Distinction of self-produced touch and social touch at cortical and spinal cord levels

Proc Natl Acad Sci U S A. 2019 Feb 5;116(6):2290-2299. doi: 10.1073/pnas.1816278116. Epub 2019 Jan 22.

Abstract

Differentiation between self-produced tactile stimuli and touch by others is necessary for social interactions and for a coherent concept of "self." The mechanisms underlying this distinction are unknown. Here, we investigated the distinction between self- and other-produced light touch in healthy volunteers using three different approaches: fMRI, behavioral testing, and somatosensory-evoked potentials (SEPs) at spinal and cortical levels. Using fMRI, we found self-other differentiation in somatosensory and sociocognitive areas. Other-touch was related to activation in several areas, including somatosensory cortex, insula, superior temporal gyrus, supramarginal gyrus, striatum, amygdala, cerebellum, and prefrontal cortex. During self-touch, we instead found deactivation in insula, anterior cingulate cortex, superior temporal gyrus, amygdala, parahippocampal gyrus, and prefrontal areas. Deactivation extended into brain areas encoding low-level sensory representations, including thalamus and brainstem. These findings were replicated in a second cohort. During self-touch, the sensorimotor cortex was functionally connected to the insula, and the threshold for detection of an additional tactile stimulus was elevated. Differential encoding of self- vs. other-touch during fMRI correlated with the individual self-concept strength. In SEP, cortical amplitudes were reduced during self-touch, while latencies at cortical and spinal levels were faster for other-touch. We thus demonstrated a robust self-other distinction in brain areas related to somatosensory, social cognitive, and interoceptive processing. Signs of this distinction were evident at the spinal cord. Our results provide a framework for future studies in autism, schizophrenia, and emotionally unstable personality disorder, conditions where symptoms include social touch avoidance and poor self-vs.-other discrimination.

Keywords: affective touch; self-concept; self-touch; sensorimotor integration; sensory attenuation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Brain Mapping* / methods
  • Cerebral Cortex / physiology*
  • Discrimination, Psychological*
  • Female
  • Healthy Volunteers
  • Humans
  • Image Processing, Computer-Assisted
  • Magnetic Resonance Imaging
  • Male
  • Social Behavior
  • Spinal Cord / physiology*
  • Touch Perception*
  • Young Adult