Multiple types of navigational information are independently encoded in the population activities of the dentate gyrus neurons

Author:

Murano Tomoyuki1ORCID,Nakajima Ryuichi1ORCID,Nakao Akito12ORCID,Hirata Nao1ORCID,Amemori Satoko13ORCID,Murakami Akira4,Kamitani Yukiyasu4ORCID,Yamamoto Jun5ORCID,Miyakawa Tsuyoshi1ORCID

Affiliation:

1. Division of Systems Medical Science, Center for Medical Science, Fujita Health University, Toyoake 470-1192, Japan

2. Department of Synthetic Chemistry and Biological Chemistry, Graduate School of Engineering, Kyoto University, Kyoto 615-8510, Japan

3. Institue for the Advanced Study of Human Biology, Kyoto University, Kyoto 606-8501, Japan

4. Graduate School of Informatics, Kyoto University, Kyoto 606-8501, Japan

5. Department of Psychiatry, University of Texas Southwestern Medical Center, Dallas, TX 75390

Abstract

The dentate gyrus (DG) plays critical roles in cognitive functions, such as learning, memory, and spatial coding, and its dysfunction is implicated in various neuropsychiatric disorders. However, it remains largely unknown how information is represented in this region. Here, we recorded neuronal activity in the DG using Ca 2+ imaging in freely moving mice and analyzed this activity using machine learning. The activity patterns of populations of DG neurons enabled us to successfully decode position, speed, and motion direction in an open field, as well as current and future location in a T-maze, and each individual neuron was diversely and independently tuned to these multiple information types. Our data also showed that each type of information is unevenly distributed in groups of DG neurons, and different types of information are independently encoded in overlapping, but different, populations of neurons. In alpha-calcium/calmodulin-dependent kinase II (αCaMKII) heterozygous knockout mice, which present deficits in spatial remote and working memory, the decoding accuracy of position in the open field and future location in the T-maze were selectively reduced. These results suggest that multiple types of information are independently distributed in DG neurons.

Funder

MEXT | Japan Society for the Promotion of Science

Japan Agency for Medical Research and Development

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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