Social experience alters socially induced serotonergic fluctuations in the inferior colliculus

Abstract

Past social experience and current social context shape the responses of animals to social signals. The serotonergic system is one potential mechanism by which both experiential and contextual factors could be conveyed to sensory systems, such as the auditory system, for multiple reasons. ) Many features of the serotonergic system are sensitive to social experience.) Elevations in serotonergic activity are triggered by social partners, and variations in socially triggered serotonergic responses reflect behavioral differences among social encounters. ) Serotonin is an auditory neuromodulator, altering how auditory neurons respond to sounds including conspecific vocalizations. In this study, we tested how social experience influences the socially triggered serotonergic response in the inferior colliculus, an auditory midbrain region with an important role in vocalization processing. We used carbon fiber voltammetry to measure serotonin during social interactions of male mice () from different social backgrounds: 4 weeks of grouped or individual housing. When paired with an unfamiliar male, both group-housed and individually housed males demonstrated elevations in serotonin; however, individually housed males exhibited socially triggered serotonergic responses with delayed time courses compared with the group-housed males. Furthermore, group-housed males displayed previously described correlations between the socially triggered serotonergic response and behaviors such as social investigation. In contrast, individually housed males did not show these serotonin-behavior relationships. These results suggest that social experience gained via social housing may shape the ability of the central serotonergic system to encode social context in sensory regions. We demonstrate that past social experience influences the fidelity with which the serotonergic system represents social context in an auditory region. Social experience altered the time course of socially triggered serotonergic responses and changed how the serotonergic system reflects behavioral variations among social encounters of the same context. These findings are significant to the study of communication, suggesting that centralized neuromodulatory systems potentially convey integrated information regarding past experience and current context to primary sensory regions.

Silence, Solitude, and Serotonin: Neural Mechanisms Linking Hearing Loss and Social Isolation

“…Not only did social isolation influence the timing of the serotonergic response to a social partner, but it also affected the relationship between serotonergic activity in the IC and behaviors displayed during the social encounter. For example, there was a negative relationship between overall serotonergic activity and behavioral inactivity across interactions between socially housed males, which replicated a finding from a previous study [ 62 , 147 ] ( Figure 2 B). Socially housed males also showed a positive correlation between serotonergic activity and social investigation behavior.…”

“…Whether social isolation reconfigures this pathway is just beginning to be explored. Two studies [ 88 , 147 ] suggest that social impoverishment modifies serotonergic anatomy and function in the auditory system at the level of the midbrain—the IC. In both studies, the effects of social isolation were investigated by manipulating the chronic social housing conditions of postweaning mice, a manipulation with behavioral and physiological consequences that include effects on the serotonergic system in non-auditory regions of the brain (see below).…”

“…Although there is no effect of social isolation in males on the density of SERT+ projections to the IC, depriving male mice of social contact does alter directly measured serotonergic activity in the IC triggered by the presence of a social partner [ 147 ]. In this study, despite demonstrating differences in the mean durations of social investigatory behavior and behavioral activity, socially isolated and social housed adult male mice did not differ in mean amplitudes in serotonergic activity during social interaction.…”

“…( ii ) No correlation between serotonin and inactivity is seen for individually housed males. Adapted from reference [ 147 ] with permission from the authors.…”

Male mice adjust courtship behavior in response to female multimodal signals

“…The house mouse (Mus musculus) is a highly social species [10,11] that uses both acoustic [12][13][14][15] and chemical [16][17][18][19][20] signals to communicate with conspecifics. For example, males produce ultrasonic vocalizations (USVs) that may function as courtship signals to females [21][22][23][24].…”