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  2. Chemogenetic sensory fMRI reveals behaviorally relevant bidirectional changes in primate somatosensory network

Chemogenetic sensory fMRI reveals behaviorally relevant bidirectional changes in primate somatosensory network

  • Neuron. 2021 Oct 20;109(20):3312-3322.e5. doi: 10.1016/j.neuron.2021.08.032.
Toshiyuki Hirabayashi 1 Yuji Nagai 2 Yukiko Hori 2 Ken-Ichi Inoue 3 Ichio Aoki 4 Masahiko Takada 5 Tetsuya Suhara 2 Makoto Higuchi 2 Takafumi Minamimoto 2
Affiliations

Affiliations

  • 1 Department of Functional Brain Imaging, National Institutes for Quantum and Radiological Sciences and Technology, Anagawa 4-9-1, Inage-ku, Chiba, Japan. Electronic address: hirabayashi.toshiyuki@qst.go.jp.
  • 2 Department of Functional Brain Imaging, National Institutes for Quantum and Radiological Sciences and Technology, Anagawa 4-9-1, Inage-ku, Chiba, Japan.
  • 3 Systems Neuroscience Section, Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan; PRESTO, Japan Science and Technology Agency, Kawaguchi, Saitama, Japan.
  • 4 Department of Molecular Imaging and Theranostics, National Institutes for Quantum and Radiological Sciences and Technology, Anagawa 4-9-1, Inage-ku, Chiba, Japan.
  • 5 Systems Neuroscience Section, Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan.
Abstract

Concurrent genetic neuromodulation and functional magnetic resonance imaging (fMRI) in primates has provided a valuable opportunity to assess the modified brain-wide operation in the resting state. However, its application to link the network operation with behavior still remains challenging. Here, we combined chemogenetic silencing of the primary somatosensory cortex (SI) with tactile fMRI and related behaviors in macaques. Focal chemogenetic silencing of functionally identified SI hand region impaired grasping behavior. The same silencing also attenuated hand stimulation-evoked fMRI signal at both the local silencing site and the anatomically and/or functionally connected downstream grasping network, suggesting altered network operation underlying the induced behavioral impairment. Furthermore, the hand region silencing unexpectedly disinhibited foot representation with accompanying behavioral hypersensitization. These results demonstrate that focal chemogenetic silencing with sensory fMRI in macaques unveils bidirectional network changes to generate multifaceted behavioral impairments, thereby opening a pivotal window toward elucidating the causal network operation underpinning higher brain functions in primates.

Keywords

chemogenetics; fMRI; macaque; neuromodulation; somatosensory.

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