Witnessing another person’s suffering elicits vicarious brain activity in areas that are active when we ourselves are in pain. Whether this activity influences prosocial behavior remains the subject of debate. Here participants witnessed a confederate express pain through a reaction of the swatted hand or through a facial expression, and could decide to reduce that pain by donating money. Participants donate more money on trials in which the confederate expressed more pain. Electroencephalography shows that activity of the somatosensory cortex I (SI) hand region explains variance in donation. Transcranial magnetic stimulation (TMS) shows that altering this activity interferes with the pain–donation coupling only when pain is expressed by the hand. High-definition transcranial direct current stimulation (HD-tDCS) shows that altering SI activity also interferes with pain perception. These experiments show that vicarious somatosensory activations contribute to prosocial decision-making and suggest that they do so by helping to transform observed reactions of affected body-parts into accurate perceptions of pain that are necessary for decision-making.

Understanding whether another's smile reflects authentic amusement is a key challenge in social life, yet, the neural bases of this ability have been largely unexplored. Here, we combined transcranial magnetic stimulation (TMS) with a novel empathic accuracy (EA) task to test whether sensorimotor and mentalizing networks are critical for understanding another's amusement. Participants were presented with dynamic displays of smiles and explicitly requested to infer whether the smiling individual was feeling authentic amusement or not. TMS over sensorimotor regions representing the face (i.e., in the inferior frontal gyrus (IFG) and ventral primary somatosensory cortex (SI)), disrupted the ability to infer amusement authenticity from observed smiles. The same stimulation did not affect performance on a nonsocial task requiring participants to track the smiling expression but not to infer amusement. Neither TMS over prefrontal and temporo-parietal areas supporting mentalizing, nor peripheral control stimulations, affected performance on either task. Thus, motor and somatosensory circuits for controlling and sensing facial movements are causally essential for inferring amusement from another's smile. These findings highlight the functional relevance of IFG and SI to amusement understanding and suggest that EA abilities may be grounded in sensorimotor networks for moving and feeling the body.

Influential theories suggest that humans predict others' upcoming actions by using their own motor system as an internal forward model. However, evidence that the motor system is causally essential for predicting others' actions is meager. Using transcranial direct current stimulation (tDCS), we tested the role of the inferior frontal cortex (IFC), in action prediction (AP). We devised a novel AP task where participants observed the initial phases of right-hand reaching-to-grasp actions and had to predict their outcome (i.e., the goal/object to be grasped). We found that suppression by cathodal (inhibitory) tDCS of the left IFC, but not the left superior temporal sulcus or the right IFC, selectively impaired performance on the AP task, but not on a difficulty-matched control task. Remarkably, anodal (excitatory) tDCS of the left IFC brought about a selective improvement in the AP task. These findings indicate that the left IFC is necessary for predicting the outcomes of observed human right-hand actions. Crucially, our study shows for the first time that down- and up-regulating excitability within the motor system can hinder and enhance AP abilities, respectively. These findings support predictive coding theories of action perception and have implications for enhancement of AP abilities.

We review neuromodulation and lesion studies that address how activations in the mirror neuron system contribute to our perception of observed actions. Past reviews showed disruptions of this parieto-premotor network impair imitation and goal and kinematic processing. Recent studies bring five new themes. First, focal perturbations of a node of that circuit lead to changes across all nodes. Second, primary somatosensory cortex is an integral part of this network suggesting embodied representations are somatosensory-motor. Third, disturbing this network impairs the ability to predict the actions of others in the close (∼300ms) future. Fourth, disruptions impair our ability to coordinate our actions with others. Fifth, disrupting this network, the insula or cingulate also impairs emotion recognition.

The primary motor cortex (M1) is strongly influenced by several frontal regions. Dual-site transcranial magnetic stimulation (dsTMS) has highlighted the timing of early (<40 ms) prefrontal/premotor influences over M1. Here we used dsTMS to investigate, for the first time, longer-latency causal interactions of the posterior inferior frontal gyrus (pIFG) and pre-supplementary motor area (pre-SMA) with M1 at rest. A suprathreshold test stimulus (TS) was applied over M1 producing a motor-evoked potential (MEP) in the relaxed hand. Either a subthreshold or a suprathreshold conditioning stimulus (CS) was administered over ipsilateral pIFG/pre-SMA sites before the TS at different CS-TS inter-stimulus intervals (ISIs: 40–150 ms). Independently of intensity, CS over pIFG and pre-SMA (but not over a control site) inhibited MEPs at an ISI of 40 ms. The CS over pIFG produced a second peak of inhibition at an ISI of 150 ms. Additionally, facilitatory modulations were found at an ISI of 60 ms, with supra- but not subthreshold CS intensities. These findings suggest differential modulatory roles of pIFG and pre-SMA in M1 excitability. In particular, the pIFG –but not the pre-SMA– exerts intensity-dependent modulatory influences over M1 within the explored time window of 40-150 ms, evidencing fine-tuned control of M1 output.

The tongue holds a unique role in gustatory disgust. However, it is unclear whether the tongue representation in the motor cortex (tM1) is affected by the sight of distaste-related stimuli. Using transcranial magnetic stimulation (TMS) in healthy humans, we recorded tongue motor-evoked potentials (MEPs) as an index of tM1 cortico-hypoglossal excitability. MEPs were recorded while participants viewed pictures associated with gustatory disgust and revulsion (i.e. rotten foods and faces expressing distaste), non-oral-related disgusting stimuli (i.e. invertebrates like worms) and control stimuli. We found that oral-related disgust pictures suppressed tM1 cortico-hypoglossal output. This tM1 suppression was predicted by interindividual differences in disgust sensitivity. No similar suppression was found for disgusting invertebrates or when MEPs were recorded from a control muscle. These findings suggest that revulsion-eliciting food pictures trigger anticipatory inhibition mechanisms, possibly preventing toxin swallowing and contamination. A similar suppression is elicited when viewing distaste expressions, suggesting vicarious motor inhibition during social perception of disgust. Our study suggests an avoidant-defensive mechanism in human cortico-hypoglossal circuits and its ‘resonant’ activation in the vicarious experience of others’ distaste. These findings support a role for the motor system in emotion-driven motor anticipation and social cognition.

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