Multiscale chemogenetic dissection of fronto-temporal top-down regulation for object memory in primates

Toshiyuki Hirabayashi (), Yuji Nagai, Yuki Hori, Yukiko Hori, Kei Oyama, Koki Mimura, Naohisa Miyakawa, Haruhiko Iwaoki, Ken-ichi Inoue, Tetsuya Suhara, Masahiko Takada, Makoto Higuchi and Takafumi Minamimoto
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Toshiyuki Hirabayashi: National Institutes for Quantum Science and Technology
Yuji Nagai: National Institutes for Quantum Science and Technology
Yuki Hori: National Institutes for Quantum Science and Technology
Yukiko Hori: National Institutes for Quantum Science and Technology
Kei Oyama: National Institutes for Quantum Science and Technology
Koki Mimura: National Institutes for Quantum Science and Technology
Naohisa Miyakawa: National Institutes for Quantum Science and Technology
Haruhiko Iwaoki: National Institutes for Quantum Science and Technology
Ken-ichi Inoue: Kyoto University
Tetsuya Suhara: National Institutes for Quantum Science and Technology
Masahiko Takada: Kyoto University
Makoto Higuchi: National Institutes for Quantum Science and Technology
Takafumi Minamimoto: National Institutes for Quantum Science and Technology

Nature Communications, 2024, vol. 15, issue 1, 1-17

Abstract: Abstract Visual object memory is a fundamental element of various cognitive abilities, and the underlying neural mechanisms have been extensively examined especially in the anterior temporal cortex of primates. However, both macroscopic large-scale functional network in which this region is embedded and microscopic neuron-level dynamics of top-down regulation it receives for object memory remains elusive. Here, we identified the orbitofrontal node as a critical partner of the anterior temporal node for object memory by combining whole-brain functional imaging during rest and a short-term object memory task in male macaques. Focal chemogenetic silencing of the identified orbitofrontal node downregulated both the local orbitofrontal and remote anterior temporal nodes during the task, in association with deteriorated mnemonic, but not perceptual, performance. Furthermore, imaging-guided neuronal recordings in the same monkeys during the same task causally revealed that orbitofrontal top-down modulation enhanced stimulus-selective mnemonic signal in individual anterior temporal neurons while leaving bottom-up perceptual signal unchanged. Furthermore, similar activity difference was also observed between correct and mnemonic error trials before silencing, suggesting its behavioral relevance. These multifaceted but convergent results provide a multiscale causal understanding of dynamic top-down regulation of the anterior temporal cortex along the ventral fronto-temporal network underpinning short-term object memory in primates.

Date: 2024
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DOI: 10.1038/s41467-024-49570-w

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