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

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.

Fig. 1.

Distinct BOLD signal during social touch and self-touch. (Top) Other-touch activated areas involved in social cognition, display of slices [53 −18 14]. (Bottom) Self-touch deactivated a widespread network of areas, display of slices [47 46 15]. Both thresholded at P < 0.05; FWE-corrected at the whole brain level; cluster size > 20.

Fig. 2.

Differential encoding of other-touch and self-touch. (Top) A widespread network showed higher activation for other-touch than for self-touch, display of slices [44 15 69], cluster size > 20. (Bottom) Conjunction of activation during other-touch and deactivation during self-touch. Display of slices [6 −6 12], cluster size > 5. Both thresholded at P < 0.05; FWE-corrected at the whole brain level.

Fig. 3.

Parameter estimates for regions involved in processing tactile sensory information differ for the three conditions. Other-touch by the experimenter (blue), self-touch (green), and object-touch (brown); main effect of condition [F(22, 136) = 18.4, P < 0.0005, Wilks’ Λ = 0.063]. Error bars represent the SE. aI, anterior insula; BR, brainstem; l, left; pI, posterior insula; r, right; thal, thalamus.

Fig. 4.

Detection thresholds for von Frey filaments during four conditions: baseline (no additional touch stimulation), self-touch, other-touch, and object-touch. The plot indicates mean (midline), 95% confidence interval (dark box), one SD (light box), and individual data points. The small plot indicates individual values for each subject during other-touch and self-touch.

Fig. 5.

Amplitude and latency of SEPs differs between other-touch and self-touch. (Left, A) Amplitudes at the cortical level (C3/4 and CZ) were higher for other-touch than for self-touch. (Left, B) Latencies at the cortical level (C3/4) and at the cervical level were shorter for other-touch than for self-touch. Gray indicates no touch stimulation; blue, other-touch; green, self-touch; brown, object-touch. Error bars indicate SE. (Right) Line plots depicting individual values for self-touch and other-touch. *P < 0.05.