Fast modulation of visual perception by basal forebrain cholinergic neurons

Nat Neurosci. 2013 Dec;16(12):1857-1863. doi: 10.1038/nn.3552. Epub 2013 Oct 27.

Abstract

The basal forebrain provides the primary source of cholinergic input to the cortex, and it has a crucial function in promoting wakefulness and arousal. However, whether rapid changes in basal forebrain neuron spiking in awake animals can dynamically influence sensory perception is unclear. Here we show that basal forebrain cholinergic neurons rapidly regulate cortical activity and visual perception in awake, behaving mice. Optogenetic activation of the cholinergic neurons or their V1 axon terminals improved performance of a visual discrimination task on a trial-by-trial basis. In V1, basal forebrain activation enhanced visual responses and desynchronized neuronal spiking; these changes could partly account for the behavioral improvement. Conversely, optogenetic basal forebrain inactivation decreased behavioral performance, synchronized cortical activity and impaired visual responses, indicating the importance of cholinergic activity in normal visual processing. These results underscore the causal role of basal forebrain cholinergic neurons in fast, bidirectional modulation of cortical processing and sensory perception.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Acetylcholine / metabolism
  • Action Potentials / drug effects
  • Action Potentials / physiology*
  • Animals
  • Archaeal Proteins / metabolism
  • Channelrhodopsins
  • Cholera Toxin / metabolism
  • Choline O-Acetyltransferase / genetics
  • Cholinergic Neurons / physiology*
  • Exercise Test
  • Glutamate Decarboxylase / genetics
  • Halorhodopsins / metabolism
  • Luminescent Proteins / genetics
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Neural Pathways / physiology
  • Photic Stimulation
  • Prosencephalon / cytology*
  • RNA, Untranslated / genetics
  • Visual Perception / physiology*

Substances

  • Archaeal Proteins
  • Channelrhodopsins
  • Gt(ROSA)26Sor non-coding RNA, mouse
  • Halorhodopsins
  • Luminescent Proteins
  • RNA, Untranslated
  • archaerhodopsin protein, Archaea
  • Cholera Toxin
  • Choline O-Acetyltransferase
  • Glutamate Decarboxylase
  • glutamate decarboxylase 2
  • Acetylcholine