Abstract
Touch is a fundamental aspect of social, parental and sexual behavior. In contrast to our detailed knowledge about cortical processing of non-social touch, we still know little about how social touch impacts 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. Spiking neural network simulations indicate 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.
Highlights
Touch is a fundamental aspect of social, parental and sexual behavior
We analyze the activity of 1156 neurons, recorded from five cortical areas, over 7408 episodes of social facial touch in 15 female and 14 male rats (58,591 unique cell-touch pairs, averaging 51 touch episodes per cell)
We recorded the activity of neurons throughout the cortical column in five cortical areas: two sensory areas, barrel cortex (‘S1’, the primary somatosensory representation of the mystacial vibrissae) and auditory cortex (‘A1’), and three frontal areas, vibrissa motor cortex (‘VMC’, the primary motor representation of the mystacial vibrissae), cingulate cortex (‘ACC’, a putative homolog of human anterior cingulate cortex), and prelimbic cortex (‘PrL’, a putative homolog of human medial prefrontal cortex) (Fig. 1b)
Summary
Touch is a fundamental aspect of social, parental and sexual behavior. In contrast to our detailed knowledge about cortical processing of non-social touch, we still know little about how social touch impacts cortical circuits. An identical pattern of touch was always given by the same experimenter, activity in anterior cingulate, orbitofrontal, somatosensory, and insular cortices is different when subjects believe they are being touched by a man or a woman[3,4] or by a partner or a stranger[5] This social-context-dependent modulation of cortical touch responses is negatively correlated with autism-like traits[4] and is increased by intranasal oxytocin administration[5]. Previous work has shown that even though whisking amplitude is lower during social facial interactions than when investigating objects, population firing rate changes[13] and membrane potential modulations[14] in rat somatosensory cortex are larger during social touch than object touch and do not correlate with whisker movements. Rat somatosensory activity is modulated in a social context before actual social facial touch[14], and firing rates depend on sociosexual context, such as estrus state[13,15]
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