dynamics. Chem. Senses. 2006;31:155–66. [PubMed: 16339269]
• Vickers N.J., Baker T.C. Reiterative responses to single strands of odor promote sustained upwind flight and odor source location by moths. Proc. Natl. Acad. Sci. USA. 1994;91:5756–60. [PMC free article: PMC44075] [PubMed: 11607476]
• Vickers N.J., Christensen T.A. Functional divergence of spatially conserved olfactory glomeruli in two related moth species. Chem. Senses. 2003;28:325–38. [PubMed: 12771019]
• Vickers N.J., Christensen T.A., Baker T.C., Hildebrand J.G. Odour-plume dynamics influence the brain’s code. Nature. 2001;410:466–70. [PubMed: 11260713]
• Vickers N.J., Christensen T.A., Hildebrand J.G. Combinatorial odor discrimination in the brain: Attractive and antagonist odor blends are represented in distinct combinations of uniquely identifiable glomeruli. J. Comp. Neurol. 1998;400:35–56. [PubMed: 9762865]
• Vickers N.J., Poole K., Linn C.E. Plasticity in central olfactory processing and pheromone blend discrimination following interspecies antennal imaginal disc transplantation. J. Comp. Neurol. 2005;491:141–56. [PMC free article: PMC2638497] [PubMed: 16127689]
• Vogt R.G., Prestwich G.D., Lerner M.R. Odorant-binding-protein subfamilies associate with distinct classes of olfactory receptor neurons in insects. J. Neurobiol. 1991;22:74–84. [PubMed: 2010751]
• Vogt R.G., Riddiford L.M. Pheromone binding and inactivation by moth antennae. Nature. 1981;293:161–63. [PubMed: 18074618]
• Vogt R.G., Riddiford L.M., Prestwich G.D. Kinetics properties of a sex pheromone-degrading enzyme: The sensillar esterase of Antheraea polyphemus. Proc. Natl. Acad. Sci. USA. 1985;82:8827–31. [PMC free article: PMC391531] [PubMed: 3001718]
• von Nickisch-Rosenegk E., Krieger J., Kubick S. et al. Cloning of biogenic amine receptors from moths (Bombyx mori and Heliothis virescens). Insect Biochem. Mol. Biol. 1996;26:817–27. [PubMed: 9014328]
• Vosshall L.B., Amrein H., Morozov P.S., Rzhetsky A., Axel R. A spatial map of olfactory receptor expression in the Drosophila antennae. Cell. 1999;96:725–36. [PubMed: 10089887]
• Vosshall L.B., Wong A.A., Axel R. An olfactory sensory map in the fly brain. Cell. 2000;102:147–59. [PubMed: 10943836]
• Wada S., Kanzaki R. Neural control mechanisms of the pheromone-triggered programmed behavior in male silk moths revealed by double-labeling of descending interneurons and a motor neuron. J. Comp. Neurol. 2005;484:168–82. [PubMed: 15736224]
• Wajtasek H., Leal W.S. Conformational change in the pheromone-binding protein from Bombyx mori induced by pH and by interaction with membranes. J. Biol. Chem. 1999;274:30950–56. [PubMed: 10521490]
• Waldrop B., Christensen T.A., Hildebrand J.G. GABA-mediated synaptic inhibition of projection neurons in the antennal lobes of the sphinx moth, Manduca sexta. J. Comp. Physiol A. 1987;161:23–32. [PubMed: 3039128]
• Wang H., Guo W.-F., Zhang P.-J., Wu Z.-Y., Liu S.-S. Experience-induced habituation and preference toward non-host plant odors in ovipositing females of a moth. J. Chem. Ecol. 2008;34:330–38. [PubMed: 18253797]
• Wanner K.W., Anderson A.R., Trowell S.C. et al. Female-biased expression of odourant receptor genes in the adult antennae of the silkworm Bombyx mori. Insect Mol. Biol. 2007;16:107–119. [PubMed: 17257213]
• Wessnitzer J., Webb B. Multimodal sensory integration in insects – toward insect brain control architectures. Bioinsp Biomim. 2006;1:63–75. [PubMed: 17671308]
• Wetzel C.H., Behrendt H.-J., Gisselmann G. et al. Functional expression and characterization of a Drosophila odorant receptor in a heterologous cell system. Proc. Natl. Acad. Sci. USA. 2001;98:9377–80. [PMC free article: PMC55428] [PubMed: 11481494]
• Wicher D., Schafer R., Bauernfeind R. et al. Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels Nature. 2008;452:1007–11. [PubMed: 18408711]
• Willis M.A., Arbas E.A. Odor-modulated upwind flight of the sphinx moth, Manduca sexta L. J Comp. Physiol. A. 1991;169:427–40. [PubMed: 1779417]
• Tumlinson J.H., Brennan M.M., Doolittle R.E. Active behavior and reflexive responses: Another perspective on odor-modulated locomotion. In: Cardé R.T., Minks A.K., editors. Insect Pheromone Research: New Directions. New York: Chapman & Hall; 1997. pp. 304–19.
• Tumlinson J.H., Brennan M.M., Doolittle R.E. Variability in odor-modulated flight by moths. J. Comp. Physiol. A. 1998;182:191–202. [PubMed: 9463918]
• Willis M.A., Baker T.C. Effects of intermittent and continuous pheromone stimulation on the flight behavior of the oriental fruit moth, Grapholita molesta. Physiol. Entomol. 1984;9:341–58.
• Willis M.A., Baker T.C. Comparison of manoeuvres used by walking versus flying Grapholita molesta males during pheromone-mediated upwind movement. J. Insect. Physiol. 1987;33:875–83.
• Wilson C.H., Christensen T.A., Nighorn A.J. Inhibition of nitric oxide and soluble guanylyl cyclase signaling affects olfactory neuron activity in the moth, Manduca sexta. J Comp. Physiol. 2007;A 193:715–28. [PMC free article: PMC2629079] [PubMed: 17551736]
• Wilson R.I., Turner G.C., Laurent G. Transformation of olfactory representation in the Drosophila antennal lobe. Science. 2004;303:366–70. [PubMed: 14684826]
• Witzgall P. Modulation of pheromone-mediated flight in male moths. In: Cardé R.T., Minks A.K., editors. Insect Pheromone Research: New Directions. New York: Chapman & Hall; 1997. pp. 265–74.
• Wu W., Anton S., Löfstedt C., Hansson B.S. Discrimination among pheromone component blends by interneurons in male antennal lobes of two populations of the turnip moth. Agrotis segetum Proc. Natl. Acad. Sci. USA. 1996;93:8022–27. [PMC free article: PMC38868] [PubMed: 8755596]
• Xiang Z., Mita K., Xia Q. et al. The genome of a lepidopteran model insect, the silkworm Bombyx mori. Insect Biochem Mol. Biol. 2008 doi: 10.1016/j.ibmb.2008.11.004. [PubMed: 19121390]
• Yamagata T., Sakurai T., Uchino K. et al. GFP labeling of neurosecretory cells with the GAL4/UAS system in the silk moth brain enables selective intracellular staining of neurons. Zool. Sci. 2008;25:509–16. [PubMed: 18558804]
• Yamasaki T., Isokawa T., Matsui N., Ikeno H., Kanzaki R. Reconstruction and simulation for three-dimensional morphological structure of insect neurons. Neurocomputing. 2006;69:1043–47.
• Yang Z., Bengtsson M., Witzgall P. Host plant volatiles synergize response to sex pheromone in codling moth. Cydia pomonella J. Chem. Ecol. 2004;30:619–29. [PubMed: 15139312]
• Zhang P.J., Liu S.S., Wang H., Zalucki M.P. The influence of early adult experience and larval food restriction on responses toward non-host plants in moths. J. Chem. Ecol. 2007;33:1528–41. [PubMed: 17593465]