Parallel processing by cortical inhibition enables context-dependent behavior

Kishore V. Kuchibhotla, Jonathan V. Gill, Grace W. Lindsay, Eleni S. Papadoyannis, Rachel E. Field, Tom A.Hindmarsh Sten, Kenneth D. Miller, Robert C. Froemke

Research output: Contribution to journalArticlepeer-review

Abstract

Physical features of sensory stimuli are fixed, but sensory perception is context dependent. The precise mechanisms that govern contextual modulation remain unknown. Here, we trained mice to switch between two contexts: passively listening to pure tones and performing a recognition task for the same stimuli. Two-photon imaging showed that many excitatory neurons in auditory cortex were suppressed during behavior, while some cells became more active. Whole-cell recordings showed that excitatory inputs were affected only modestly by context, but inhibition was more sensitive, with PV +, SOM +, and VIP + interneurons balancing inhibition and disinhibition within the network. Cholinergic modulation was involved in context switching, with cholinergic axons increasing activity during behavior and directly depolarizing inhibitory cells. Network modeling captured these findings, but only when modulation coincidently drove all three interneuron subtypes, ruling out either inhibition or disinhibition alone as sole mechanism for active engagement. Parallel processing of cholinergic modulation by cortical interneurons therefore enables context-dependent behavior.

Original languageEnglish (US)
Pages (from-to)62-71
Number of pages10
JournalNature neuroscience
Volume20
Issue number1
DOIs
StatePublished - Jan 1 2017
Externally publishedYes

ASJC Scopus subject areas

  • Neuroscience(all)

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