Conjunctive processing of spatial border and locomotion in retrosplenial cortex during spatial navigation.

cognition integration retrosplenial cortex self‐motion spatial navigation

Journal

The Journal of physiology
ISSN: 1469-7793
Titre abrégé: J Physiol
Pays: England
ID NLM: 0266262

Informations de publication

Date de publication:
31 Aug 2024
Historique:
received: 04 03 2024
accepted: 24 07 2024
medline: 1 9 2024
pubmed: 1 9 2024
entrez: 31 8 2024
Statut: aheadofprint

Résumé

Spatial information and dynamic locomotor behaviours are equally important for achieving locomotor goals during spatial navigation. However, it remains unclear how spatial and locomotor information is integrated during the processing of self-initiated spatial navigation. Anatomically, the retrosplenial cortex (RSC) has reciprocal connections with brain regions related to spatial processing, including the hippocampus and para-hippocampus, and also receives inputs from the secondary motor cortex. In addition, RSC is functionally associated with allocentric and egocentric spatial targets and head-turning. So, RSC may be a critical region for integrating spatial and locomotor information. In this study, we first examined the role of RSC in spatial navigation using the Morris water maze and found that mice with inactivated RSC took a longer time and distance to reach their destination. Then, by imaging neuronal activity in freely behaving mice within two open fields of different sizes, we identified a large proportion of border cells, head-turning cells and locomotor speed cells in the superficial layer of RSC. Interestingly, some RSC neurons exhibited conjunctive coding for both spatial and locomotor signals. Furthermore, these conjunctive neurons showed higher prediction accuracy compared with simple spatial or locomotor neurons in special navigator scenes using the border, turning and positive-speed conjunctive cells. Our study reveals that the RSC is an important conjunctive brain region that processes spatial and locomotor information during spatial navigation. KEY POINTS: Retrosplenial cortex (RSC) is indispensable during spatial navigation, which was displayed by the longer time and distance of mice to reach their destination after the inactivation of RSC in a water maze. The superficial layer of RSC has a larger population of spatial-related border cells, and locomotion-related head orientation and speed cells; however, it has few place cells in two-dimensional spatial arenas. Some RSC neurons exhibited conjunctive coding for both spatial and locomotor signals, and the conjunctive neurons showed higher prediction accuracy compared with simple spatial or locomotor neurons in special navigation scenes. Our study reveals that the RSC is an important conjunctive brain region that processes both spatial and locomotor information during spatial navigation.

Identifiants

pubmed: 39216077
doi: 10.1113/JP286434
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : MOST | National Natural Science Foundation of China (NSFC)
ID : 32071097
Organisme : MOST | National Natural Science Foundation of China (NSFC)
ID : 31871056
Organisme : MOST | National Natural Science Foundation of China (NSFC)
ID : 61703365
Organisme : MOST | National Natural Science Foundation of China (NSFC)
ID : 91732302
Organisme : MOST | National Natural Science Foundation of China (NSFC)
ID : 81625006
Organisme : National Key R&D Program of China
ID : 2018YFC1005003
Organisme : MOE | Fundamental Research Funds for the Central Universities (Fundamental Research Fund for the Central Universities)
ID : 2019XZZX001-01-20
Organisme : MOE | Fundamental Research Funds for the Central Universities (Fundamental Research Fund for the Central Universities)
ID : 2018QN81008
Organisme : National Key Research and Development Program of the Ministry of Science and Technology of China
ID : 2020YFB1313500
Organisme : the MOE Frontier Science Center for Brain Science & Brain-Machine Integration, Zhejiang University

Informations de copyright

© 2024 The Authors. The Journal of Physiology © 2024 The Physiological Society.

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Auteurs

Hao Sun (H)

Department of Neurology of the Second Affiliated Hospital and Interdisciplinary Institute of Neuroscience and Technology, Zhejiang University School of Medicine, Hangzhou, China.
Nanhu Brain-computer Interface Institute, Hangzhou, China.
Key Laboratory of Biomedical Engineering of Ministry of Education, College of Biomedical Engineering and Instrument Science, Zhejiang University, Hangzhou, China.

Ruolan Cai (R)

Department of Neurology of the Second Affiliated Hospital and Interdisciplinary Institute of Neuroscience and Technology, Zhejiang University School of Medicine, Hangzhou, China.

Rui Li (R)

Department of Neurology of the Second Affiliated Hospital and Interdisciplinary Institute of Neuroscience and Technology, Zhejiang University School of Medicine, Hangzhou, China.

Mingxuan Li (M)

Shanghai Ping He School, Shanghai, China.

Lixia Gao (L)

Department of Neurology of the Second Affiliated Hospital and Interdisciplinary Institute of Neuroscience and Technology, Zhejiang University School of Medicine, Hangzhou, China.
Nanhu Brain-computer Interface Institute, Hangzhou, China.
Key Laboratory of Biomedical Engineering of Ministry of Education, College of Biomedical Engineering and Instrument Science, Zhejiang University, Hangzhou, China.
MOE Frontier Science Center for Brain Science and Brain-machine Integration, School of Brain Science and Brain Medicine, Zhejiang University, Hangzhou, China.

Xinjian Li (X)

Department of Neurology of the Second Affiliated Hospital and Interdisciplinary Institute of Neuroscience and Technology, Zhejiang University School of Medicine, Hangzhou, China.
MOE Frontier Science Center for Brain Science and Brain-machine Integration, School of Brain Science and Brain Medicine, Zhejiang University, Hangzhou, China.
Key Laboratory of Medical Neurobiology of Zhejiang Province, Hangzhou, China.

Classifications MeSH