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New Research, Cognition and Behavior

Stable neural population dynamics in the regression subspace for continuous and categorical task parameters in monkeys

He Chen, Kunimatsu Jun, Tomomichi Oya, Yuri Imaizumi, Yukiko Hori, Masayuki Matsumoto, Takafumi Minamimoto, Yuji Naya and Hiroshi Yamada
eNeuro 29 June 2023, ENEURO.0016-23.2023; https://doi.org/10.1523/ENEURO.0016-23.2023
He Chen
1School of Psychological and Cognitive Sciences, Peking University, No. 52, Haidian Road, Haidian District, Beijing 100805, China
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Kunimatsu Jun
2Division of Biomedical Science, Institute of Medicine, University of Tsukuba, 1-1-1 Tenno-dai, Tsukuba, Ibaraki 305-8577, Japan
3Transborder Medical Research Center, University of Tsukuba, 1-1-1 Tenno-dai, Tsukuba, Ibaraki 305-8577, Japan
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Tomomichi Oya
4The Brain and Mind Institute, University of Western Ontario, London, N6A 3K7, Canada
5Department of Physiology and Pharmacology, University of Western Ontario, N6A 3K7, London, Canada
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Yuri Imaizumi
6Medical Sciences, University of Tsukuba, 1-1-1 Tenno-dai, Tsukuba, Ibaraki 305-8577, Japan
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Yukiko Hori
7Department of Functional Brain Imaging, National Institutes for Quantum Science and Technology, 4-9-1 Anagawa, Inage-ku, Chiba 263-8555, Japan
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Masayuki Matsumoto
2Division of Biomedical Science, Institute of Medicine, University of Tsukuba, 1-1-1 Tenno-dai, Tsukuba, Ibaraki 305-8577, Japan
3Transborder Medical Research Center, University of Tsukuba, 1-1-1 Tenno-dai, Tsukuba, Ibaraki 305-8577, Japan
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Takafumi Minamimoto
7Department of Functional Brain Imaging, National Institutes for Quantum Science and Technology, 4-9-1 Anagawa, Inage-ku, Chiba 263-8555, Japan
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Yuji Naya
1School of Psychological and Cognitive Sciences, Peking University, No. 52, Haidian Road, Haidian District, Beijing 100805, China
8IDG/McGovern Institute for Brain Research at Peking University, No. 52, Haidian Road, Haidian District, Beijing 100805, China
9Beijing Key Laboratory of Behavior and Mental Health, Peking University, No. 52, Haidian Road, Haidian District, Beijing 100805, China
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Hiroshi Yamada
2Division of Biomedical Science, Institute of Medicine, University of Tsukuba, 1-1-1 Tenno-dai, Tsukuba, Ibaraki 305-8577, Japan
3Transborder Medical Research Center, University of Tsukuba, 1-1-1 Tenno-dai, Tsukuba, Ibaraki 305-8577, Japan
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Abstract

Neural population dynamics provide a key computational framework for understanding information processing in the sensory, cognitive, and motor functions of the brain. They systematically depict complex neural population activity, dominated by strong temporal dynamics as trajectory geometry in a low-dimensional neural space. However, neural population dynamics are poorly related to the conventional analytical framework of single-neuron activity, the rate-coding regime that analyzes firing-rate modulations using task parameters. To link the rate-coding and dynamical models, we developed a variant of state-space analysis in the regression subspace, which describes the temporal structures of neural modulations using continuous and categorical task parameters. In macaque monkeys, using two neural population datasets containing either of two standard task parameters, contiguous and categorical, we revealed that neural modulation structures are reliably captured by these task parameters in the regression subspace as trajectory geometry in a lower dimension. Furthermore, we combined the classical optimal-stimulus response analysis (usually used in rate-coding analysis) with the dynamical model and found that the most prominent modulation dynamics in the lower dimension were derived from these optimal responses. Using those analyses, we successfully extracted geometries for both task parameters that formed a straight geometry, suggesting that their functional relevance is characterized as a unidimensional feature in their neural modulation dynamics. Collectively, our approach bridges neural modulation in the rate-coding model and the dynamical system and provides researchers with a significant advantage in exploring the temporal structure of neural modulations for pre-existing datasets.

Significant statement

Our results differ from earlier studies and suggest that our state-space analysis in the regression subspace provides a mechanistic neural population structure for visual recognition of items when monkeys perceived continuous and categorical task parameters. The neural population dynamics obtained from different brain regions using different behavioral tasks were similar and may share some common underlying information processing in a neural network. Our approach provides a simple framework for incorporating the single-neuron approach into the dynamical model as a procedure for describing neural modulation dynamics in the brain. This analytic extension gives researchers a significant advantage in that all types of pre-existing data for single neuron activity are useful for easily exploring their dynamics in a low-dimensional neural modulation space.

  • dimensional reduction
  • monkey
  • neural population dynamics
  • regression subspace

Footnotes

  • The authors declare no competing interests.

  • This research was supported by JSPS KAKENHI (Grant number: JP 22H04832), the Research Foundation for the Electrotechnology of Chubu, JST Moonshot R&D JPMJMS2294 (H.Y.), and the National Natural Science Foundation of China (Grant 31871139) (Y.N.).

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Stable neural population dynamics in the regression subspace for continuous and categorical task parameters in monkeys
He Chen, Kunimatsu Jun, Tomomichi Oya, Yuri Imaizumi, Yukiko Hori, Masayuki Matsumoto, Takafumi Minamimoto, Yuji Naya, Hiroshi Yamada
eNeuro 29 June 2023, ENEURO.0016-23.2023; DOI: 10.1523/ENEURO.0016-23.2023

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Stable neural population dynamics in the regression subspace for continuous and categorical task parameters in monkeys
He Chen, Kunimatsu Jun, Tomomichi Oya, Yuri Imaizumi, Yukiko Hori, Masayuki Matsumoto, Takafumi Minamimoto, Yuji Naya, Hiroshi Yamada
eNeuro 29 June 2023, ENEURO.0016-23.2023; DOI: 10.1523/ENEURO.0016-23.2023
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Keywords

  • dimensional reduction
  • monkey
  • neural population dynamics
  • regression subspace

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