Cellular Mechanisms of Brain State-dependent Gain Modulation in Visual Cortex

Overview

Journal Nat Neurosci

Date 2013 Jul 23

PMID 23872595

Citations 340

Authors

Pierre-Olivier Polack

Jonathan Friedman

Peyman Golshani

Affiliations

Soon will be listed here.

Abstract

Visual cortical neurons fire at higher rates to visual stimuli during locomotion than during immobility, while maintaining orientation selectivity. The mechanisms underlying this change in gain are not understood. We performed whole-cell recordings from layer 2/3 and layer 4 visual cortical excitatory neurons and from parvalbumin-positive and somatostatin-positive inhibitory neurons in mice that were free to rest or run on a spherical treadmill. We found that the membrane potential of all cell types became more depolarized and (with the exception of somatostatin-positive interneurons) less variable during locomotion. Cholinergic input was essential for maintaining the unimodal membrane potential distribution during immobility, whereas noradrenergic input was necessary for the tonic depolarization associated with locomotion. Our results provide a mechanism for how neuromodulation controls the gain and signal-to-noise ratio of visual cortical neurons during changes in the state of vigilance.

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References

Fellous J, Rudolph M, Destexhe A, Sejnowski T . Synaptic background noise controls the input/output characteristics of single cells in an in vitro model of in vivo activity. Neuroscience. 2003; 122(3):811-29. PMC: 2928821. DOI: 10.1016/j.neuroscience.2003.08.027. View

Soma S, Shimegi S, Osaki H, Sato H . Cholinergic modulation of response gain in the primary visual cortex of the macaque. J Neurophysiol. 2011; 107(1):283-91. DOI: 10.1152/jn.00330.2011. View

Pologruto T, Sabatini B, Svoboda K . ScanImage: flexible software for operating laser scanning microscopes. Biomed Eng Online. 2003; 2:13. PMC: 161784. DOI: 10.1186/1475-925X-2-13. View

Wang Z, McCormick D . Control of firing mode of corticotectal and corticopontine layer V burst-generating neurons by norepinephrine, acetylcholine, and 1S,3R-ACPD. J Neurosci. 1993; 13(5):2199-216. PMC: 6576582. View

Haider B, Duque A, Hasenstaub A, Yu Y, McCormick D . Enhancement of visual responsiveness by spontaneous local network activity in vivo. J Neurophysiol. 2007; 97(6):4186-202. DOI: 10.1152/jn.01114.2006. View

Goard M, Dan Y . Basal forebrain activation enhances cortical coding of natural scenes. Nat Neurosci. 2009; 12(11):1444-9. PMC: 3576925. DOI: 10.1038/nn.2402. View

Buchanan J, Bilkey D . Transfer between atropine-induced spiking in the perirhinal cortex and electrical kindling of the amygdala. Brain Res. 1998; 771(1):63-70. DOI: 10.1016/s0006-8993(97)00778-6. View

Herrero J, Roberts M, Delicato L, Gieselmann M, Dayan P, Thiele A . Acetylcholine contributes through muscarinic receptors to attentional modulation in V1. Nature. 2008; 454(7208):1110-4. PMC: 2666819. DOI: 10.1038/nature07141. View

Metherate R, Cox C, Ashe J . Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine. J Neurosci. 1992; 12(12):4701-11. PMC: 6575759. View

10.

Gonchar Y, Wang Q, Burkhalter A . Multiple distinct subtypes of GABAergic neurons in mouse visual cortex identified by triple immunostaining. Front Neuroanat. 2008; 1:3. PMC: 2525923. DOI: 10.3389/neuro.05.003.2007. View

11.

Mueller D, Porter J, Quirk G . Noradrenergic signaling in infralimbic cortex increases cell excitability and strengthens memory for fear extinction. J Neurosci. 2008; 28(2):369-75. PMC: 6670514. DOI: 10.1523/JNEUROSCI.3248-07.2008. View

12.

Klinkenberg I, Sambeth A, Blokland A . Acetylcholine and attention. Behav Brain Res. 2010; 221(2):430-42. DOI: 10.1016/j.bbr.2010.11.033. View

13.

Rodriguez R, Kallenbach U, Singer W, Munk M . Stabilization of visual responses through cholinergic activation. Neuroscience. 2009; 165(3):944-54. DOI: 10.1016/j.neuroscience.2009.10.059. View

14.

Botly L, De Rosa E . Impaired visual search in rats reveals cholinergic contributions to feature binding in visuospatial attention. Cereb Cortex. 2011; 22(10):2441-53. DOI: 10.1093/cercor/bhr331. View

15.

Harris K, Thiele A . Cortical state and attention. Nat Rev Neurosci. 2011; 12(9):509-23. PMC: 3324821. DOI: 10.1038/nrn3084. View

16.

Ringach D . Spontaneous and driven cortical activity: implications for computation. Curr Opin Neurobiol. 2009; 19(4):439-44. PMC: 3319344. DOI: 10.1016/j.conb.2009.07.005. View

17.

Gentet L, Avermann M, Matyas F, Staiger J, Petersen C . Membrane potential dynamics of GABAergic neurons in the barrel cortex of behaving mice. Neuron. 2010; 65(3):422-35. DOI: 10.1016/j.neuron.2010.01.006. View

18.

McCormick D . Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity. Prog Neurobiol. 1992; 39(4):337-88. DOI: 10.1016/0301-0082(92)90012-4. View

19.

Gentet L, Kremer Y, Taniguchi H, Huang Z, Staiger J, Petersen C . Unique functional properties of somatostatin-expressing GABAergic neurons in mouse barrel cortex. Nat Neurosci. 2012; 15(4):607-12. DOI: 10.1038/nn.3051. View

20.

Sarter M, Bruno J . Cortical cholinergic inputs mediating arousal, attentional processing and dreaming: differential afferent regulation of the basal forebrain by telencephalic and brainstem afferents. Neuroscience. 2000; 95(4):933-52. DOI: 10.1016/s0306-4522(99)00487-x. View