Cortical layer-specific critical dynamics triggering perception

James H. Marshel, Yoon Seok Kim, Timothy A. Machado, Sean Quirin, Brandon Benson, Jonathan Kadmon, Cephra Raja, Adelaida Chibukhchyan, Charu Ramakrishnan, Masatoshi Inoue, Janelle C. Shane, Douglas J. McKnight, Susumu Yoshizawa, Hideaki E. Kato, Surya Ganguli, Karl Deisseroth*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

331 Scopus citations

Abstract

Perceptual experiences may arise from neuronal activity patterns in mammalian neocortex. We probed mouse neocortex during visual discrimination using a red-shifted channelrhodopsin (ChRmine, discovered through structure-guided genome mining) alongside multiplexed multiphoton-holography (MultiSLM), achieving control of individually specified neurons spanning large cortical volumes with millisecond precision. Stimulating a critical number of stimulus-orientationselective neurons drove widespread recruitment of functionally related neurons, a process enhanced by (but not requiring) orientation-discrimination task learning. Optogenetic targeting of orientation-selective ensembles elicited correct behavioral discrimination. Cortical layer-specific dynamics were apparent, as emergent neuronal activity asymmetrically propagated from layer 2/3 to layer 5, and smaller layer 5 ensembles were as effective as larger layer 2/3 ensembles in eliciting orientation discrimination behavior. Population dynamics emerging after optogenetic stimulation both correctly predicted behavior and resembled natural internal representations of visual stimuli at cellular resolution over volumes of cortex.

Original languageAmerican English
Article number558
JournalScience
Volume365
Issue number6453
DOIs
StatePublished - 9 Aug 2019
Externally publishedYes

Bibliographical note

Publisher Copyright:
© 2019 American Association for the Advancement of Science. All rights reserved.

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