Subject sex and partner sex modulate social touch responses across multiple cortical areas

Abstract

Touch is a fundamental aspect of social, parental and sexual behavior. Despite our detailed knowledge about cortical processing of non-social touch, we still know little about how social touch cortical circuits. We investigated neural activity across five frontal, motor and sensory cortical areas in rats engaging in naturalistic social facial touch. Information about social touch and the sex of the interaction partner (a biologically significant feature) is a major determinant of cortical activity. 25.3% of units were modulated during social touch and 8.3% of units displayed 'sex-touch' responses (responded differently, depending on the sex of the interaction partner). Single-unit responses were part of a structured, partner-sex-and, in some cases, subject-sex-dependent population response. Simulations suggest that a change in inhibitory drive might underlie these population dynamics. 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. Single cortical neurons signal social touch and partner sex= 1 = −1 Figure 1 | Diverse cortical responses and variable behavioral timing during social facial touch. (a) The social gap paradigm 27 . Rats separated on two platforms will reach across the gap to engage in social facial touch. In social facial touch, rats align their snouts and whisk to palpate each other's face with their mystacial vibrissae. We recorded the behavior of male and female rats by videography from above in visual darkness under infrared illumination 29,33,34 . (b) Anatomical location of vibrissa motor cortex ('VMC'the primary motor representation of the mystacial vibrissae), cingulate cortex ('ACC'a putative homolog of human/primate anterior cingulate cortex), prelimbic cortex ('PrL'a putative homolog of human/primate medial prefrontal cortex), barrel cortex ('S1'the primary somatosensory representation of the mystacial vibrissae) and auditory cortex ('A1'). (c) Example peri-stimulus time histograms (PSTHs) of touch-activated single neurons (Wilcoxon signed-rank test), aligned to the first whisker-to-whisker touch in each social touch episode. Raster plot above shows single trials, black dots indicate single spikes and vertical line indicates beginning of social facial touch. Black line below indicates mean firing rate, smoothed with an Alpha kernel ( = 75 ms), shaded area indicates s.e.m. (d) Example PSTHs of touch-suppressed single neurons (Wilcoxon signed-rank test), aligned to the first whisker-to-whisker touch in each social touch episode. Same plotting convention as in (c). (e) Top: Histograms of touch duration (red) and inter-touch-time (blue) of social facial touch episodes. The time axes of both plots are clipped at 10 s. Below: Probability distributions of touch duration (red) and inter-touch-interval (blue) of social touch episodes, plotted on a logarithmic time scale. The two distributions span multiple orders of magnitude and strongly overlap.