انجماد و یا فرار؟ مدولاسیون مقابل واکنش پذیری همدلانه برای درد دیگران

Abstract Perceiving pain in others may induce the covert simulation of both sensory and emotional components of others' pain experience. Previous transcranial magnetic stimulation (TMS) studies have investigated the motor counterpart of this resonant mapping by showing suppression of motor-evoked potentials (MEPs) during the observation of a needle entering body parts of another person. Here we explored whether MEPs recorded from an onlooker's hand (e.g., the right hand, TMS to the left motor cortex) are differentially influenced by the observation of painfully stimuli delivered to the same (right) or the opposite (left) hand in a model. Congruency between observed (model) and recorded (onlooker) hand brought about a reduction of MEPs amplitude. This resonant inhibitory response in the onlooker was specific for the muscle penetrated in the model. In contrast, observing pain on the model's hand opposite to that from which MEPs were recorded brought about a generalized increase of hand corticospinal excitability. Corticospinal inhibition and facilitation effects were comparable in the two hemispheres and specific for the corresponding and opposite hand. Results suggest that observing pain in another person's hand automatically induces the covert simulation of potentially adaptive freezing and avoidance responses in the onlooker's corticospinal system.

. Introduction Studies suggest that observing or imagining the pain of others activates neural circuits largely overlapping with those involved in the first-hand experience of pain (Avenanti and Aglioti, 2006). These circuits comprise both regions processing the affective dimension of pain (e.g., the unpleasantness of a noxious stimulus), such as the anterior insula and the anterior cingulate cortex (Singer et al., 2004), and regions processing the sensory dimension of pain (e.g., intensity, localization of a noxious stimulus) including the somatosensory cortices (Bufalari et al., 2007, Lamm et al., 2007, Cheng et al., 2008, Benuzzi et al., 2008 and Valeriani et al., 2008). Using single-pulse transcranial magnetic stimulation (TMS) it has been demonstrated that the direct observation of ‘flesh and bone’ painful stimulations delivered to the body of a stranger human model brings about a decrease of amplitude of motor-evoked potentials (MEPs) in the onlooker (Avenanti et al., 2005 and Fecteau et al., 2008). Importantly, this inhibition was specific to the muscle the subjects observed being painfully stimulated and correlated with the evaluations of the intensity (Avenanti et al., 2006 and Avenanti et al., 2009) and spread (Minio-Paluello et al., 2006) of the pain ascribed to the observed model, suggesting that corticospinal inhibition may reflect a ‘sensorimotor contagion’, i.e., an automatic embodiment of sensory qualities of pain onto the observers' motor system. What remains unclear if whether observing painful stimuli on the body of another person may induce a more complex modulation of the onlooker's motor system in addition to the resonant freezing response of the muscle vicariously involved in the painful stimulation. In principle, feeling pain on one hand may be associated to a higher reactivity of the opposite hand that can be used to try and reduce the effect of the noxious stimulus (Melzack and Casey, 1968 and Williams, 2002). Therefore, it is possible that the sensorimotor contagion contingent upon the vicarious feeling of others' pain may involve not only corticospinal inhibition of the hand corresponding to that painfully stimulated in the other person (freezing) but also corticospinal facilitation of the hand opposite to the one stimulated in the model (implementation of reactions aimed at reducing pain, escaping). We explored this issue in two groups of participants who undergone single-pulse TMS over the left or right motor cortex (M1) while they observed needles entering both the right and the left hand of a stranger model. Corticospinal reactivity to the model's pain was recorded from both the left and the right hand of the experimental subjects in order to explore the relationship between the model and the onlookers' hands and hemispheres

Results Participants were presented with stimuli depicting left or right static hands or left or right hands being penetrated by a needle. Subjects were divided in two groups according to the stimulated hemisphere (left M1, right M1). In the left M1 group, MEPs were recorded from the right hand during presentation of right hand (congruent) and left hand (opposite) stimuli. In the right M1 group MEPs were recorded from the left hand during presentation of left hand (congruent) or right hand (opposite) stimuli. ANOVA on pain intensity evaluations showed no effect of Hemisphere, hand congruency nor their interaction (Fs < 2.82, ps > .11, Fig. 1). This indicates that pain inflicted on congruent and opposite hand was similarly judged in the two groups. Pain intensity judgements in the two groups of subjects who received TMS pulses ... Fig. 1. Pain intensity judgements in the two groups of subjects who received TMS pulses over the left or right M1. Error bars indicate s.e.m. Figure options In contrast to the similarity in subjective evaluations, pain on congruent and opposite hand was associated to different patterns of corticospinal excitability (Fig. 2). ANOVA on MEP ratios revealed a significant triple interaction Muscle × Hand × Condition (F1,22 = 4.86, p = .038). To analyze this interaction two separate ANOVAs, one for each muscle, were performed. Normalized MEP amplitude (% of fixation baseline) recorded from the FDI (A) and ... Fig. 2. Normalized MEP amplitude (% of fixation baseline) recorded from the FDI (A) and the TE (B) during the observation of the experimental stimuli. Error bars indicate s.e.m. Asterisks (*) indicate significant post-hoc comparisons (p < .05). Icons on the left show the position of the active electrodes on right hand for exemplificative purpose. Note that MEPs were recorded from the right hand in the group receiving the TMS over the left M1, and from the left hand in the group receiving the TMS over the right M1. Figure options Analysis of MEPs recorded from the FDI muscle revealed a significant main effect of Hand (F1,22 = 47.42, p = .000001) which was accounted for by the higher MEPs amplitude during observation of opposite hand (mean ± s.e.m.: 117% ± 6%) than congruent hand (95% ± 6%) corresponding to that from which MEPs were recorded ( Fig. 2A). Importantly, a significant interaction Hand × Condition was found (F1,22 = 25.17, p = .00005). Post-hoc analysis revealed that amplitudes of MEPs recorded during the observation of painful stimulation on the congruent hand (84% ± 5%) were lower than those recorded when watching the static view of the congruent hand (105% ± 5%, p = .027) or opposite hand (103% ± 4%, p = .046) and when watching pain on the opposite hand (131% ± 7%, p = .0002). Moreover MEPs recorded during the observation of pain on the opposite hand were higher than MEPs recorded during the observation of opposite (p = .003) and congruent (p = .005) static hand. MEPs were comparable for the two static hand stimuli with no painful stimulation (p = .81). Thus, observing pain on the congruent hand reduced the excitability of the FDI corticospinal representation while observing pain on the opposite hand facilitated the FDI. These two different effects hold true also with respect to the fixation baseline (t23 = −2.97, p = .007; t23 = 4.80, p = .00008 respectively). No other significant effect was found for MEPs recorded from the FDI muscle (Fs < 2.06, ps > .16). ANOVA on MEPs recorded from the TE showed a main effect of Hand (F1,22 = 28.25, p = .00002) with higher amplitudes during observation of opposite (121% ± 8%) than congruent hand stimuli (98% ± 7%) and a main effect of Condition (F1,22 = 28.98, p = .00002) with higher amplitudes during the observation of painful (125% ± 8%) than during static stimuli with no painful stimulations (93% ± 6%). Importantly, a significant interaction Hand × Condition was found (F1,22 = 7.74, p = .011). Post-hoc analysis shows that MEP amplitudes were higher during observation of pain on the opposite hand (145% ± 6%) compared to observation of opposite (98% ± 6%, p = .0002) or congruent static hand stimuli (89 ± 6%, p = .0004) or pain on congruent hand (106 ± 8%, p = .0002), which in turn did not differ from one another (ps > .13) ( Fig. 2B). MEP amplitudes during the observation of pain on the opposite hand were higher also with respect to the fixation baseline (t23 = 4.10, p = .0004). No other significant effects were found for MEPs recorded from the TE (Fs < .67, ps > .42).