Transcranial magnetic stimulation over supramarginal gyrus stimulates primary motor cortex directly and impairs manual dexterity: implications for TMS focality.

Based on human motor cortex, the effective spatial resolution of transcranial magnetic stimulation (TMS) is often described as 5-20 mm, because small changes in TMS coil position can have large effects on motor-evoked potentials (MEPs). MEPs are often studied at rest, with muscles relaxed. During muscle contraction and movement, corticospinal excitability is higher, thresholds for effective stimulation are lower, and MEPs can be evoked from larger regions of scalp, so the effective spatial resolution of TMS is larger. We found that TMS over the supramarginal gyrus (SMG) impaired manual dexterity in the grooved pegboard task. It also resulted in short-latency MEPs in hand muscles, despite the coil being 55 mm away from the motor cortex hand area (M1). MEPs might be evoked by either a specific corticospinal connection from SMG or a remote but direct electromagnetic stimulation of M1. To distinguish these alternatives, we mapped MEPs across the scalp during rest, isotonic contraction, and manual dexterity tasks and ran electric field simulations to model the expected M1 activation from 27 scalp locations and four coil orientations. We also systematically reviewed studies using TMS during movement. Across five experiments, TMS over SMG reliably evoked MEPs during hand movement. These MEPs were consistent with direct M1 stimulation and substantially decreased corticospinal thresholds during natural movement. Systematic review suggested that 54 published experiments may have suffered from similar motor activation confounds. Our results have implications for the assumed spatial resolution of TMS, and especially when TMS is presented within 55 mm of the motor cortex.NEW & NOTEWORTHY Transcranial magnetic stimulation (TMS) is often described as having an effective spatial resolution of ∼10 mm, because of the limited area of the scalp on which TMS produces motor-evoked potentials (MEPs) in resting muscles. We find that during natural hand movement TMS evokes MEPs from a much larger scalp area, in particular when stimulating over the supramarginal gyrus 55 mm away. Our results show that TMS can be effective at much larger distances than generally assumed.

Investigating the relationship between self-reported interoceptive experience and risk propensity.

Risky behaviour may be associated with visceral experiences, such as increased heart rate. Previous studies examining the relationship between perception of such signals (interoception) and risk-taking typically used behavioural tasks with potential for monetary reward. This approach may be less informative for understanding general risk propensity. In addition, such research does not usually consider the varied ways individuals engage with interoceptive signals. However, examining these different forms of engagement may help us understand how subjective experience of interoception influences risk-taking. As such, we performed two surveys (n = 471, primarily young adults) to examine the relationship between self-reported engagement with interoceptive signals (measured using the Multidimensional Assessment of Interoceptive Awareness) and a generalised measure of risk propensity (the General Risk Propensity Scale). Results indicated that different ways of interpreting or engaging with interoceptive signals were differentially associated with risk propensity. In particular, they provide preliminary evidence that those with the ability to ignore or not worry about visceral signals when they are uncomfortable display greater risk propensity (and these effects may possibly be gender-specific).

Subcortical contributions to the sense of body ownership.

The sense of body ownership (i.e. the feeling that our body or its parts belong to us) plays a key role in bodily self-consciousness and is believed to stem from multisensory integration. Experimental paradigms such as the rubber hand illusion have been developed to allow the controlled manipulation of body ownership in laboratory settings, providing effective tools for investigating malleability in the sense of body ownership and the boundaries that distinguish self from other. Neuroimaging studies of body ownership converge on the involvement of several cortical regions, including the premotor cortex and posterior parietal cortex. However, relatively less attention has been paid to subcortical structures that may also contribute to body ownership perception, such as the cerebellum and putamen. Here, on the basis of neuroimaging and neuropsychological observations, we provide an overview of relevant subcortical regions and consider their potential role in generating and maintaining a sense of ownership over the body. We also suggest novel avenues for future research targeting the role of subcortical regions in making sense of the body as our own.

No reduction in motor-evoked potential amplitude during the rubber hand illusion.

INTRODUCTION: In the rubber hand illusion (RHI), touches are applied to a fake hand at the same time as touches are applied to a participant's real hand that is hidden in a congruent position. Synchronous (but not asynchronous) tactile stimulation of the two hands may induce the sensation that the fake hand is the participant's own. As such, the illusion is commonly used to examine the sense of body ownership. Some studies indicate that in addition to the subjective experience of limb ownership reported by participants, the RHI can also reduce corticospinal excitability (e.g., as reflected in motor-evoked potential [MEP] amplitude) and alter parietal-motor cortical connectivity in passive participants. These findings have been taken to support a link between motor cortical processing and the subjective experience of body ownership. METHODS: In this study, we tried to replicate the reduction in MEP amplitude associated with the RHI and uncover the components of the illusion that might explain these changes. As such, we used single-pulse transcranial magnetic stimulation to probe the excitability of the corticospinal motor system as participants experienced the RHI. RESULTS: Despite participants reporting the presence of the illusion and showing shifts in perceived real hand position towards the fake limb supporting its elicitation, we did not observe any associated reduction in MEP amplitude. CONCLUSION: We conclude that a reduction in MEP amplitude is not a reliable outcome of the RHI and argue that if such effects do occur, they are unlikely to be large or functionally relevant.

Smaller preferred interpersonal distance for joint versus parallel action.

During social interaction, humans prefer to keep a certain distance between themselves and other individuals. This preferred 'interpersonal distance' (IPD) is known to be sensitive to social context, and in the present study we aimed to further investigate the extent to which IPD is affected by the specific type of social interaction. In particular, we focused on the contrast between joint actions, where two or more individuals coordinate their actions in space and time to achieve a shared goal, and parallel actions, where individuals act alongside each other but individually. We predicted that joint action would be associated with a smaller preferred IPD compared to parallel action. Additionally, given that this research took place in the midst of the COVID-19 pandemic, we aimed to assess whether IPD preferences are affected by individuals' concerns about infection in general, as well as COVID-19 in particular. We predicted that higher individual concerns would be associated with greater preferred IPD. To test these hypotheses, we asked participants to imagine different social scenarios (involving either joint or parallel actions alongside a stranger) and indicate, on a visual scale, their preferred IPD. The results of two experiments (n = 211, n = 212) showed that participants preferred a shorter distance when they imagined acting jointly compared to when they imagined acting in parallel. Moreover, participants who reported higher discomfort for potential pathogen contact and who were more aware of the COVID-19 context in which the study took place preferred a larger IPD in general. Our results provide further evidence that different types of social interaction shape IPD preference. We discuss potential reasons for this phenomenon and highlight remaining questions for future research.

Variability of EEG electrode positions and their underlying brain regions: visualizing gel artifacts from a simultaneous EEG-fMRI dataset.

INTRODUCTION: We investigated the between-subject variability of EEG (electroencephalography) electrode placement from a simultaneously recorded EEG-fMRI (functional magnetic resonance imaging) dataset. METHODS: Neuro-navigation software was used to localize electrode positions, made possible by the gel artifacts present in the structural magnetic resonance images. To assess variation in the brain regions directly underneath electrodes we used MNI coordinates, their associated Brodmann areas, and labels from the Harvard-Oxford Cortical Atlas. We outline this relatively simple pipeline with accompanying analysis code. RESULTS: In a sample of 20 participants, the mean standard deviation of electrode placement was 3.94 mm in x, 5.55 mm in y, and 7.17 mm in z, with the largest variation in parietal and occipital electrodes. In addition, the brain regions covered by electrode pairs were not always consistent; for example, the mean location of electrode PO7 was mapped to BA18 (secondary visual cortex), whereas PO8 was closer to BA19 (visual association cortex). Further, electrode C1 was mapped to BA4 (primary motor cortex), whereas C2 was closer to BA6 (premotor cortex). CONCLUSIONS: Overall, the results emphasize the variation in electrode positioning that can be found even in a fixed cap. This may be particularly important to consider when using EEG positioning systems to inform non-invasive neurostimulation.

Little evidence for an effect of the rubber hand illusion on basic movement.

Body ownership refers to the distinct sensation that our observed body belongs to us, which is believed to stem from multisensory integration. This is commonly shown through the rubber hand illusion (RHI), which induces a sense of ownership over a false limb. Whilst the RHI may interfere with object-directed action and alter motor cortical activity, it is not yet clear whether a sense of ownership over an artificial hand has functional consequences for movement production per se. As such, we performed two motion-tracking experiments (n = 117) to examine the effects of the RHI on the reaction time, acceleration, and velocity of rapid index finger abduction. We observed little convincing evidence that the induction of the RHI altered these kinematic variables. Moreover, the subjective sensations of rubber hand ownership, referral of touch, and agency did not convincingly correlate with kinematic variables, and nor did proprioceptive drift, suggesting that changes in body representation elicited by the RHI may not influence basic movement. Whilst experiment 1 suggested that individuals reporting a greater sensation of the real hand disappearing performed movements with smaller acceleration and velocity following illusion induction, we did not replicate this effect in a second experiment, suggesting that these effects may be small or not particularly robust. Overall, these results indicate that manipulating the conscious experience of body ownership has little impact on basic motor control, at least in the RHI with healthy participants.

The Relationship Between Referral of Touch and the Feeling of Ownership in the Rubber Hand Illusion.

The rubber hand illusion (RHI) is one of the most commonly used paradigms to examine the sense of body ownership. Touches are synchronously applied to the real hand, hidden from view, and a false hand in an anatomically congruent position. During the illusion one may perceive that the feeling of touch arises from the false hand (referral of touch), and that the false hand is one's own. The relationship between referral of touch and body ownership in the illusion is unclear, and some articles average responses to statements addressing these experiences, which may be inappropriate depending on the research question of interest. To address these concerns, we re-analyzed three freely available datasets to better understand the relationship between referral of touch and feeling of ownership in the RHI. We found that most participants who report a feeling of ownership also report referral of touch, and that referral of touch and ownership show a moderately strong positive relationship that was highly replicable. In addition, referral of touch tends to be reported more strongly and more frequently than the feeling of ownership over the hand. The former observations confirm that referral of touch and ownership are related experiences in the RHI. The latter, however, indicate that when pooling the statements one may obtain a higher number of illusion 'responders' compared to considering the ownership statements in isolation. These results have implications for the RHI as an experimental paradigm.

Weakening the subjective sensation of own hand ownership does not interfere with rapid finger movements.

When we perform a movement we generally have a clear distinction between which parts of the world constitute our body and which parts do not. However, how the sense of ownership over our body supports movement is not yet fully understood. We aimed to see whether a sense of ownership over the hand supports the performance of rapid hand movements. In three experiments (n = 48, n = 30, n = 24), we presented participants with congruent and incongruent visuotactile and visuoproprioceptive information regarding their own hand. In keeping with previous experiments, multisensory disintegration resulted in a reduction in the subjective sensation of ownership over the hand, as reflected in questionnaire responses. Following sensory stimulation, participants were required to rapidly abduct their index finger whilst the movement was tracked. We examined the hypothesis that, should a sense of ownership over the limb be necessary for generating rapid movements with that limb, reaction time would increase when hand ownership was reduced, whilst the acceleration and velocity of the movement would decrease. We observed that reductions in own hand ownership did not interfere with rapid index finger abduction, suggesting that the motor system may not be reliant on a subjective sense of ownership over the body in order to generate movement.

Repetitive Transcranial Magnetic Stimulation Over the Left Posterior Middle Temporal Gyrus Reduces Wrist Velocity During Emblematic Hand Gesture Imitation.

Results from neuropsychological studies, and neuroimaging and behavioural experiments with healthy individuals, suggest that the imitation of meaningful and meaningless actions may be reliant on different processing routes. The left posterior middle temporal gyrus (pMTG) is one area that might be important for the recognition and imitation of meaningful actions. We studied the role of the left pMTG in imitation using repetitive transcranial magnetic stimulation (rTMS) and two-person motion-tracking. Participants imitated meaningless and emblematic meaningful hand and finger gestures performed by a confederate actor whilst both individuals were motion-tracked. rTMS was applied during action observation (before imitation) over the left pMTG or a vertex control site. Since meaningless action imitation has been previously associated with a greater wrist velocity and longer correction period at the end of the movement, we hypothesised that stimulation over the left pMTG would increase wrist velocity and extend the correction period of meaningful actions (i.e., due to interference with action recognition). We also hypothesised that imitator accuracy (actor-imitator correspondence) would be reduced following stimulation over the left pMTG. Contrary to our hypothesis, we found that stimulation over the pMTG, but not the vertex, during action observation reduced wrist velocity when participants later imitated meaningful, but not meaningless, hand gestures. These results provide causal evidence for a role of the left pMTG in the imitation of meaningful gestures, and may also be in keeping with proposals that left posterior temporal regions play a role in the production of postural components of gesture.

Correction to: 'The left ventral premotor cortex is involved in hand shaping for intransitive gestures: evidence from a two-person imitation experiment'.

[This corrects the article DOI: 10.1098/rsos.181356.].

The left ventral premotor cortex is involved in hand shaping for intransitive gestures: evidence from a two-person imitation experiment.

The ventral premotor cortex (PMv) is involved in grasping and object manipulation, while the dorsal premotor cortex (PMd) has been suggested to play a role in reaching and action selection. These areas have also been associated with action imitation, but their relative roles in different types of action imitation are unclear. We examined the role of the left PMv and PMd in meaningful and meaningless action imitation by using repetitive transcranial magnetic stimulation (rTMS). Participants imitated meaningful and meaningless actions performed by a confederate actor while both individuals were motion-tracked. rTMS was applied over the left PMv, left PMd or a vertex control site during action observation or imitation. Digit velocity was significantly greater following stimulation over the PMv during imitation compared with stimulation over the PMv during observation, regardless of action meaning. Similar effects were not observed over the PMd or vertex. In addition, stimulation over the PMv increased finger movement speed in a (non-imitative) finger-thumb opposition task. We suggest that claims regarding the role of the PMv in object-directed hand shaping may stem from the prevalence of object-directed designs in motor control research. Our results indicate that the PMv may have a broader role in 'target-directed' hand shaping, whereby different areas of the hand are considered targets to act upon during intransitive gesturing.

A kinematic examination of dual-route processing for action imitation.

The dual-route model of imitation suggests that meaningful and meaningless actions are processed through either an indirect or a direct route, respectively. Evidence indicates that the direct route is more cognitively demanding since it relies on mapping visuospatial properties of the observed action on to a performed one. These cognitive demands might negatively influence reaction time and accuracy for actions performed following a meaningless action under time constraints. However, how meaningful and meaningless action imitation processing is reflected in movement kinematics is not yet clear. We wanted to confirm whether meaningless action performance incurs a reaction time cost, whether the cost is reflected in kinematics, and, more generally, to examine kinematic markers of emblematic meaningful and meaningless action imitation. We examined participants' reaction time and wrist movements when they imitated emblematic meaningful or matched meaningless gestures in either blocks of the same action type or mixed blocks. Meaningless actions were associated with a greater correction period at the end of the movement, possibly reflecting a strategy designed to ensure accurate completion for less familiar actions under time constraints. Furthermore, in mixed blocks, trials following meaningless actions had a significantly increased reaction time, supporting previous claims that route selection for action imitation may be stimulus-driven. However, there was only convincing evidence for this effect with an interval of ~2,948ms, but not ~3,573ms or ~2,553ms, between movements. Future work motion-tracking the entire hand to assess imitation accuracy, and more closely examining the influence of duration between movements, may help to explain these effects.

Repetitive transcranial magnetic stimulation reveals a role for the left inferior parietal lobule in matching observed kinematics during imitation.

Apraxia (a disorder of complex movement) suggests that the left inferior parietal lobule (IPL) plays a role in kinematic or spatial aspects of imitation, which may be particularly important for meaningless (i.e. unfamiliar intransitive) actions. Mirror neuron theories indicate that the IPL is part of a frontoparietal system that can support imitation by linking observed and stored actions through visuomotor matching, and have less to say about different subregions of the left IPL, or how different types of action (i.e. meaningful or meaningless) are processed for imitation. We used repetitive transcranial magnetic stimulation (rTMS) to bridge this gap and better understand the roles of the left supramarginal gyrus (SMG) and left angular gyrus (AG) in imitation. We also examined whether these areas are differentially involved in meaningful and meaningless action imitation. We applied rTMS over the left SMG, over the left AG or during a no-rTMS baseline condition, and then asked participants to imitate a confederate's actions whilst the arm and hand movements of both individuals were motion-tracked. rTMS over both the left SMG and the left AG reduced the velocity of participants' finger movements relative to the actor during imitation of finger gestures, regardless of action meaning. Our results support recent claims in apraxia and confirm a role for the left IPL in kinematic processing during gesture imitation, regardless of action meaning.

Optimal motor synergy extraction for novel actions and virtual environments.

Dimensionality reduction techniques such as factor analysis can be used to identify the smallest number of components (motor synergies) that explain motion. Lambert-Shirzad and Van der Loos (J Neurophysiol 117: 290-302, 2017) compared dimensionality reduction techniques in bimanual hand movements, concluding that nonnegative matrix factorization was the optimal technique for extracting meaningful synergies. Their results provide a useful measure for examining how the motor system deals with novel motor tasks that allow the actor to engage with a virtual environment.

Examining ecological validity in social interaction: problems of visual fidelity, gaze, and social potential.

Social interaction is an essential part of the human experience, and much work has been done to study it. However, several common approaches to examining social interactions in psychological research may inadvertently either unnaturally constrain the observed behaviour by causing it to deviate from naturalistic performance, or introduce unwanted sources of variance. In particular, these sources are the differences between naturalistic and experimental behaviour that occur from changes in visual fidelity (quality of the observed stimuli), gaze (whether it is controlled for in the stimuli), and social potential (potential for the stimuli to provide actual interaction). We expand on these possible sources of extraneous variance and why they may be important. We review the ways in which experimenters have developed novel designs to remove these sources of extraneous variance. New experimental designs using a 'two-person' approach are argued to be one of the most effective ways to develop more ecologically valid measures of social interaction, and we suggest that future work on social interaction should use these designs wherever possible.

Video stimuli reduce object-directed imitation accuracy: a novel two-person motion-tracking approach.

Imitation is an important form of social behavior, and research has aimed to discover and explain the neural and kinematic aspects of imitation. However, much of this research has featured single participants imitating in response to pre-recorded video stimuli. This is in spite of findings that show reduced neural activation to video vs. real life movement stimuli, particularly in the motor cortex. We investigated the degree to which video stimuli may affect the imitation process using a novel motion tracking paradigm with high spatial and temporal resolution. We recorded 14 positions on the hands, arms, and heads of two individuals in an imitation experiment. One individual freely moved within given parameters (moving balls across a series of pegs) and a second participant imitated. This task was performed with either simple (one ball) or complex (three balls) movement difficulty, and either face-to-face or via a live video projection. After an exploratory analysis, three dependent variables were chosen for examination: 3D grip position, joint angles in the arm, and grip aperture. A cross-correlation and multivariate analysis revealed that object-directed imitation task accuracy (as represented by grip position) was reduced in video compared to face-to-face feedback, and in complex compared to simple difficulty. This was most prevalent in the left-right and forward-back motions, relevant to the imitator sitting face-to-face with the actor or with a live projected video of the same actor. The results suggest that for tasks which require object-directed imitation, video stimuli may not be an ecologically valid way to present task materials. However, no similar effects were found in the joint angle and grip aperture variables, suggesting that there are limits to the influence of video stimuli on imitation. The implications of these results are discussed with regards to previous findings, and with suggestions for future experimentation.