Evolutionarily conserved neural responses to affective touch transcend consciousness and change with age

Affective touch is thought to be a critical substrate for the formation of the social relationships which exist as a foundation for primate societies. Although grooming behavior in monkeys appears to recapitulate features of affective touch behavior in humans, it is unknown whether affective touch activates the same neural networks in other primate species and whether this activation requires conscious perception or changes across the lifespan. We stimulated lightly anesthetized macaques at affective (slow) and discriminative (fast) touch speeds during the acquisition of functional MRI data. We demonstrate evolutionarily conserved activation of interoceptive neural networks which change significantly in old age.

Affective touch—a slow, gentle, and pleasant form of touch—activates a different neural network than which is activated during discriminative touch in humans. Affective touch perception is enabled by specialized low-threshold mechanoreceptors in the skin with unmyelinated fibers called C tactile (CT) afferents. These CT afferents are conserved across mammalian species, including macaque monkeys. However, it is unknown whether the neural representation of affective touch is the same across species and whether affective touch’s capacity to activate the hubs of the brain that compute socioaffective information requires conscious perception. Here, we used functional MRI to assess the preferential activation of neural hubs by slow (affective) vs. fast (discriminative) touch in anesthetized rhesus monkeys (Macaca mulatta). The insula, anterior cingulate cortex (ACC), amygdala, and secondary somatosensory cortex were all significantly more active during slow touch relative to fast touch, suggesting homologous activation of the interoceptive-allostatic network across primate species during affective touch. Further, we found that neural responses to affective vs. discriminative touch in the insula and ACC (the primary cortical hubs for interoceptive processing) changed significantly with age. Insula and ACC in younger animals differentiated between slow and fast touch, while activity was comparable between conditions for aged monkeys (equivalent to >70 y in humans). These results, together with prior studies establishing conserved peripheral nervous system mechanisms of affective touch transduction, suggest that neural responses to affective touch are evolutionarily conserved in monkeys, significantly impacted in old age, and do not necessitate conscious experience of touch.