Cholinergic suppression of visual responses in primate V1 is mediated by GABAergic inhibition

Anita A. Disney, Chiye Aoki, Michael Hawken

Research output: Contribution to journalArticle

Abstract

Acetylcholine (ACh) has been implicated in selective attention. To understand the local circuit action of ACh, we iontophoresed cholinergic agonists into the primate primary visual cortex (V1) while presenting optimal visual stimuli. Consistent with our previous anatomical studies showing that GABAergic neurons in V1 express ACh receptors to a greater extent than do excitatory neurons, we observed suppressed visual responses in 36% of recorded neurons outside V1's primary thalamorecipient layer (4c). This suppression is blocked by the GABAA receptor antagonist gabazine. Within layer 4c, ACh release produces a response gain enhancement (Disney AA, Aoki C, Hawken MJ. Neuron 56: 701-713, 2007); elsewhere, ACh suppresses response gain by strengthening inhibition. Our finding contrasts with the observation that the dominant mechanism of suppression in the neocortex of rats is reduced glutamate release. We propose that in primates, distinct cholinergic receptor subtypes are recruited on specific cell types and in specific lamina to yield opposing modulatory effects that together increase neurons' responsiveness to optimal stimuli without changing tuning width.

Original languageEnglish (US)
Pages (from-to)1907-1923
Number of pages17
JournalJournal of Neurophysiology
Volume108
Issue number7
DOIs
StatePublished - Oct 1 2012

Fingerprint

Cholinergic Agents
Primates
Acetylcholine
Neurons
Cholinergic Receptors
GABA-A Receptor Antagonists
GABAergic Neurons
Cholinergic Agonists
Neocortex
Visual Cortex
Glutamic Acid

Keywords

  • Muscarinic receptor
  • Neuromodulation
  • Visual cortex

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

Cholinergic suppression of visual responses in primate V1 is mediated by GABAergic inhibition. / Disney, Anita A.; Aoki, Chiye; Hawken, Michael.

In: Journal of Neurophysiology, Vol. 108, No. 7, 01.10.2012, p. 1907-1923.

Research output: Contribution to journalArticle

@article{acb52c7597e44e0ab948673cc78659de,
title = "Cholinergic suppression of visual responses in primate V1 is mediated by GABAergic inhibition",
abstract = "Acetylcholine (ACh) has been implicated in selective attention. To understand the local circuit action of ACh, we iontophoresed cholinergic agonists into the primate primary visual cortex (V1) while presenting optimal visual stimuli. Consistent with our previous anatomical studies showing that GABAergic neurons in V1 express ACh receptors to a greater extent than do excitatory neurons, we observed suppressed visual responses in 36{\%} of recorded neurons outside V1's primary thalamorecipient layer (4c). This suppression is blocked by the GABAA receptor antagonist gabazine. Within layer 4c, ACh release produces a response gain enhancement (Disney AA, Aoki C, Hawken MJ. Neuron 56: 701-713, 2007); elsewhere, ACh suppresses response gain by strengthening inhibition. Our finding contrasts with the observation that the dominant mechanism of suppression in the neocortex of rats is reduced glutamate release. We propose that in primates, distinct cholinergic receptor subtypes are recruited on specific cell types and in specific lamina to yield opposing modulatory effects that together increase neurons' responsiveness to optimal stimuli without changing tuning width.",
keywords = "Muscarinic receptor, Neuromodulation, Visual cortex",
author = "Disney, {Anita A.} and Chiye Aoki and Michael Hawken",
year = "2012",
month = "10",
day = "1",
doi = "10.1152/jn.00188.2012",
language = "English (US)",
volume = "108",
pages = "1907--1923",
journal = "Journal of Neurophysiology",
issn = "0022-3077",
publisher = "American Physiological Society",
number = "7",

}

TY - JOUR

T1 - Cholinergic suppression of visual responses in primate V1 is mediated by GABAergic inhibition

AU - Disney, Anita A.

AU - Aoki, Chiye

AU - Hawken, Michael

PY - 2012/10/1

Y1 - 2012/10/1

N2 - Acetylcholine (ACh) has been implicated in selective attention. To understand the local circuit action of ACh, we iontophoresed cholinergic agonists into the primate primary visual cortex (V1) while presenting optimal visual stimuli. Consistent with our previous anatomical studies showing that GABAergic neurons in V1 express ACh receptors to a greater extent than do excitatory neurons, we observed suppressed visual responses in 36% of recorded neurons outside V1's primary thalamorecipient layer (4c). This suppression is blocked by the GABAA receptor antagonist gabazine. Within layer 4c, ACh release produces a response gain enhancement (Disney AA, Aoki C, Hawken MJ. Neuron 56: 701-713, 2007); elsewhere, ACh suppresses response gain by strengthening inhibition. Our finding contrasts with the observation that the dominant mechanism of suppression in the neocortex of rats is reduced glutamate release. We propose that in primates, distinct cholinergic receptor subtypes are recruited on specific cell types and in specific lamina to yield opposing modulatory effects that together increase neurons' responsiveness to optimal stimuli without changing tuning width.

AB - Acetylcholine (ACh) has been implicated in selective attention. To understand the local circuit action of ACh, we iontophoresed cholinergic agonists into the primate primary visual cortex (V1) while presenting optimal visual stimuli. Consistent with our previous anatomical studies showing that GABAergic neurons in V1 express ACh receptors to a greater extent than do excitatory neurons, we observed suppressed visual responses in 36% of recorded neurons outside V1's primary thalamorecipient layer (4c). This suppression is blocked by the GABAA receptor antagonist gabazine. Within layer 4c, ACh release produces a response gain enhancement (Disney AA, Aoki C, Hawken MJ. Neuron 56: 701-713, 2007); elsewhere, ACh suppresses response gain by strengthening inhibition. Our finding contrasts with the observation that the dominant mechanism of suppression in the neocortex of rats is reduced glutamate release. We propose that in primates, distinct cholinergic receptor subtypes are recruited on specific cell types and in specific lamina to yield opposing modulatory effects that together increase neurons' responsiveness to optimal stimuli without changing tuning width.

KW - Muscarinic receptor

KW - Neuromodulation

KW - Visual cortex

UR - http://www.scopus.com/inward/record.url?scp=84867188344&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84867188344&partnerID=8YFLogxK

U2 - 10.1152/jn.00188.2012

DO - 10.1152/jn.00188.2012

M3 - Article

VL - 108

SP - 1907

EP - 1923

JO - Journal of Neurophysiology

JF - Journal of Neurophysiology

SN - 0022-3077

IS - 7

ER -