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Cortical layer-specific critical dynamics triggering perception

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

Science (American Association for the Advancement of Science), 2019-08, Vol.365 (6453) [Periódico revisado por pares]

United States: The American Association for the Advancement of Science

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Título:
Cortical layer-specific critical dynamics triggering perception
Autor: Marshel, James H ; Kim, Yoon Seok ; Machado, Timothy A ; Quirin, Sean ; Benson, Brandon ; Kadmon, Jonathan ; Raja, Cephra ; Chibukhchyan, Adelaida ; Ramakrishnan, Charu ; Inoue, Masatoshi ; Shane, Janelle C ; McKnight, Douglas J ; Yoshizawa, Susumu ; Kato, Hideaki E ; Ganguli, Surya ; Deisseroth, Karl
Assuntos: Activity patterns ; Animals ; Aquatic Organisms - genetics ; BASIC (programming language) ; Brain ; Calcium imaging ; Calcium ions ; Cells, Cultured ; Cerebral cortex ; Channelrhodopsins - genetics ; Circuits ; Coding ; Cortex (temporal) ; Crystal structure ; Driving ability ; Dynamics ; Electrical stimuli ; Firing pattern ; Gene mapping ; Genomes ; Gratings (spectra) ; Holography ; Holography - methods ; Laboratory animals ; Mammals ; Mapping ; Mice ; Microorganisms ; Molecular Imaging ; Neocortex - physiology ; Neocortex - ultrastructure ; Neuroimaging ; Neurons ; Neurons - physiology ; Neurosurgery ; Opsins - genetics ; Optogenetics ; Orientation ; Orientation - physiology ; Perception ; Photic Stimulation ; Photoelectric effect ; Photoelectric emission ; Population dynamics ; Representations ; Selectivity ; Stimulation ; Visual cortex ; Visual discrimination ; Visual observation ; Visual pathways ; Visual perception ; Visual Perception - genetics ; Visual Perception - physiology ; Visual stimuli
É parte de: Science (American Association for the Advancement of Science), 2019-08, Vol.365 (6453)
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These authors contributed equally to this work.
Author contributions: Y.S.K., H.E.K., S.Y., Ch.R., and K.D. initiated the opsin mining project that led to ChRmine identification, engineering, and optimization. Ch.R. prepared and transduced cell cultures and designed all viral vectors. Y.S.K. performed opsin electrophysiology. Y.S.K. and M.I. contributed 1P opsin characterization. Y.S.K. contributed 2P opsin characterization. J.H.M. and K.D. initiated the MultiSLM project. J.H.M., S.Q., J.C.S., D.J.M., and K.D. contributed to the design, manufacturing, and characterization of the MacroSLM. S.Q. and J.H.M. contributed the MultiSLM optics, optomechanics, and control software, and built the microscope. J.H.M. and A.C. contributed animal surgery protocols. J.H.M. and S.Q. contributed in vivo MultiSLM characterization experiments. J.H.M. and K.D. planned behavioral experiments with T.A.M. and S.Q. contributing. J.H.M., Ce.R., and A.C. performed behavioral training. Ce.R. and Ch.R. contributed the histology. J.H.M., T.A.M., S.Q., S.G., and K.D. analyzed behavioral and neural activity data. S.G. guided modeling and theory. T.A.M. and S.G. contributed classifier and state-space analyses. J.K., B.B., and S.G. contributed computational network modeling and theory. J.H.M., Y.S.K., T.A.M., S.Q., M.I., H.E.K., B.B., J.K., S.G., and K.D. designed and prepared the figures. J.H.M., Y.S.K., T.A.M., S.Q., S.G., and K.D. wrote the manuscript with contributions from all authors. K.D. supervised all aspects of the work.
Descrição: 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-orientation-selective 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.
Editor: United States: The American Association for the Advancement of Science
Idioma: Inglês

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Cortical layer-specific critical dynamics triggering perception

United States: The American Association for the Advancement of Science

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