Highly structured, partner-sex- and subject-sex-dependent cortical responses during social facial touch

Abstract

Touch is a fundamental aspect of mammalian social, parental and sexual behavior. Human affective touch is critical for healthy child development and shows great promise as a novel therapeutic strategy for mental disorders characterized by social dysfunction, such as anxiety, depression and autism spectrum disorder. However, despite our detailed knowledge about cortical processing of non-social touch, we still know very little about how social touch modulates cortical circuits. We investigated the activity patterns of single neurons (N = 1156) across five sensory and frontal cortical areas in both male and female rats (N = 28) engaging in naturalistic social facial touch with male and female conspecifics. We found that information about social touch is widely available across cortex. Besides touch, the sex of the interaction partner (a biologically significant feature) is a major determinant of single neuron activity, and across cortex we observed 25.7% touch and 11.9% sex-touch responses. Although all areas investigated had access to social touch and partner sex information, social touch modulated different cortical areas in different ways. Finally, we found that network activity patterns during social touch depend on both subject sex and partner sex. Interestingly, these sex-differences in network activity patterns were differences in response magnitude and would not be evident without single cell resolution. Our observations suggest that socio-sexual characteristics of touch (subject and partner sex) widely modulate cortical activity and need to be investigated with cellular resolution.