Visual experience and subsequent sleep induce sequential plastic changes in putative inhibitory and excitatory cortical neurons

Sara J Aton; Christopher Broussard; Michelle Dumoulin; Julie Seibt; Adam Watson; Tammi Coleman; Marcos G Frank

doi:10.1073/pnas.1208093110

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Visual experience and subsequent sleep induce sequential plastic changes in putative inhibitory and excitatory cortical neurons

Journal article

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Visual experience and subsequent sleep induce sequential plastic changes in putative inhibitory and excitatory cortical neurons

Sara J Aton, Christopher Broussard, Michelle Dumoulin, Julie Seibt, Adam Watson, Tammi Coleman and Marcos G Frank

Proceedings of the National Academy of Sciences - PNAS, Vol.110(8), pp.3101-3106

02/19/2013

DOI: https://doi.org/10.1073/pnas.1208093110

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https://hdl.handle.net/2376/103264

PMCID: PMC3581875

PMID: 23300282

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Abstract

GABA

striate cortex

Biological Sciences

critical period

non-REM sleep

REM sleep

Ocular dominance plasticity in the developing primary visual cortex is initiated by monocular deprivation (MD) and consolidated during subsequent sleep. To clarify how visual experience and sleep affect neuronal activity and plasticity, we continuously recorded extragranular visual cortex fast-spiking (FS) interneurons and putative principal (i.e., excitatory) neurons in freely behaving cats across periods of waking MD and post-MD sleep. Consistent with previous reports in mice, MD induces two related changes in FS interneurons: a response shift in favor of the closed eye and depression of firing. Spike-timing–dependent depression of open-eye–biased principal neuron inputs to FS interneurons may mediate these effects. During post-MD nonrapid eye movement sleep, principal neuron firing increases and becomes more phase-locked to slow wave and spindle oscillations. Ocular dominance (OD) shifts in favor of open-eye stimulation—evident only after post-MD sleep—are proportional to MD-induced changes in FS interneuron activity and to subsequent sleep-associated changes in principal neuron activity. OD shifts are greatest in principal neurons that fire 40–300 ms after neighboring FS interneurons during post-MD slow waves. Based on these data, we propose that MD-induced changes in FS interneurons play an instructive role in ocular dominance plasticity, causing disinhibition among open-eye–biased principal neurons, which drive plasticity throughout the visual cortex during subsequent sleep.

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Title: Visual experience and subsequent sleep induce sequential plastic changes in putative inhibitory and excitatory cortical neurons
Creators: Sara J Aton - Departments of
Christopher Broussard - Psychology
Michelle Dumoulin - Departments of
Julie Seibt - Departments of
Adam Watson - Departments of
Tammi Coleman - Departments of
Marcos G Frank - Departments of
Publication Details: Proceedings of the National Academy of Sciences - PNAS, Vol.110(8), pp.3101-3106
Academic Unit: Biomedical Sciences, Department of
Publisher: National Academy of Sciences
Identifiers: 99900546510001842
Language: English
Resource Type: Journal article