Prioritized neural processing of social threats during perceptual decision-making.

Emotional signals, notably those signaling threat, benefit from prioritized processing in the human brain. Yet, it remains unclear whether perceptual decisions about the emotional, threat-related aspects of stimuli involve specific or similar neural computations compared to decisions about their non-threatening/non-emotional components. We developed a novel behavioral paradigm in which participants performed two different detection tasks (emotion vs. color) on the same, two-dimensional visual stimuli. First, electroencephalographic (EEG) activity in a cluster of central electrodes reflected the amount of perceptual evidence around 100 ms following stimulus onset, when the decision concerned emotion, not color. Second, participants' choice could be predicted earlier for emotion (240 ms) than for color (380 ms) by the mu (10 Hz) rhythm, which reflects motor preparation. Taken together, these findings indicate that perceptual decisions about threat-signaling dimensions of facial displays are associated with prioritized neural coding in action-related brain regions, supporting the motivational value of socially relevant signals.

Can we simulate an action that we temporarily cannot perform?

AIMS OF THE STUDY: The scope of individuals' motor repertoire and expertise influences the way they perceive the actions of others. When observing skilled actions, experts recruit the cortical network subserving action perception (action observation network, AON) to a greater extent than non-experts. However, it remains unknown whether and how a temporary motor injury affects activation within the AON. MATERIALS AND METHODS: To investigate this issue, brain hemodynamic activity was recorded twice in thirteen national female gymnasts suffering from a lower extremity injury at the onset of the experiment. The gymnasts were scanned one month after the injury and were shown gymnastics routines they were able and temporarily unable to perform. Six months later, after complete recovery, they were scanned again and shown the same routines they were now able to practice. RESULTS: Results showed: first, that the level of activity within the inferior parietal lobule and MT/V5/EBA (extrastriate body area), areas constitutive of the AON, was independent of the gymnasts' physical condition. Second, when gymnasts were hurt (vs. when recovered), higher activity in the cerebellum was detected. CONCLUSION: The equal contribution of MT/V5/EBA and inferior parietal lobule during the observation of movements the gymnasts were able or unable to practice suggests respectively that physical provisional incapacity does not interfere with the perceptual processing of body shape and motion information, and that motor expertise may prevent the decay of sensorimotor representations. Higher activations in the cerebellum may suggest that this structure plays a role in dissociating perceived physically feasible movements from those that are provisionally unfeasible.

Similarities and differences in perceiving threat from dynamic faces and bodies. An fMRI study.

Neuroscientific research on the perception of emotional signals has mainly focused on how the brain processes threat signals from photographs of facial expressions. Much less is known about body postures or about the processing of dynamic images. We undertook a systematic comparison of the neurofunctional network dedicated to processing facial and bodily expressions. Two functional magnetic resonance imaging (fMRI) experiments investigated whether areas involved in processing social signals are activated differently by threatening signals (fear and anger) from facial or bodily expressions. The amygdala (AMG) was more active for facial than for bodily expressions. Body stimuli triggered higher activation than face stimuli in a number of areas. These were the cuneus, fusiform gyrus (FG), extrastriate body area (EBA), temporoparietal junction (TPJ), superior parietal lobule (SPL), primary somatosensory cortex (SI), as well as the thalamus. Emotion-specific effects were found in TPJ and FG for bodies and faces alike. EBA and superior temporal sulcus (STS) were more activated by threatening bodies.

A failure to grasp the affective meaning of actions in autism spectrum disorder subjects.

The ability to grasp emotional messages in everyday gestures and respond to them is at the core of successful social communication. The hypothesis that abnormalities in socio-emotional behavior in people with autism are linked to a failure to grasp emotional significance conveyed by gestures was explored. We measured brain activity using fMRI during perception of fearful or neutral actions and showed that whereas similar activation of brain regions known to play a role in action perception was revealed in both autistics and controls, autistics failed to activate amygdala, inferior frontal gyrus and premotor cortex when viewing gestures expressing fear. Our results support the notion that dysfunctions in this network may contribute significantly to the characteristic communicative impairments documented in autism.

Decreased differential activity in the amygdala in response to fearful expressions in Type D personality.

Recent advances in functional brain imaging offer unique opportunities to explore the neurofunctional basis of tools used to assess personality differences which have proven their clinical usefulness. In this functional magnetic resonance imaging (fMRI) study, the focus was on the amygdala activation and we investigated whether individual differences in activity of the amygdala following presentation of emotional expressions in the face and the whole body may be systematically related to the presence of Type D (distressed) personality or to its constituting factors, Negative Affectivity (NA) and Social Inhibition (SI). Our results show that the observed difference in amygdala activity between fearful and neutral expressions was present in participants that did not meet the criteria for Type D personality, while this effect was absent in participants that could be classified as Type D personality. Our correlation analyses further showed that the activation in the left amygdala elicited by fearful versus neutral bodily expressions correlated negatively with the Negative Affectivity score. The same pattern was observed for the right amygdala for fearful facial and bodily expressions when contrasted with neutral facial and bodily expressions.

What is "mirror" in the premotor cortex? A review.

We review the findings of 24 fMRI studies examining activations in the premotor cortex (Brodmann's areas 6 and 44) during passive observation of actions. We found that such activations regularly occurred. Looking for functional differentiation in the premotor cortex, we found that one parameter was associated with systematic differences in location: this was the presence or absence of targets. Observing biological actions with a physical target, compared to a visual control showing no action at all, consistently activated the ventral premotor cortex (BA 6), and did so significantly more than observing target-less actions (with the same control). In contrast, the activity in BA 44 ("Broca's area") was not modulated by the presence or absence of targets. We propose that the ventral precentral gyrus, and not BA 44, shares the visual properties of "mirror" neurons found in area F5 of the macaque brain.

Rapid detection of fear in body expressions, an ERP study.

Recent findings indicate that the perceptual processing of fearful expressions in the face can already be initiated around 100-120 ms after stimulus presentation, demonstrating that emotional information of a face can be encoded before the identity of the face is fully recognized. At present it is not clear whether fear signals from body expressions may be encoded equally as rapid. To answer this question we investigated the early temporal dynamics of perceiving fearful body expression by measuring EEG. Participants viewed images of whole body actions presented either in a neutral or a fearful version. We observed an early emotion effect on the P1 peak latency around 112 ms post stimulus onset hitherto only found for facial expressions. Also consistent with the majority of facial expression studies, the N170 component elicited by perceiving bodies proved not to be sensitive for the expressed fear. In line with previous work, its vertex positive counterpart, the VPP, did show a condition-specific influence for fearful body expression. Our results indicate that the information provided by fearful body expression is already encoded in the early stages of visual processing, and suggest that similar early processing mechanisms are involved in the perception of fear in faces and bodies.

Perceiving fear in dynamic body expressions.

Characteristic fear behaviour like putting the hands in front of the face and running for cover provides strong fear signals to observers who may not themselves be aware of any danger. Using event-related functional magnetic resonance imaging (fMRI) in humans, we investigated how such dynamic fear signals from the whole body are perceived. A factorial design allowed us to investigate brain activity induced by viewing bodies, bodily expressions of fear and the role of dynamic information in viewing them. Our critical findings are threefold. We find that viewing neutral and fearful body expressions enhances amygdala activity; moreover actions expressing fear activate the temporal pole and lateral orbital cortex more than neutral actions; and finally differences in activations between static and dynamic bodily expressions were larger for actions expressing fear in the STS and premotor cortex compared to neutral actions.

Affective response to one's own moral violations.

Morality depends on a set of cultural rules that regulate interpersonal behaviour and provide a basis for social cohesion. The interpretation of moral transgressions and their affective consequences depends on whether the action is intentional or accidental, and whether one is the agent of or witness to the action. We used event-related functional magnetic resonance imaging (fMRI) to investigate whether the amygdala is involved in judging one's own moral violation of social norms. In this study, participants (n = 12) were asked to make evaluations regarding the degree of inappropriateness of social behaviours described in stories in which they themselves, or someone else, transgressed social norms either intentionally or accidentally. Consistent with our hypothesis, the amygdala was activated when participants considered stories narrating their own intentional transgression of social norms. This result suggests the amygdala is important for affective responsiveness to moral transgressions.

Amygdala activation when one is the target of deceit: did he lie to you or to someone else?

The ability to figure out whether a person is being honest or deceitful is an important part of social competence. Reactions to deceit may however differ depending on whether one is being deceived oneself or observes a deceitful exchange between others. In the present study, we investigated whether personal involvement influenced the neural responses associated with the detection of deceit. Subjects watched videos of actors lifting a box and judged whether the actors had been misled about the real weight of the box. Personal involvement was manipulated by having the participants themselves among the actors. The critical finding was that there was activity in amygdala and fusiform gyrus only for the condition in which participants observed themselves being deceived. In contrast, the superior temporal sulcus and anterior cingulate cortex were activated irrespective of whether the participants detected that the experimenter had deceived themselves or another. These four brain areas are all interconnected and are part of the discrete neural system subserving social cognition. Our results provide direct evidence, using judgments of deceit in a social context, that the crucial factor for amygdala activation is the involvement of the subjects because they are the target of the deceit. We interpret the activation of the amygdala in this situation as reflecting the greater affective reaction when one is deceived oneself. Our results suggest that when one is personally involved, deceit is taken as a potential threat.

Action observation and acquired motor skills: an FMRI study with expert dancers.

When we observe someone performing an action, do our brains simulate making that action? Acquired motor skills offer a unique way to test this question, since people differ widely in the actions they have learned to perform. We used functional magnetic resonance imaging to study differences in brain activity between watching an action that one has learned to do and an action that one has not, in order to assess whether the brain processes of action observation are modulated by the expertise and motor repertoire of the observer. Experts in classical ballet, experts in capoeira and inexpert control subjects viewed videos of ballet or capoeira actions. Comparing the brain activity when dancers watched their own dance style versus the other style therefore reveals the influence of motor expertise on action observation. We found greater bilateral activations in premotor cortex and intraparietal sulcus, right superior parietal lobe and left posterior superior temporal sulcus when expert dancers viewed movements that they had been trained to perform compared to movements they had not. Our results show that this 'mirror system' integrates observed actions of others with an individual's personal motor repertoire, and suggest that the human brain understands actions by motor simulation.

Inferring false beliefs from the actions of oneself and others: an fMRI study.

The ability to make judgments about mental states is critical to social interactions. Simulation theory suggests that the observer covertly mimics the activity of the observed person, leading to shared states of mind between the observer and the person observed. We tested this hypothesis by investigating the neural networks activated while subjects watched videos of themselves and of others lifting a box, and judged the beliefs of the actors about the weight of the box. A parietal premotor circuit was recruited during action perception, and the activity started earlier when making judgments about one's own actions as opposed to those of others. This earlier activity in action-related structures can be explained by simulation theory on the basis that when one observes one's own actions, there is a closer match between the simulated and perceived action than there is when one observes the actions of others. When the observers judged the actions to reflect a false belief, there was activation in the superior temporal sulcus, orbitofrontal, paracingulate cortex and cerebellum. We suggest that this reflects a mismatch between the perceived action and the predicted action's outcomes derived from simulation.

Objects automatically potentiate action: an fMRI study of implicit processing.

Behavioural data have shown that the perception of an object automatically potentiates motor components (affordances) of possible actions toward that object, irrespective of the subject's intention. We carried out an event-related fMRI study to investigate the influence of the intrinsic properties of an object on motor responses which were either compatible or incompatible with the action that the object affords. The subjects performed power or precision grip responses based on the categorization of objects into natural or man-made. The objects were either 'small' (usually grasped with a precision grip) or 'large' (usually grasped with a power grip). As expected, the motor responses were fastest to objects that afforded the same grip (congruent) and slowest to objects that afforded the other grip (incongruent). Imaging revealed activations which covaried with compatibility in the parietal, dorsal premotor and inferior frontal cortex. We suggest that the greater the difference in reaction times between congruent and incongruent trials, the greater the competition between the action afforded by the object and the action specified by the task, and thus the greater the activation within this network.

Activations related to "mirror" and "canonical" neurones in the human brain: an fMRI study.

In the macaque monkey ventral premotor cortex (F5), "canonical neurones" are active when the monkey observes an object and when the monkey grasps that object. In the same area, "mirror neurones" fire both when the monkey observes another monkey grasping an object and when the monkey grasps that object. We used event-related fMRI to investigate where in the human brain activation can be found that reflects both canonical and mirror neuronal activity. There was activation in the intraparietal and ventral limbs of the precentral sulcus when subjects observed objects and when they executed movements in response to the objects (canonical neurones). There was activation in the dorsal premotor cortex, the intraparietal cortex, the parietal operculum (SII), and the superior temporal sulcus when subjects observed gestures (mirror neurones). Finally, activations in the ventral premotor cortex and inferior frontal gyrus (area 44) were found when subjects imitated gestures and executed movements in response to objects. We suggest that in the human brain, the ventral limb of the precentral sulcus may form part of the area designated F5 in the macaque monkey. It is possible that area 44 forms an anterior part of F5, though anatomical studies suggest that it may be a transitional area between the premotor and prefrontal cortices.

A PET exploration of the neural mechanisms involved in reciprocal imitation.

Imitation is a natural mechanism involving perception-action coupling which plays a central role in the development of understanding that other people, like the self, are mental agents. PET was used to examine the hemodynamic changes occurring in a reciprocal imitation paradigm. Eighteen subjects (a) imitated the actions of the experimenter, (b) had their actions imitated by the experimenter, (c) freely produced actions, or (d) freely produced actions while watching different actions made by the experimenter. In a baseline condition, subjects simply watched the experimenter's actions. Specific increases were detected in the left STS and in the inferior parietal cortex in conditions involving imitation. The left inferior parietal is specifically involved in producing imitation, whereas the right homologous region is more activated when one's own actions are imitated by another person. This pattern of results suggests that these regions play a specific role in distinguishing internally produced actions from those generated by others.

Does visual perception of object afford action? Evidence from a neuroimaging study.

Positron emission tomography (PET) was used to explore the neural correlates of a potential involvement of motor representation during the perception of visually presented objects with different tasks. The main result of this study was that the perception of objects, irrespective of the task (judgement of the vertical orientation, motor imagery, and silent generation of the noun or of the corresponding action verb), versus perception of non-objects, was associated with rCBF increases in a common set of cortical regions. The occipito-temporal junction, the inferior parietal lobule, the SMA-proper, the pars triangularis in the inferior frontal gyrus, the dorsal and ventral precentral gyrus were engaged in the left hemisphere. The ipsilateral cerebellum was also involved. These activations are congruent with the idea of an involvement of motor representation already during the perception of object and thus provide neurophysiological evidence that the perception of objects automatically affords actions that can be made toward them. Besides this common set of cortical areas, each task engaged specific regions.

Does perception of biological motion rely on specific brain regions?

Perception of biological motions plays a major adaptive role in identifying, interpreting, and predicting the actions of others. It may therefore be hypothesized that the perception of biological motions is subserved by a specific neural network. Here we used fMRI to verify this hypothesis. In a group of 10 healthy volunteers, we explored the hemodynamic responses to seven types of visual motion displays: drifting random dots, random dot cube, random dot cube with masking elements, upright point-light walker, inverted point-light walker, upright point-light walker display with masking elements, and inverted point-light walker display with masking elements. A gradient in activation was observed in the occipitotemporal junction. The responses to rigid motion were localized posteriorly to those responses elicited by nonrigid motions. Our results demonstrate that in addition to the posterior portion of superior temporal sulcus, the left intraparietal cortex is involved in the perception of nonrigid biological motions.

Functional anatomy of execution, mental simulation, observation, and verb generation of actions: a meta-analysis.

There is a large body of psychological and neuroimaging experiments that have interpreted their findings in favor of a functional equivalence between action generation, action simulation, action verbalization, and perception of action. On the basis of these data, the concept of shared motor representations has been proposed. Indeed several authors have argued that our capacity to understand other people's behavior and to attribute intention or beliefs to others is rooted in a neural, most likely distributed, execution/observation mechanism. Recent neuroimaging studies have explored the neural network engaged during motor execution, simulation, verbalization, and observation. The focus of this metaanalysis is to evaluate in specific detail to what extent the activated foci elicited by these studies overlap.

The effects of learning and intention on the neural network involved in the perception of meaningless actions.

PET was used to explore the neural network involved in the perception of meaningless action. In two conditions, subjects observed learned and unknown meaningless actions without any purpose. In two other conditions, subjects observed the same type of stimuli for later imitation. The control condition, which consisted of the presention of stationary hands, served as a baseline. Unsurprisingly, a common network that forms part of the dorsal pathway was engaged in all conditions when compared with stationary hands, and this was interpreted as being devoted to the analysis of hand movements. One of the most striking results of the present study was that some brain areas were strongly modulated by the learning level, independent of the subject's intention. Two different effects were observed: a reduced activity in posterior regions within the common network, which correlated with specific increases in the frontopolar area 10 and in the angular gyrus during the perception of learned meaningless actions compared with the perception of unknown actions. Finally, the major effect of the subject's intention to imitate was a strong increase in the dorsal pathway extending to the lateral premotor cortex and to the dorsolateral prefrontal cortex, which reflects the information processing needed for prospective action. Overall, our results provide evidence for both an effect of the visuomotor learning level and of the subject's intention on the neural network involved during the perception of human meaningless actions.

Neural mechanisms subserving the perception of human actions.

Our ability to generate actions and to recognize actions performed by others is the bedrock of our social life. Behavioral evidence suggests that the processes underlying perception and action might share a common representational framework. That is, observers might understand the actions of another individual in terms of the same neural code that they use to produce the same actions themselves. What neurophysiological evidence, if any, supports such a hypothesis? In this article, brain imaging studies addressing this question are reviewed and examined in the light of the functional segregation of the perceptual mechanisms subtending visual recognition and those used for action. We suggest that there are not yet conclusive arguments for a clear neurophysiological substrate supporting a common coding between perception and action.