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Research Articles, Behavioral/Cognitive

Mixed Selectivity Coding of Content-Temporal Detail by Dorsomedial Posterior Parietal Neurons

Lei Wang, Xufeng Zhou, Fu Zeng, Mingfeng Cao, Shuzhen Zuo, Jie Yang, Makoto Kusunoki, Huimin Wang, Yong-di Zhou, Aihua Chen and Sze Chai Kwok
Journal of Neuroscience 17 January 2024, 44 (3) e1677232023; https://doi.org/10.1523/JNEUROSCI.1677-23.2023
Lei Wang
1Shanghai Key Laboratory of Brain Functional Genomics, Affiliated Mental Health Center (ECNU), School of Psychology and Cognitive Science, East China Normal University, Shanghai 200062, China
2Phylo-Cognition Laboratory, Division of Natural and Applied Sciences, Duke Kunshan University, Duke Institute for Brain Sciences, Kunshan 215316, Jiangsu, China
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  • ORCID record for Lei Wang
Xufeng Zhou
1Shanghai Key Laboratory of Brain Functional Genomics, Affiliated Mental Health Center (ECNU), School of Psychology and Cognitive Science, East China Normal University, Shanghai 200062, China
2Phylo-Cognition Laboratory, Division of Natural and Applied Sciences, Duke Kunshan University, Duke Institute for Brain Sciences, Kunshan 215316, Jiangsu, China
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Fu Zeng
3Key Laboratory of Brain Functional Genomics (Ministry of Education), East China Normal University, Shanghai 200062, China
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Mingfeng Cao
2Phylo-Cognition Laboratory, Division of Natural and Applied Sciences, Duke Kunshan University, Duke Institute for Brain Sciences, Kunshan 215316, Jiangsu, China
4Whiting School of Engineering, department of biomedical engineering, Johns Hopkins University, Baltimore, Maryland 21218
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Shuzhen Zuo
1Shanghai Key Laboratory of Brain Functional Genomics, Affiliated Mental Health Center (ECNU), School of Psychology and Cognitive Science, East China Normal University, Shanghai 200062, China
5Laboratory for Circuit and Behavioral Physiology, RIKEN Center for Brain Science, Wako-shi, Saitama 351-0198, Japan
6Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, Tokyo 153-8902, Japan
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Jie Yang
1Shanghai Key Laboratory of Brain Functional Genomics, Affiliated Mental Health Center (ECNU), School of Psychology and Cognitive Science, East China Normal University, Shanghai 200062, China
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Makoto Kusunoki
7MRC Cognition and Brain Sciences Unit, University of Cambridge, Cambridge CB2 7EF, United Kingdom
8Department of Experimental Psychology, University of Oxford, Oxford OX2 6GG, United Kingdom
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Huimin Wang
1Shanghai Key Laboratory of Brain Functional Genomics, Affiliated Mental Health Center (ECNU), School of Psychology and Cognitive Science, East China Normal University, Shanghai 200062, China
3Key Laboratory of Brain Functional Genomics (Ministry of Education), East China Normal University, Shanghai 200062, China
9Shanghai Changning Mental Health Center, Shanghai 200335, China
10NYU-ECNU Institute of Brain and Cognitive Science at NYU Shanghai, Shanghai 200062, China
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Yong-di Zhou
11School of Psychology, Shenzhen University, Shenzhen 518052, China
12Department of Neurosurgery, Johns Hopkins University, Baltimore, Maryland 21218
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Aihua Chen
3Key Laboratory of Brain Functional Genomics (Ministry of Education), East China Normal University, Shanghai 200062, China
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Sze Chai Kwok
1Shanghai Key Laboratory of Brain Functional Genomics, Affiliated Mental Health Center (ECNU), School of Psychology and Cognitive Science, East China Normal University, Shanghai 200062, China
2Phylo-Cognition Laboratory, Division of Natural and Applied Sciences, Duke Kunshan University, Duke Institute for Brain Sciences, Kunshan 215316, Jiangsu, China
3Key Laboratory of Brain Functional Genomics (Ministry of Education), East China Normal University, Shanghai 200062, China
9Shanghai Changning Mental Health Center, Shanghai 200335, China
13State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing 100875, China
14Shanghai Key Laboratory of Magnetic Resonance, East China Normal University, Shanghai 200062, China
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Abstract

The dorsomedial posterior parietal cortex (dmPPC) is part of a higher-cognition network implicated in elaborate processes underpinning memory formation, recollection, episode reconstruction, and temporal information processing. Neural coding for complex episodic processing is however under-documented. Here, we recorded extracellular neural activities from three male rhesus macaques (Macaca mulatta) and revealed a set of neural codes of “neuroethogram” in the primate parietal cortex. Analyzing neural responses in macaque dmPPC to naturalistic videos, we discovered several groups of neurons that are sensitive to different categories of ethogram items, low-level sensory features, and saccadic eye movement. We also discovered that the processing of category and feature information by these neurons is sustained by the accumulation of temporal information over a long timescale of up to 30 s, corroborating its reported long temporal receptive windows. We performed an additional behavioral experiment with additional two male rhesus macaques and found that saccade-related activities could not account for the mixed neuronal responses elicited by the video stimuli. We further observed monkeys’ scan paths and gaze consistency are modulated by video content. Taken altogether, these neural findings explain how dmPPC weaves fabrics of ongoing experiences together in real time. The high dimensionality of neural representations should motivate us to shift the focus of attention from pure selectivity neurons to mixed selectivity neurons, especially in increasingly complex naturalistic task designs.

  • dorsomedial posterior parietal cortex
  • information accumulation
  • mixed selective representation
  • neuroethology
  • scan path and gaze consistency
  • temporal receptive window

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The Journal of Neuroscience: 44 (3)
Journal of Neuroscience
Vol. 44, Issue 3
17 Jan 2024
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Mixed Selectivity Coding of Content-Temporal Detail by Dorsomedial Posterior Parietal Neurons
Lei Wang, Xufeng Zhou, Fu Zeng, Mingfeng Cao, Shuzhen Zuo, Jie Yang, Makoto Kusunoki, Huimin Wang, Yong-di Zhou, Aihua Chen, Sze Chai Kwok
Journal of Neuroscience 17 January 2024, 44 (3) e1677232023; DOI: 10.1523/JNEUROSCI.1677-23.2023

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Mixed Selectivity Coding of Content-Temporal Detail by Dorsomedial Posterior Parietal Neurons
Lei Wang, Xufeng Zhou, Fu Zeng, Mingfeng Cao, Shuzhen Zuo, Jie Yang, Makoto Kusunoki, Huimin Wang, Yong-di Zhou, Aihua Chen, Sze Chai Kwok
Journal of Neuroscience 17 January 2024, 44 (3) e1677232023; DOI: 10.1523/JNEUROSCI.1677-23.2023
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Keywords

  • dorsomedial posterior parietal cortex
  • information accumulation
  • mixed selective representation
  • neuroethology
  • scan path and gaze consistency
  • temporal receptive window

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