Sara Borgomaneri

Motor mapping of implied actions during perception of emotional body language

BACKGROUND Perceiving and understanding emotional cues is critical for survival. Using the International Affective Picture System (IAPS) previous TMS studies have found that watching humans in emotional pictures increases motor excitability relative to seeing landscapes or household objects, suggesting that emotional cues may prime the body for action. OBJECTIVE/HYPOTHESIS Here we tested whether motor facilitation to emotional pictures may reflect the simulation of the human motor behavior implied in the pictures occurring independently of its emotional valence. METHODS Motor-evoked potentials (MEPs) to single-pulse TMS of the left motor cortex were recorded from hand muscles during observation and categorization of emotional and neutral pictures. In experiment 1 participants watched neutral, positive and negative IAPS stimuli, while in experiment 2, they watched pictures depicting human emotional (joyful, fearful), neutral body movements and neutral static postures. RESULTS Experiment 1 confirms the increase in excitability for emotional IAPS stimuli found in previous research and shows, however, that more implied motion is perceived in emotional relative to neutral scenes. Experiment 2 shows that motor excitability and implied motion scores for emotional and neutral body actions were comparable and greater than for static body postures. CONCLUSIONS In keeping with embodied simulation theories, motor response to emotional pictures may reflect the simulation of the action implied in the emotional scenes. Action simulation may occur independently of whether the observed implied action carries emotional or neutral meanings. Our study suggests the need of controlling implied motion when exploring motor response to emotional pictures of humans.

Temporal dynamics of motor cortex excitability during perception of natural emotional scenes

Although it is widely assumed that emotions prime the body for action, the effects of visual perception of natural emotional scenes on the temporal dynamics of the human motor system have scarcely been investigated. Here, we used single-pulse transcranial magnetic stimulation (TMS) to assess motor excitability during observation and categorization of positive, neutral and negative pictures from the International Affective Picture System database. Motor-evoked potentials (MEPs) from TMS of the left motor cortex were recorded from hand muscles, at 150 and 300 ms after picture onset. In the early temporal condition we found an increase in hand motor excitability that was specific for the perception of negative pictures. This early negative bias was predicted by interindividual differences in the disposition to experience aversive feelings (personal distress) in interpersonal emotional contexts. In the later temporal condition, we found that MEPs were similarly increased for both positive and negative pictures, suggesting an increased reactivity to emotionally arousing scenes. By highlighting the temporal course of motor excitability during perception of emotional pictures, our study provides direct neurophysiological support for the evolutionary notions that emotion perception is closely linked to action systems and that emotionally negative events require motor reactions to be more urgently mobilized.

Seeing fearful body language rapidly freezes the observer's motor cortex.

Fearful body language is a salient signal alerting the observer to the presence of a potential threat in the surrounding environment. Although detecting potential threats may trigger an immediate reduction of motor output in animals (i.e., freezing behavior), it is unclear at what point in time similar reductions occur in the human motor cortex and whether they originate from excitatory or inhibitory processes. Using single-pulse and paired-pulse transcranial magnetic stimulation (TMS), here we tested the hypothesis that the observers motor cortex implements extremely fast suppression of motor readiness when seeing emotional bodies - and fearful body expressions in particular. Participants observed pictures of body postures and categorized them as happy, fearful or neutral while receiving TMS over the right or left motor cortex at 100-125 msec after picture onset. In three different sessions, we assessed corticospinal excitability, short intracortical inhibition (SICI) and intracortical facilitation (ICF). Independently of the stimulated hemisphere and the time of the stimulation, watching fearful bodies suppressed ICF relative to happy and neutral body expressions. Moreover, happy expressions reduced ICF relative to neutral actions. No changes in corticospinal excitability or SICI were found during the task. These findings show extremely rapid bilateral modulation of the motor cortices when seeing emotional bodies, with stronger suppression of motor readiness when seeing fearful bodies. Our results provide neurophysiological support for the evolutionary notions that emotion perception is inherently linked to action systems and that fear-related cues induce an urgent mobilization of motor reactions.

Sensorimotor Network Crucial for Inferring Amusement from Smiles

Abstract Understanding whether anothers 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 anothers 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 anothers 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.

Early changes in corticospinal excitability when seeing fearful body expressions

Quick inhibition of approach tendencies in response to signals of potential threats is thought to promote survival. However, little is known about the effect of viewing fearful expressions on the early dynamics of the human motor system. We used the high temporal resolution of single-pulse and paired-pulse transcranial magnetic stimulation (TMS) over the motor cortex to assess corticospinal excitability (CSE) and intracortical facilitation (ICF) during observation of happy, fearful and neutral body postures. To test motor circuits involved in approach tendencies, CSE and ICF were recorded from the first dorsal interosseous (FDI), a muscle involved in grasping, and the abductor pollicis brevis (APB), which served as a control. To test early motor dynamics, CSE and ICF were measured 70–90 ms after stimulus onset. We found a selective reduction in CSE in the FDI when participants observed fearful body expressions. No changes in ICF or in the excitability of APB were detected. Our study establishes an extremely rapid motor system reaction to observed fearful body expressions. This motor modulation involves corticospinal downstream projections but not cortical excitatory mechanisms, and appears to reflect an inhibition of hand grasping. Our results suggest a fast visuo-motor route that may rapidly inhibit inappropriate approaching actions.

The effect of alexithymia on early visual processing of emotional body postures.

Body postures convey emotion and motion-related information useful in social interactions. Early visual encoding of body postures, reflected by the N190 component, is modulated both by motion (i.e., postures implying motion elicit greater N190 amplitudes than static postures) and by emotion-related content (i.e., fearful postures elicit the largest N190 amplitude). At a later stage, there is a fear-related increase in attention, reflected by an early posterior negativity (EPN) (Borhani et al., 2015). Here, we tested whether difficulties in emotional processing (i.e., alexithymia) affect early and late visual processing of body postures. Low alexithymic participants showed emotional modulation of the N190, with fearful postures specifically enhancing N190 amplitude. In contrast, high alexithymic participants showed no emotional modulation of the N190. Both groups showed preserved encoding of the motion content. At a later stage, a fear-related modulation of the EPN was found for both groups, suggesting that selective attention to salient stimuli is the same in both low and high alexithymia.

Pictures of disgusting foods and disgusted facial expressions suppress the tongue motor cortex

Abstract 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.

Long-latency modulation of motor cortex excitability by ipsilateral posterior inferior frontal gyrus and pre-supplementary motor area

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.

Visual, sensorimotor and cognitive routes to understanding others' enjoyment: An individual differences rTMS approach to empathic accuracy

ABSTRACT Functional imaging studies suggest that accurate understanding of others’ emotional feelings (i.e., empathic accuracy, EA) recruits high‐order visual, sensorimotor and mentalizing brain networks. However, the behavioral relevance of these findings is unclear. To fill in this gap, we used repetitive transcranial magnetic stimulation (rTMS) to interfere with the right superior temporal sulcus (STS), inferior frontal gyrus (IFG) and temporoparietal junction (TPJ) during an EA task requiring participants to infer the enjoyment felt by a social target while smiling/laughing. Relative to a baseline condition (sham rTMS), active rTMS of STS, IFG and TPJ (but not of a control site) disrupted the efficiency of EA task performance, mainly by lowering task accuracy; rTMS of IFG and TPJ also slowed down response speeds. Importantly, the effects of rTMS on EA task efficiency were predicted by baseline EA performance, with high‐performers showing a performance decrease when the TPJ was targeted, and low‐performers showing a performance decrease when the STS or the IFG was targeted. The double dissociation in the effect of rTMS between low‐ and high‐performers suggests distinct roles of STS, IFG and TPJ in efficient understanding of the enjoyment felt by others. These findings provide causal evidence of distinct visual, sensorimotor and cognitive routes to EA and suggest that individual differences in EA are underpinned by differential recruitment of these routes. HIGHLIGHTSrTMS over STS, IFG and TPJ impaired empathic accuracy (EA).Individual differences in EA moderated the effects of rTMS.Low EA‐performers showed impaired EA following rTMS over STS and IFG.High EA‐performers showed impaired EA following rTMS over TPJ.Low and high EA‐performers differentially recruited the brain regions supporting EA.

Long-latency interhemispheric interactions between motor-related areas and the primary motor cortex: a dual site TMS study

The primary motor cortex (M1) is highly influenced by premotor/motor areas both within and across hemispheres. Dual site transcranial magnetic stimulation (dsTMS) has revealed interhemispheric interactions mainly at early latencies. Here, we used dsTMS to systematically investigate long-latency causal interactions between right-hemisphere motor areas and the left M1 (lM1). We stimulated lM1 using a suprathreshold test stimulus (TS) to elicit motor-evoked potentials (MEPs) in the right hand. Either a suprathreshold or a subthreshold conditioning stimulus (CS) was applied over the right M1 (rM1), the right ventral premotor cortex (rPMv), the right dorsal premotor cortex (rPMd) or the supplementary motor area (SMA) prior to the TS at various CS-TS inter-stimulus intervals (ISIs: 40–150 ms). The CS strongly affected lM1 excitability depending on ISI, CS site and intensity. Inhibitory effects were observed independently of CS intensity when conditioning PMv, rM1 and SMA at a 40-ms ISI, with larger effects after PMv conditioning. Inhibition was observed with suprathreshold PMv and rM1 conditioning at a 150-ms ISI, while site-specific, intensity-dependent facilitation was detected at an 80-ms ISI. Thus, long-latency interhemispheric interactions, likely reflecting indirect cortico-cortical/cortico-subcortical pathways, cannot be reduced to nonspecific activation across motor structures. Instead, they reflect intensity-dependent, connection- and time-specific mechanisms.