A midbrain-thalamus-cortex circuit reorganizes cortical dynamics to initiate movement

Hidehiko K. Inagaki; Susu Chen; Margreet C. Ridder; Pankaj Sah; Nuo Li; Zidan Yang; Hana Hasanbegovic; Zhenyu Gao; Charles R. Gerfen; Karel Svoboda

doi:10.1016/j.cell.2022.02.006

A midbrain-thalamus-cortex circuit reorganizes cortical dynamics to initiate movement

Hidehiko K. Inagaki^*, Susu Chen, Margreet C. Ridder, Pankaj Sah, Nuo Li, Zidan Yang, Hana Hasanbegovic, Zhenyu Gao, Charles R. Gerfen, Karel Svoboda^*

^*Corresponding author for this work

Neurosciences

Research output: Contribution to journal › Article › Academic › peer-review

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Abstract

Motor behaviors are often planned long before execution but only released after specific sensory events. Planning and execution are each associated with distinct patterns of motor cortex activity. Key questions are how these dynamic activity patterns are generated and how they relate to behavior. Here, we investigate the multi-regional neural circuits that link an auditory “Go cue” and the transition from planning to execution of directional licking. Ascending glutamatergic neurons in the midbrain reticular and pedunculopontine nuclei show short latency and phasic changes in spike rate that are selective for the Go cue. This signal is transmitted via the thalamus to the motor cortex, where it triggers a rapid reorganization of motor cortex state from planning-related activity to a motor command, which in turn drives appropriate movement. Our studies show how midbrain can control cortical dynamics via the thalamus for rapid and precise motor behavior.

Original language	English
Pages (from-to)	1065-1081.e23
Journal	Cell
Volume	185
Issue number	6
DOIs	https://doi.org/10.1016/j.cell.2022.02.006
Publication status	Published - 17 Mar 2022

Bibliographical note

Funding Information:
We thank Svoboda and Inagaki lab members and B. Sauerbrei for comments on the manuscript; M.N. Economo and S. Romani for discussions; M. Inagaki for animal training; T. Harris, B. Barbarits, J. Colonell, B. Karsh, W. L. Sun, J.J. James, A. Liddell, and M. Pachitariu for help with silicon probe recordings and spike sorting; T. Wang for help with HCR; L. Narayan for help with high-speed videography; K. Ritola and H.A. Yi for viruses; and M. Mahn and O. Yizhar for GtACR plasmids. This work was funded by ZIA MH002487-32 (C.R.G.), NOW-Vidi and ERC-Stg grants (Z.G.), Australian National Health and Medical Research Council and the Australian Research Council : CE140100007 (P.S.), Searle Scholars Program (N.L. and H.K.I.), Klingenstein-Simons Fellowship (H.K.I.), NIH NS112312 (N.L.), Simons Collaboration on the Global Brain (K.S. and N.L.), Wellcome Trust (S.C.), Helen Hay Whitney Foundation (H.K.I.), Max Planck Florida Institute (H.K.I.), and Howard Hughes Medical Institute , including the Janelia Visitor Program (S.C., N.L., and K.S.).

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A midbrain-thalamus-cortex circuit reorganizesFinal published version, 24.8 MBLicence: CC BY-NC-ND

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title = "A midbrain-thalamus-cortex circuit reorganizes cortical dynamics to initiate movement",

abstract = "Motor behaviors are often planned long before execution but only released after specific sensory events. Planning and execution are each associated with distinct patterns of motor cortex activity. Key questions are how these dynamic activity patterns are generated and how they relate to behavior. Here, we investigate the multi-regional neural circuits that link an auditory “Go cue” and the transition from planning to execution of directional licking. Ascending glutamatergic neurons in the midbrain reticular and pedunculopontine nuclei show short latency and phasic changes in spike rate that are selective for the Go cue. This signal is transmitted via the thalamus to the motor cortex, where it triggers a rapid reorganization of motor cortex state from planning-related activity to a motor command, which in turn drives appropriate movement. Our studies show how midbrain can control cortical dynamics via the thalamus for rapid and precise motor behavior.",

author = "Inagaki, {Hidehiko K.} and Susu Chen and Ridder, {Margreet C.} and Pankaj Sah and Nuo Li and Zidan Yang and Hana Hasanbegovic and Zhenyu Gao and Gerfen, {Charles R.} and Karel Svoboda",

note = "Funding Information: We thank Svoboda and Inagaki lab members and B. Sauerbrei for comments on the manuscript; M.N. Economo and S. Romani for discussions; M. Inagaki for animal training; T. Harris, B. Barbarits, J. Colonell, B. Karsh, W. L. Sun, J.J. James, A. Liddell, and M. Pachitariu for help with silicon probe recordings and spike sorting; T. Wang for help with HCR; L. Narayan for help with high-speed videography; K. Ritola and H.A. Yi for viruses; and M. Mahn and O. Yizhar for GtACR plasmids. This work was funded by ZIA MH002487-32 (C.R.G.), NOW-Vidi and ERC-Stg grants (Z.G.), Australian National Health and Medical Research Council and the Australian Research Council : CE140100007 (P.S.), Searle Scholars Program (N.L. and H.K.I.), Klingenstein-Simons Fellowship (H.K.I.), NIH NS112312 (N.L.), Simons Collaboration on the Global Brain (K.S. and N.L.), Wellcome Trust (S.C.), Helen Hay Whitney Foundation (H.K.I.), Max Planck Florida Institute (H.K.I.), and Howard Hughes Medical Institute , including the Janelia Visitor Program (S.C., N.L., and K.S.). Publisher Copyright: {\textcopyright} 2022",

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AU - Ridder, Margreet C.

AU - Sah, Pankaj

AU - Li, Nuo

AU - Yang, Zidan

AU - Hasanbegovic, Hana

AU - Gao, Zhenyu

AU - Gerfen, Charles R.

AU - Svoboda, Karel

N1 - Funding Information: We thank Svoboda and Inagaki lab members and B. Sauerbrei for comments on the manuscript; M.N. Economo and S. Romani for discussions; M. Inagaki for animal training; T. Harris, B. Barbarits, J. Colonell, B. Karsh, W. L. Sun, J.J. James, A. Liddell, and M. Pachitariu for help with silicon probe recordings and spike sorting; T. Wang for help with HCR; L. Narayan for help with high-speed videography; K. Ritola and H.A. Yi for viruses; and M. Mahn and O. Yizhar for GtACR plasmids. This work was funded by ZIA MH002487-32 (C.R.G.), NOW-Vidi and ERC-Stg grants (Z.G.), Australian National Health and Medical Research Council and the Australian Research Council : CE140100007 (P.S.), Searle Scholars Program (N.L. and H.K.I.), Klingenstein-Simons Fellowship (H.K.I.), NIH NS112312 (N.L.), Simons Collaboration on the Global Brain (K.S. and N.L.), Wellcome Trust (S.C.), Helen Hay Whitney Foundation (H.K.I.), Max Planck Florida Institute (H.K.I.), and Howard Hughes Medical Institute , including the Janelia Visitor Program (S.C., N.L., and K.S.). Publisher Copyright: © 2022

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JF - Cell

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A midbrain-thalamus-cortex circuit reorganizes cortical dynamics to initiate movement

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