2.1. INSECT OLFACTORY RECEPTORS

Most organisms rely on their olfactory system to detect and analyze olfactory cues in the environment, cues that are subsequently utilized in the context of behavior. Odorants are recognized by olfactory sensory neurons (OSNs), which are located in the olfactory epithelia of vertebrates or in the dendrites of olfactory sensory cells within the sensilla on the antennal surface of insects (Buck and Axel 1991; Carlson 2001; Chess et al. 1992; Vosshall et al. 2000). The OSNs express odorant receptors (ORs), which are related to seven transmembrane G-protein-coupled receptors (GPCR) and transduce odorant binding to cellular excitation (see also Chapter 7). The olfactory system of the genetic model organism, the fruit fly Drosophila melanogaster, has been the focus of numerous investigations. Drosophila has two pairs of olfactory organs, the antennae and the maxillary palps. Each antenna contains about 1200 OSNs housed in a total of 410 olfactory sensilla covering the antenna, while the maxillary palp has about 120 OSNs and 60 olfactory sensilla (Laissue and Vosshall 2007). The sensilla are of three morphological types: basiconic sensilla, trichoid sensilla, and coeloconic sensilla (Venkatesh and Singh 1984). Across insects, there is a beautiful diversity of sensillar morphologies, including pore plate sensilla, campaniform sensilla, sensilla ampullacea, and more (Kleineidam and Tautz 1996; Steinbrecht 1996). In recent studies, the OR gene family of D. melanogaster has been identified and shown to comprise 62 defned members (Table 2.1) (Clyne et al. 1999; Gao and Chess 1999; Vosshall et al. 1999). Several studies have been dedicated to characterize the molecular receptive ranges of identified ORs (Dobritsa et al. 2003; Hallem and Carlson 2006; Pelz et al. 2006).

TABLE 2.1

List of Sensilla, OR type, Innervated Glomerulus, and Best Ligand for Drosophila Melanogaster.

ORs are expressed following a conserved pattern in Drosophila as well as in mammals (see Chapter 7). Every OSN typically expresses only one type of OR (as well as the ubiquitous Or83b, see below). However, a given OSN can also coexpress up to three conventional ORs determining a specific molecular response profile along with the Or83 coreceptor (Table 2.1). OSNs expressing the same type of OR, converge to a single glomerulus in the antennal lobe (AL), which represents the first olfactory neuropil in the insect brain (see below). However, a few cases of 1:2 and 2:1 innervation ratios in Drosophila have also been described (Couto et al. 2005; Fishilevich and Vosshall 2005).

Interestingly, ORs in Drosophila possess no significant homology to other known GPCRs. However, the total length of the receptor proteins and the size of the internal and external loops are similar to most members of the GPCR protein family (Clyne et al. 1999). The identified genes of the OR family are highly divergent, even among drosophilid species. At least two receptors generate alternative splicing products (Clyne et al. 1999; Robertson et al. 2003).

While the functional organization of the olfactory system in vertebrates and insects shows clear similarities, the atypical heteromeric and topological design of the ORs in Drosophila appears to be insect-specific. Almost all OSNs express a chaperon receptor, called Or83b. Or83b is highly conserved in many insect species (Dahanukar et al. 2005), and it is also possible to functionally exchange Or83b with orthologous Or83b proteins from other insects (Hill et al. 2002; Jones et al. 2005; Krieger et al. 2003; Pitts et al. 2004).

Or83b has a membrane topology that differs from the related GPCR topology, with the N-terminus and the most conserved loops located in the cytoplasm (Benton et al. 2006). Furthermore, Or83b has a 70-amino acid long insert in the second intracellular loop, which might be responsible for the distinct function of Or83b vis-à-vis the remaining members of the insect OR family (Benton et al. 2006). In recent studies, it was shown that Or83b is a nonselective cation channel that interacts directly with the endogenous ligand-tuned OR (Sato et al. 2008; Wicher et al. 2008). In addition, Or83b is needed for the functional integration of receptor proteins in the dendritic part of the OSNs within the sensillum shaft (Larsson et al. 2004; Neuhaus et al. 2005per).

The possible role of the G-proteins expressed in OSNs remains unclear, and the involvement of G-proteins in the signal pathway is a controversial topic. While Sato et al. (2008) give evidence primarily for a direct ligand gating of the receptor complex, Wicher et al. (2008) show that the Or83b channel is also activated by internal cAMP or cGMP. The activation of the G-protein-coupled signal cascade appears considerably slower than the ionotropic response of the receptor complex. The G-protein-coupled signal cascade modulates the activation of the odorant through either cAMP and the subsequent opening of cyclic nucleotide-gated channels or through an IP₃-mediated signal cascade (Krieger and Breer 1999). In OSNs of the maxillary palps, a phospholipase C could be substantiated as an important part of the IP₃-signal pathway (Riesgo-Escovar et al. 1995). Even though molecular response profiles are known for many Drosophila receptors, the interaction of ORs with the component of the signal cascade is not yet well understood. An important task will be to localize both the binding sites of ORs with the odor ligand, and with the intracellular signaling components. Furthermore, it has to be solved which domains of the ORs and the Or83b channel interact with each other, and how this interaction leads to a functional cellular response.

Not all OSNs express ORs that are related to GPCRs. In Drosophila, a recent study has identified the receptors that are expressed in coeloconic sensilla. These receptors are related to the gene family encoding ionotropic glutamate receptors and were therefore named ionotropic receptors (IRs) (Benton et al. 2009). Their sequence shows that they do not belong to the hitherto described kainate, AMPA, or NMDA classes. IRs are expressed in a combinatorial fashion in OSNs housed in coeloconic sensilla that respond to many distinct odors, but do not express either insect ORs or gustatory receptors.

Another important player in the primary odor response consists of a family of odorant binding proteins (OBPs). OBPs are assumed to guide the odorous molecules through the sensillum lymph to allow interaction with a specific OR in the dendritic membrane of the OSNs, but more complex models of their action draw a multifunctional picture (Kaissling 2001). Evidence from various insect species indicates a complex interplay of several sensory molecules in the subsequent pheromone reception and transduction process (Vogt 2003; Vosshall 2008). While specialized pheromone binding proteins (PBPs) are supposed to shuttle hydrophobic pheromone molecules through the sensillum lymph toward specific receptors (Leal 2003; Xu et al. 2005), a so-called sensory neuron membrane protein is suggested to stabilize a functional receptor complex or dock PBPs to the receptor site (Vogt 2003; Jin et al. 2008). The former concept that a PBP just passively transports pheromones to sensory cells has been challenged by studies showing that PBPs specifically interact with pheromones and undergo distinct conformational changes (Mohl et al. 2002; Grosse-Wilde et al. 2006; Laughlin et al. 2008). Interestingly, the conformational change of a PBP has been found to be sufficient for neuronal activation, suggesting a direct interaction of a pheromone/PBP complex with the receptor (Laughlin et al. 2008). One identified member of the PBP family is the OBP, LUSH, which is expressed and secreted exclusively by non neuronal support cells in trichoid sensilla (Kim et al. 1998; Shanbhag et al. 2005). A study by Xu et al. (2005) shows that LUSH is required for activation of pheromone-sensitive OSNs in Drosophila. LUSH mutants lack the detection of the pheromone, cis-vaccenyl acetate, at the physiological as well as at the behavioral level. Unlike the situation in vertebrates, where OBPs are present in the olfactory mucosa and thus potentially in contact with all OSNs, the compartmentalization of OSNs into sensilla gives insects a much more specific control: OPBs are selectively present in particular sensilla, and are more likely to contribute to odor-specific response profles.

2.2. THE ANTENNAL LOBE (AL)

The first neuropil in the insect brain that processes olfactory information is the AL, a structure common to all insects, and secondarily lost in some anosmic species (Strausfeld and Hildebrand 1999). It is analogous in structure and function to the vertebrate olfactory bulb, but evolved independently (Strausfeld and Hildebrand 1999). However, unlike in mammals, insect neurons generally have their cell bodies outside the brain, and synaptic computation is accomplished entirely in the somaless neuropil. Similarly, while the mammalian bulb is structured in layers (glomerular layer, soma layer, etc.,) the insect AL is structured entirely in glomerular units, which are the interaction sites of OSNs, local neurons (LNs), projection neurons (PNs), and others (Figure 2.1A and B). Most synap-tic contacts are within olfactory glomeruli (Boeckh and Tolbert 1993; Gascuel and Masson 1991).

FIGURE 2.1

Olfactory system in the fruit fy, Drosophila melanogaster. (A) Schematic view of the fy head, with a cut-open brain. Olfactory sensory neurons (OSNs) are located on the antennae and project into the antennal lobe, where they interact with local neurons (more...)

Even though the structure and function of ALs appears close to universal, there is considerable diversity of AL organization across insects (Schachtner et al. 2005). Indeed, insects have an evolutionary history of over 400 million years, and most modern insect orders were already present 250 million years ago, allowing for considerable divergent evolution (Grimaldi and Engel 2004). Thus, glomerular arrangements, numbers, position of soma groups, neuron populations and more, differ across species. Several examples will be considered in the following section.

2.2.5. Glomerular Odor Responses

Stimulation with an odor leads to characteristic spatiotemporal glomerular activity patterns (Figure 2.2). Optical imaging of intracellular calcium concentration has been performed in bees (Galizia and Menzel 2001), in flies (Fiala et al. 2002; Wang et al. 2003), in moths (Carlsson et al. 2002; Galizia et al. 2000b; Skiri et al. 2004), and in ants (Galizia et al. 1999b). The conceptional similarity of these results in species other than Drosophila suggests that, also in these species, OSNs expressing the same OR are likely to converge generally onto a single glomerulus (an assertion that is commonly assumed, but not shown). Additional support comes from the observation that in the honeybee, Apis mellifera, the number of OR genes is close to 160, matching the number of glomeruli (Robertson and Wanner 2006). However, in the beetle, Tribolium, there are fewer glomeruli than the number of 341 receptor genes—more research is needed to investigate whether the same processing logic is implemented differently, or whether the logic itself differs (Engsontia et al. 2008).

FIGURE 2.2

Examples for odor-evoked activity in the fruit fly. (A) (left) Responses to the odor isoamyl acetate in OSNs on the antenna (their dendritic compartments) and in the antennal lobe (their axonal compartments) are shown left. The calcium sensor was expressed (more...)

Some glomeruli are narrowly tuned (i.e., respond to a single or, at best, very few substances). Thus, activity in OSNs innervating this glomerules is sufficient information for an animal to behave assuming that the substance is in the environment. Such a specialized system would be able to code for only as many odors as there are glomeruli (which is approximately 43 in the adult Drosophila). Other glomeruli are broadly tuned, and create a combinatorial code. Here, the information carried by individual glomeruli is ambiguous, but by a comparison across glomeruli, odor information becomes precise. Many OSNs are broadly tuned at high concentration, but may be narrowly tuned at concentrations several orders of magnitude lower (Pelz et al. 2004; Røstelien et al. 2000; Stensmyr et al. 2003). In their natural environment, animals experience odorants over a large range of concentrations. Thus, the low-concentration mode may be useful in some situations; here, even though only a single receptor may be active, the lack of activity in the remaining glomeruli would signal the low-concentration mode. Thus, even the low-concentration coding scheme has a combinatorial logic.

Labeled lines are often mentioned in the context of sexual pheromones. However, in most cases, these are also combinatorial signals. Indeed, most pheromones consist of blends of several substances, which activate several glomeruli, and extraction of the correct pheromone-blend information is done by a combinatorial analysis of the respective glomerular activities (Christensen and Hildebrand 2002; Galizia et al. 2000b; Shirokova et al. 2005). Closely related species can thus use the same substances for their species-specific sex-pheromone signals, as long as they use them in a species-specific concentration ratio.

Most glomerular responses are temporally structured, and inherit this property from OSNs: some are inhibited by odors, some show rebound excitation at the end of the stimulus, some fre for a long time irrespective of stimulus duration, others only fre for a very short time, and stop even if the stimulus continues (de Bruyne et al. 2001). This is in addition to the intrinsic temporal complexity that airborne odors always have (Murlis et al. 1992; Vetter et al. 2006). As a consequence, odor-evoked activity patterns are already temporally complex at the input level of the olfactory system. These temporal patterns are further shaped by neural networks within the ALs (see Section 2.2.14). Possibly, these temporal structures are used for odor analysis.

2.3. THE MUSHROOM BODIES (MBs)

MBs are multimodal structures in the insect protocerebrum. They are involved in learning (Davis 2004; Heisenberg 2003; Strausfeld and Gilbert 1992), and receive both olfactory and visual input in most insect species (Farris 2005; Strausfeld et al. 1998). Their names derive from the massive peduncles with large, cup-shaped protuberances, which are called the calyces. In hymenoptera, the calyces are subdivided into lip, collar, and basal ring, which correspond to three separate bands in the α lobe (or vertical lobe). In Drosophila, subdivisions from the calyces can be traced to a concentrically circular arrangement in the α/β lobe and to a layered structure in the α’/β’ lobes (Tanaka et al. 2004). The peduncles generally branch into two lobes, the vertical (α) lobe and the horizontal (β) lobe. In addition, in Drosophila, they form the α’ and the β’ lobes (Strausfeld et al. 2003). A third lobe, the γ lobe, is physically attached to the vertical lobe (the α lobe) in honeybees, but is morphologically distinct in Drosophila (Farris et al. 2004; Strausfeld 2002). The intrinsic neurons in the MBs are called KCs.

In the olfactory pathway, uniglomerular PNs form the input to MB calyces. In hymenoptera, this input is targeted at the lip and the basal ring of the calyces, while the intermediate area, the collar, receives input from the optic lobes (Gronenberg 1999, 2001). In Drosophila, each PN axon travels over large areas of the calyx, forming synapses with many intrinsic KCs (Marin et al. 2002; Wong et al. 2002). This is reminiscent of the situation in the mammalian olfactory cortex (Zou et al. 2005), and allows for a combinatorial readout of PN response patterns. PNs within the MB calyx region occupy concentric layers (Tanaka et al. 2004). PNs from identified glomeruli branch in a stereotypical manner within the MB calyces, and segregate in a functionally dictated way. For example, fruit odors and pheromone odors target other areas (Jefferis et al. 2007). On average, three uniglomerular PNs innervate each glomerulus, and these have the same projection pattern in MB and LP, suggesting that they are not functionally distinct (Wong et al. 2002).

Schematically, MB input can be described as a scaffold, with arrays of PN axons crossing arrays of KCs, and forming synapses with some, but not all KCs (Heisenberg 2003). In neural network language, this is ideal for combinatorial readout across PNs.

KC numbers differs widely among species: in honeybees, there are ~170,000 KCs in each hemisphere (Mobbs 1982; Witthöft 1967), Drosophila counts give ~2500 KCs (Stocker 1994). In adult cockroaches, the number is ~175,000 (Neder 1959), but juveniles have much smaller numbers (Farris and Strausfeld 2001), adult locusts have ~50,000 KCs (Farivar 2005). KC somata lie close to the MB calyces, in a densely packed manner. Their axons are long and thin and form the peduncles. The γ lobe is formed by the axons of the clawed KCs, the first subpopulation of KCs to occur in development (Farris et al. 2004; Mobbs 1982; Rybak and Menzel 1993; Strausfeld 2002). The name “clawed” derives from their claw-like dendritic shapes within the calyces.

KC morphology, pharmacology, and peptide expression shows a considerable variability across all species studied so far (Iwasaki et al. 1999; Sinakevitch et al. 2001; Strausfeld 2002; Strausfeld et al. 2000, 2003; Strausfeld and Li 1999a, 1999b). Glutamate labels a KC subpopulation of bees (Bicker et al. 1988). Aspartate, glutamate, and taurine immunocytochemistry label different KC populations in Drosophila (Strausfeld et al. 2003) and in cockroaches (Sinakevitch et al. 2001). In addition, in Drosophila, KCs produce NO (Schürmann 2000), but ACh and GABA are excluded as KC transmitters (Yusuyama et al. 2002).

2.4. OLFACTORY MEMORY AND PLASTICITY

2.5. THE LARVAL SYSTEM

In this chapter, we have only looked at the adult olfactory system in insects, and not at the maggot, for which there are several recent reviews that can be accessed (Cobb 1999; Heimbeck et al. 1999; Kreher et al. 2005; Marin et al. 2005; Scherer et al. 2003; Stocker 2001; Gerber and Stocker 2007). The main difference between the two systems is the greater simplicity in larvae, both in terms of cell numbers and organization, even though important principles are shared (Python and Stocker 2002a, 2002b). Odor perception is good in larvae, and odor learning is robust (Gerber et al. 2004a; Hendel et al. 2005; Scherer et al. 2003). The main pathway, OSN-PN-KC, is also realized in larvae, but the main difference is that—at least in Drosophila—each glomerulus only receives input from a single OSN axon, and is innervated only by a single PN (Kreher et al. 2005; Ramaekers et al. 2005). The larval MBs also share several features of their adult counterparts (Marin et al. 2005). In Drosophila larvae, there are 21 OSNs that express ~25 OR genes, of which only 13 are also expressed in adults (Kreher et al. 2005; Ramaekers et al. 2005), suggesting that the olfactory space of the larva is substantially different from the adult one.

ABBREVIATIONS

ACh:

acetylcholine

AL:

antennal lobe

ARM:

anesthesia-resistant memory

CS:

conditioned stimulus

GPCR:

G-protein-coupled receptor

KC:

Kenyon cell

LN:

local neurons

LP:

lateral protocerebrum

LTM:

long-term memory

MB:

mushroom bodies

MTM:

middle-term memory

NO:

nitric oxide

OBP:

odorant–binding protein

OR:

odorant receptor

OSN:

olfactory sensory neuron

PBP:

pheromone binding protein

SEG:

subesophageal ganglion

STM:

short-term memory

US:

unconditioned stimulus

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