Encoding of social exploration by neural ensembles in the insular cortex

Isamu Miura; Masaaki Sato; Eric T N Overton; Nobuo Kunori; Junichi Nakai; Takakazu Kawamata; Nobuhiro Nakai; Toru Takumi

doi:10.1371/journal.pbio.3000584

Encoding of social exploration by neural ensembles in the insular cortex

PLoS Biol. 2020 Sep 21;18(9):e3000584. doi: 10.1371/journal.pbio.3000584. eCollection 2020 Sep.

Authors

Isamu Miura^{1

2}, Masaaki Sato^{1

3}, Eric T N Overton¹, Nobuo Kunori^{1

4}, Junichi Nakai^{3

5}, Takakazu Kawamata², Nobuhiro Nakai^{1

6}, Toru Takumi^{1

3

6}

Affiliations

¹ RIKEN Brain Science Institute, Wako, Saitama, Japan.
² Department of Neurosurgery, Tokyo Women's Medical University, Shinjuku, Tokyo, Japan.
³ Graduate School of Science and Engineering, Saitama University, Sakura, Saitama, Japan.
⁴ The National Institute of Advanced Industrial Science and Technology, Tsukuba, Ibaraki, Japan.
⁵ Division of Oral Physiology, Department of Oral Function and Morphology, Tohoku University Graduate School of Dentistry, Aoba, Sendai, Japan.
⁶ Department of Physiology and Cell Biology, Kobe University School of Medicine, Chuo, Kobe, Japan.

Abstract

The insular cortex (IC) participates in diverse complex brain functions, including social function, yet their cellular bases remain to be fully understood. Using microendoscopic calcium imaging of the agranular insular cortex (AI) in mice interacting with freely moving and restrained social targets, we identified 2 subsets of AI neurons-a larger fraction of "Social-ON" cells and a smaller fraction of "Social-OFF" cells-that change their activity in opposite directions during social exploration. Social-ON cells included those that represented social investigation independent of location and consisted of multiple subsets, each of which was preferentially active during exploration under a particular behavioral state or with a particular target of physical contact. These results uncover a previously unknown function of AI neurons that may act to monitor the ongoing status of social exploration while an animal interacts with unfamiliar conspecifics.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Behavior, Animal / physiology*
Cerebral Cortex / cytology
Cerebral Cortex / physiology*
Male
Mice
Social Behavior*

Grants and funding

This work was supported in part by KAKENHI (16H06316, 16H06463) from Japan Society for the Promotion of Science (JSPS) (https://www.jsps.go.jp/english/e-grants/index.html), Intramural Research Grant for Neurological and Psychiatric Disorders of NCNP (https://www.ncnp.go.jp/en/), the Takeda Science Foundation (https://www.takeda-sci.or.jp/index.html) to TT, KAKENHI (17H05985, 19H04942) to MS, and KAKENHI (15H05723) to JN. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.