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

Author:

Sun Hao123,Cai Ruolan1,Li Rui1,Li Mingxuan4,Gao Lixia1235,Li Xinjian156ORCID

Affiliation:

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

2. Nanhu Brain‐computer Interface Institute Hangzhou China

3. Key Laboratory of Biomedical Engineering of Ministry of Education, College of Biomedical Engineering and Instrument Science Zhejiang University Hangzhou China

4. Shanghai Ping He School Shanghai China

5. MOE Frontier Science Center for Brain Science and Brain‐machine Integration, School of Brain Science and Brain Medicine Zhejiang University Hangzhou China

6. Key Laboratory of Medical Neurobiology of Zhejiang Province Hangzhou China

Abstract

AbstractSpatial 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. imageKey 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.

Funder

National Key Research and Development Program of China

Publisher

Wiley

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