Neural dynamics in the limbic system during male social behaviors

• Published in: Neuron (Cambridge, Mass.) Vol. 111; no. 20; pp. 3288 - 3306.e4
• Main Authors: Guo, Zhichao, Yin, Luping, Diaz, Veronica, Dai, Bing, Osakada, Takuya, Lischinsky, Julieta E., Chien, Jonathan, Yamaguchi, Takashi, Urtecho, Ashley, Tong, Xiaoyu, Chen, Zhe S., Lin, Dayu
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 18.10.2023
• Subjects: aggression; Aggression - physiology; Animals; estrogen receptor alpha expressing cells; limbic system; Limbic System - physiology; Male; Mice; multi-fiber photometric recording; Sexual Behavior, Animal - physiology; sexual behaviors; Social Behavior; multi-fiber photometric recording; estrogen receptor alpha expressing cells; limbic system; aggression; sexual behaviors; mice
• ISSN: 0896-6273; 1097-4199; 1097-4199
• DOI: 10.1016/j.neuron.2023.07.011

Sexual and aggressive behaviors are vital for species survival and individual reproductive success. Although many limbic regions have been found relevant to these behaviors, how social cues are represented across regions and how the network activity generates each behavior remains elusive. To answer these questions, we utilize multi-fiber photometry (MFP) to simultaneously record Ca2+ signals of estrogen receptor alpha (Esr1)-expressing cells from 13 limbic regions in male mice during mating and fighting. We find that conspecific sensory information and social action signals are widely distributed in the limbic system and can be decoded from the network activity. Cross-region correlation analysis reveals striking increases in the network functional connectivity during the social action initiation phase, whereas late copulation is accompanied by a “dissociated” network state. Based on the response patterns, we propose a mating-biased network (MBN) and an aggression-biased network (ABN) for mediating male sexual and aggressive behaviors, respectively. [Display omitted] •Intruder sex is widely represented in the expanded social behavior network (SBN)•Mating and fighting evoke distinct activation patterns in the expanded SBN•The network functional connectivity increases widely during social action initiation•Intromission and ejaculation are accompanied by “dissociated” brain states Guo et al. use multi-fiber photometry to simultaneously record Ca2+ activity from 13 brain regions in the expanded social behavior network during mating and fighting in male mice. The recordings reveal widespread activities in the network that evolve in distinct ways throughout male-male and male-female social interactions.