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

• 成果类型: Article
• 署名作者: Charbonneau, Joey A.; Santistevan, Anthony C.; Raven, Erika P.; Bennett, Jeffrey L.; Russ, Brian E.; Bliss-Moreau, Eliza
• 署名单位: University of California System; University of California Davis; University of California System; University of California Davis; University of California System; University of California Davis; New York University; University of California System; University of California Davis; California State University System; California State University Sacramento; Nathan Kline Institute for Psychiatric Research; Icahn School of Medicine at Mount Sinai; Icahn School of Medicine at Mount Sinai; New York University
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-11386
• DOI: 10.1073/pnas.2322157121
• 发表日期: 2024-04-22
• 关键词: medial prefrontal cortex; von economo neurons; psychophysiological interactions; cingulate cortex; pleasant touch; architectonic subdivision; physiological condition; unmyelinated afferents; anterior insula; rhesus-monkey

摘要

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.