INTRODUCTION: TMS studies indicate that watching painful stimuli shown on the body of a human model induces a decrease of corticospinal excitability in the onlooker’s muscle correspondent to the one stimulated in the model (Avenanti et al., 2005). This muscle-specific, pain observation-related inhibition (PORI) is similar to that found during actual pain perception (Farina et al., 2003), suggesting that seeing pain in others triggers pain embodied resonance in the onlooker’s corticospinal system. However, information on the relation between PORI and the activity of sensorimotor cortical regions recruited during pain perception is meagre. METHODS: In two experiments we used a perturb-and-measure TMS paradigm (Avenanti et al., 2007), combining repetitive TMS (15 min 1Hz-rTMS, to suppress neural activity in selected cortical regions) and single-pulse TMS (spTMS, to assess PORI by recording MEPs during pain observation). In both experiments MEPs were recorded in 3 spTMS sessions (1 baseline, and 2 post-rTMS sessions) during the observation of videos showing needles penetrating the FDI muscle of a human model (needle-in-FDI) and control videos (needles-in-foot, needle-in-tomato). MEPs were collected from the FDI (target) and the ADM (control) muscle. In exp1 (N=11), we applied image-guided rTMS over the hand representation in dorsal premotor (PMc) and primary motor cortex (M1). In exp2 (N=11), we applied rTMS over the hand representation in the somatosensory cortex (S1) and over the visual cortex (V1). After TMS, subjects judged the pain supposedly felt by the model and filled-out the Interpersonal Reactivity Index, assessing dispositional empathy. RESULTS: In the baseline sessions (no rTMS) of exp1-2, we found a typical PORI effect: watching needle-in-FDI stimuli brought about a reduction of MEPs recorded from the very same muscle in the observer (relative to visual controls), without modulating the ADM control muscle. The effect was stronger in the subjects who showed greater dispositional empathy and provided higher observed-pain scores. Exp1: After M1 suppression, the PORI effect was disrupted: MEPs were comparable in the three visual conditions. After PMc suppression, the PORI effect was reversed: MEPs from the FDI muscle were greater during “needle-in-FDI” than during “needle-in-foot” and “needle-in-tomato” conditions. Exp2: After V1 suppression, the PORI was not different from the baseline session. After S1 suppression PORI was enhanced with greater inhibitory response for “needle-in the-hand” stimuli relative to baseline. CONCLUSIONS: PORI was disrupted and enhanced by M1 and S1 suppression, respectively, and left unaffected by V1 suppression. Importantly, suppression of PMc changed the PORI into a muscle-specific facilitatory response. Thus, while S1 normal functioning seems to keep under control a potentially excessive embodiment of others’ pain, normal functioning of PMc and M1 exert a same-direction, different-strength modulatory effect that allows an optimal tuning of resonant corticospinal mapping of observed pain. Our findings highlight the causal connectivity between PMc-M1-S1 regions and the corticospinal system during embodied empathy for pain and suggest that TMS can disclose specific inter-regional neural interactions during social perception. REFERENCES: Avenanti A et al. (2005) Nature Neuroscience 8:955-960. Avenanti A et al. (2007) Current Biology 17:2129-2135. Farina S et al. (2003) Neurological Research 25:130-142.

Causative connectivity of sensorimotor regions during embodied empathy for pain as revealed by perturb-and-measure TMS

BORGOMANERI, SARA;AVENANTI, ALESSIO
2011

Abstract

INTRODUCTION: TMS studies indicate that watching painful stimuli shown on the body of a human model induces a decrease of corticospinal excitability in the onlooker’s muscle correspondent to the one stimulated in the model (Avenanti et al., 2005). This muscle-specific, pain observation-related inhibition (PORI) is similar to that found during actual pain perception (Farina et al., 2003), suggesting that seeing pain in others triggers pain embodied resonance in the onlooker’s corticospinal system. However, information on the relation between PORI and the activity of sensorimotor cortical regions recruited during pain perception is meagre. METHODS: In two experiments we used a perturb-and-measure TMS paradigm (Avenanti et al., 2007), combining repetitive TMS (15 min 1Hz-rTMS, to suppress neural activity in selected cortical regions) and single-pulse TMS (spTMS, to assess PORI by recording MEPs during pain observation). In both experiments MEPs were recorded in 3 spTMS sessions (1 baseline, and 2 post-rTMS sessions) during the observation of videos showing needles penetrating the FDI muscle of a human model (needle-in-FDI) and control videos (needles-in-foot, needle-in-tomato). MEPs were collected from the FDI (target) and the ADM (control) muscle. In exp1 (N=11), we applied image-guided rTMS over the hand representation in dorsal premotor (PMc) and primary motor cortex (M1). In exp2 (N=11), we applied rTMS over the hand representation in the somatosensory cortex (S1) and over the visual cortex (V1). After TMS, subjects judged the pain supposedly felt by the model and filled-out the Interpersonal Reactivity Index, assessing dispositional empathy. RESULTS: In the baseline sessions (no rTMS) of exp1-2, we found a typical PORI effect: watching needle-in-FDI stimuli brought about a reduction of MEPs recorded from the very same muscle in the observer (relative to visual controls), without modulating the ADM control muscle. The effect was stronger in the subjects who showed greater dispositional empathy and provided higher observed-pain scores. Exp1: After M1 suppression, the PORI effect was disrupted: MEPs were comparable in the three visual conditions. After PMc suppression, the PORI effect was reversed: MEPs from the FDI muscle were greater during “needle-in-FDI” than during “needle-in-foot” and “needle-in-tomato” conditions. Exp2: After V1 suppression, the PORI was not different from the baseline session. After S1 suppression PORI was enhanced with greater inhibitory response for “needle-in the-hand” stimuli relative to baseline. CONCLUSIONS: PORI was disrupted and enhanced by M1 and S1 suppression, respectively, and left unaffected by V1 suppression. Importantly, suppression of PMc changed the PORI into a muscle-specific facilitatory response. Thus, while S1 normal functioning seems to keep under control a potentially excessive embodiment of others’ pain, normal functioning of PMc and M1 exert a same-direction, different-strength modulatory effect that allows an optimal tuning of resonant corticospinal mapping of observed pain. Our findings highlight the causal connectivity between PMc-M1-S1 regions and the corticospinal system during embodied empathy for pain and suggest that TMS can disclose specific inter-regional neural interactions during social perception. REFERENCES: Avenanti A et al. (2005) Nature Neuroscience 8:955-960. Avenanti A et al. (2007) Current Biology 17:2129-2135. Farina S et al. (2003) Neurological Research 25:130-142.
2011
Magstim TMS Summer school 2011 - abstracts
10
11
Borgomaneri S; Avenanti A
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Utilizza questo identificativo per citare o creare un link a questo documento: https://hdl.handle.net/11585/391795
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