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

doi:10.1126/science.aaw5202

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 journal › Article › peer-review

287 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 language	American English
Article number	558
Journal	Science
Volume	365
Issue number	6453
DOIs	https://doi.org/10.1126/science.aaw5202
State	Published - 9 Aug 2019
Externally published	Yes

Bibliographical note

Funding Information:
K.D. is supported by the DARPA Neuro-FAST program, NIMH, NIDA, NSF, the Simons Foundation, the Wiegers Family Fund, the Nancy and James Grosfeld Foundation, the H.L. Snyder Medical Foundation, and the Samuel and Betsy Reeves Fund. S.G. was supported by the Burroughs-Wellcome, McKnight, Simons, and James S. McDonnell foundations. J.K. was supported by the Swartz Foundation. This work was also supported by a Simons LSRF fellowship (J.H.M.), the Japan Society for the Promotion of Science (18H04136, S.Y.), a Kwanjeong Fellowship and a Stanford Bio-X fellowship (Y.S.K.), Stanford Dean's fellowships (J.H.M. and T.A.M.), and an AP Giannini fellowship.

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

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Marshel, J. H., Kim, Y. S., Machado, T. A., Quirin, S., Benson, B., Kadmon, J., Raja, C., Chibukhchyan, A., Ramakrishnan, C., Inoue, M., Shane, J. C., McKnight, D. J., Yoshizawa, S., Kato, H. E., Ganguli, S., & Deisseroth, K. (2019). Cortical layer-specific critical dynamics triggering perception. Science, 365(6453), Article 558. https://doi.org/10.1126/science.aaw5202

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title = "Cortical layer-specific critical dynamics triggering perception",

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.",

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

note = "Funding Information: K.D. is supported by the DARPA Neuro-FAST program, NIMH, NIDA, NSF, the Simons Foundation, the Wiegers Family Fund, the Nancy and James Grosfeld Foundation, the H.L. Snyder Medical Foundation, and the Samuel and Betsy Reeves Fund. S.G. was supported by the Burroughs-Wellcome, McKnight, Simons, and James S. McDonnell foundations. J.K. was supported by the Swartz Foundation. This work was also supported by a Simons LSRF fellowship (J.H.M.), the Japan Society for the Promotion of Science (18H04136, S.Y.), a Kwanjeong Fellowship and a Stanford Bio-X fellowship (Y.S.K.), Stanford Dean's fellowships (J.H.M. and T.A.M.), and an AP Giannini fellowship. Publisher Copyright: {\textcopyright} 2019 American Association for the Advancement of Science. All rights reserved.",

year = "2019",

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doi = "10.1126/science.aaw5202",

language = "American English",

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AU - Marshel, James H.

AU - Kim, Yoon Seok

AU - Machado, Timothy A.

AU - Quirin, Sean

AU - Benson, Brandon

AU - Kadmon, Jonathan

AU - Raja, Cephra

AU - Chibukhchyan, Adelaida

AU - Ramakrishnan, Charu

AU - Inoue, Masatoshi

AU - Shane, Janelle C.

AU - McKnight, Douglas J.

AU - Yoshizawa, Susumu

AU - Kato, Hideaki E.

AU - Ganguli, Surya

AU - Deisseroth, Karl

N1 - Funding Information: K.D. is supported by the DARPA Neuro-FAST program, NIMH, NIDA, NSF, the Simons Foundation, the Wiegers Family Fund, the Nancy and James Grosfeld Foundation, the H.L. Snyder Medical Foundation, and the Samuel and Betsy Reeves Fund. S.G. was supported by the Burroughs-Wellcome, McKnight, Simons, and James S. McDonnell foundations. J.K. was supported by the Swartz Foundation. This work was also supported by a Simons LSRF fellowship (J.H.M.), the Japan Society for the Promotion of Science (18H04136, S.Y.), a Kwanjeong Fellowship and a Stanford Bio-X fellowship (Y.S.K.), Stanford Dean's fellowships (J.H.M. and T.A.M.), and an AP Giannini fellowship. Publisher Copyright: © 2019 American Association for the Advancement of Science. All rights reserved.

PY - 2019/8/9

Y1 - 2019/8/9

N2 - 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.

AB - 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.

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DO - 10.1126/science.aaw5202

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SN - 0036-8075

VL - 365

JO - Science

JF - Science

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ER -

Cortical layer-specific critical dynamics triggering perception

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