[The contribution of forensic neuroscience to psychopathy]. / La psychopathie ­ L'éclairage des neurosciences médicolégales.

Psychopathy is a construct characterized by symptoms of emotional detachment, a lack of empathy, guilt and remorse, irresponsibility and a propensity for impulsive behavior. This article critically evaluates the contribution of structural and functional neuroimaging to the understanding of this personality disorder in North American forensic populations with psychopathic traits. Neuroimaging results are highly variable. They report numerous structural and functional abnormalities that are not limited to the amygdala and the ventromedial prefrontal cortex but include the striatum, hippocampus, and uncinate fasciculus. These brain abnormalities underlie an attenuated emotion processing functioning (but not an absence) and aversion to negative and threats signals, reinforcement learning, representation of rewards and modulation of attention that have an impact in decision-making, caring for others, and moral judgment. It is important to note that the neuroanatomical, neurofunctional, and behavioral differences between individuals with high psychopathic traits and those with low traits are highly heterogeneous and of degree rather than of nature.

Neural networks underlying implicit and explicit moral evaluations in psychopathy.

Psychopathy, characterized by symptoms of emotional detachment, reduced guilt and empathy and a callous disregard for the rights and welfare of others, is a strong risk factor for immoral behavior. Psychopathy is also marked by abnormal attention with downstream consequences on emotional processing. To examine the influence of task demands on moral evaluation in psychopathy, functional magnetic resonance imaging was used to measure neural response and functional connectivity in 88 incarcerated male subjects (28 with Psychopathy Checklist Revised (PCL-R) scores ⩾ 30) while they viewed dynamic visual stimuli depicting interpersonal harm and interpersonal assistance in two contexts, implicit and explicit. During the implicit task, high psychopathy was associated with reduced activity in the dorsolateral prefrontal cortex and caudate when viewing harmful compared with helpful social interactions. Functional connectivity seeded in the right amygdala and right temporoparietal junction revealed decreased coupling with the anterior cingulate cortex (ACC), anterior insula, striatum and ventromedial prefrontal cortex. In the explicit task, higher trait psychopathy predicted reduced signal change in ACC and amygdala, accompanied by decreased functional connectivity to temporal pole, insula and striatum, but increased connectivity with dorsal ACC. Psychopathy did not influence behavioral performance in either task, despite differences in neural activity and functional connectivity. These findings provide the first direct evidence that hemodynamic activity and neural coupling within the salience network are disrupted in psychopathy, and that the effects of psychopathy on moral evaluation are influenced by attentional demands.

The role of oxytocin in empathy to the pain of conflictual out-group members among patients with schizophrenia.

BACKGROUND: Oxytocin (OT) is associated with our ability to empathize and has been shown to play a major role in mediating social behaviors within the context of intergroup dynamics. Schizophrenia is associated with impaired empathy, and with a dysfunctional oxytocinergic system. The effect of OT on the empathic responses of patients with schizophrenia within the context of intergroup relationships has not been studied. The present study examined the effect of OT on the patients' empathic responses to pain experienced by in-group, conflictual out-group and neutral out-group members. METHOD: In a double-blind, placebo-controlled, within-subject cross-over design, the responses on the Pain Evaluation Task of 28 male patients with schizophrenia were compared to 27 healthy male controls. All participants received a single intranasal dose of 24 IU OT or placebo, 1 week apart. RESULTS: OT induced an empathy bias in the healthy controls towards the conflictual out-group members. Although this effect was absent in the patient group, OT seems to heighten an empathic bias in the patient group towards the in-group members when rating non-painful stimuli. CONCLUSIONS: The study demonstrates that the administration of OT can result in empathic bias towards adversary out-group members in healthy controls but not in patients with schizophrenia. However, the OT-induced bias in both the patients (in the no-pain condition towards the in-group members) and the healthy controls (in the no-pain and pain conditions towards the adversary out-group) suggests that OT enhances the distinction between conflictual in-group and out-group members.

I know the pain you feel-how the human brain's default mode predicts our resonance to another's suffering.

Introspective and self-referential in nature, the human brain's default mode network (DMN) is presumed to influence our behavior in response to the environment in predictive manner [Raichle ME, Gusnard DA (2005) J Comp Neurol 493:167-176; Bar M (2009) Philos Trans R Soc Lond B Biol Sci 364:1235-1243]. In the current study, we hypothesize that the strength of DMN-connectivity contributes to distinct introspective psychological processes in every-day social life such as the intuitive understanding of other people through inner representation of their affective states -e. g. his or her pain. 19 healthy individuals underwent functional MRI scanning, which consisted of a resting-state-scan followed by the presentation of visual stimuli depicting human limbs in painful and non-painful situations. After scanning, participants were asked to evaluate the stimuli in terms of pain intensity perceived from the first person perspective. Independent component analysis (ICA) demonstrated that higher integration of the left medial orbitofrontal cortex (BA 32) into the anterior default mode network (aDMN) was associated with higher post-scan pain ratings. Furthermore, the exposition to the "Pain"-pictures led to relative increases of aDMN-activity compared to "No Pain"-stimuli which were also correlated with the subjective pain intensity. The behaviorally predictive functional architecture during a task-free period supports the notion that the DMN serves as a "memory of the future" [Ingvar DH (1985) Hum Neurobiol 4:127-136] in terms of a neuronal cache, storing "a priori scripts," which are recalled to deal efficiently with upcoming environmental events. In addition, our results suggest that an individual predisposition to identify oneself with another's pain influences the automatic response of the DMN during the observation of painful situations.

Sex differences in the neuroanatomy of human mirror-neuron system: a voxel-based morphometric investigation.

Females frequently perform better in empathy, interpersonal sensitivity, and emotional recognition than do males. The mirror-neuron system has been proposed to play an important role in social cognition. It remains to be clarified, however, whether the neuroanatomy underlying the human mirror neuron system exhibits sex differences. With the use of voxel-based morphometry analysis, a whole-brain unbiased technique to characterize regional cerebral volume differences in structural magnetic resonance images, concurrent with the dispositional empathy measures, we demonstrate that young adult females (n=25) had significantly larger gray matter volume in the pars opercularis and inferior parietal lobule than matched males (n=25) participants. Moreover, higher self-report scores in the emotional empathic disposition was tightly coupled with larger gray matter volume of the pars opercularis across all female and male participants (P=0.002). These results indicate that the existence of neuroanatomical sex differences in the human mirror-neuron system. They also suggest that the network of the human mirror-neuron system is strongly linked to empathy competence.

Perspective taking is associated with specific facial responses during empathy for pain.

Witnessing the distress of others can result both in empathy and personal distress. Perspective-taking has been assigned a major role in the elicitation and modulation of these vicarious responses. However, little is known about how perspective-taking affects the psychophysiological correlates of empathy vs. personal distress. We recorded facial electromyographic and electrocardiographic activity while participants watched videos of patients undergoing painful sonar treatment. These videos were watched using two distinct perspectives: a) imagining the patient's feelings ('imagine other'), or b) imagining to be in the patient's place ('imagine self'). The results revealed an unspecific frowning response as well as activity over the M. orbicularis oculi region which was specific to the 'imagine self' perspective. This indicates that the pain-related tightening of the patients orbits was matched by participants when adopting this perspective. Our findings provide a physiological explanation for the more direct personal involvement and higher levels of personal distress associated with putting oneself explicitly into someone elses shoes. They provide further evidence that empathy does not only rely on automatic processes, but is also strongly influenced by top-down control and cognitive processes.

The detection of intentional contingencies in simple animations in patients with delusions of persecution.

BACKGROUND: It has been proposed that delusions of persecution are caused by the tendency to over-attribute malevolent intentions to other people's actions. One aspect of intention attribution is detecting contingencies between an agent's actions and intentions. Here, we used simplified stimuli to test the hypothesis that patients with persecutory delusions over-attribute contingency to agents' movements. METHOD: Short animations were presented to three groups of subjects: (1) schizophrenic patients; (2) patients with affective disorders; and (3) normal control subjects. Patients were divided on the basis of the presence or absence of delusions of persecution. Participants watched four types of film featuring two shapes. In half the films one shape's movement was contingent on the other shape. Contingency was either 'intentional': one shape moved when it 'saw' another shape; or 'mechanical': one shape was launched by the other shape. Subjects were asked to rate the strength of the relationship between the movement of the shapes. RESULTS: Normal control subjects and patients without delusions of persecution rated the relationship between the movement of the shapes as stronger in both mechanical and intentional contingent conditions than in non-contingent conditions. In contrast, there was no significant difference between the ratings of patients with delusions of persecution for the conditions in which movement was animate. Patients with delusions of persecution perceived contingency when there was none in the animate non-contingent condition. CONCLUSIONS: The results suggest that delusions of persecution may be associated with the over-attribution of contingency to the actions of agents.

The detection of contingency and animacy from simple animations in the human brain.

Contingencies between objects and people can be mechanical or intentional-social in nature. In this fMRI study we used simplified stimuli to investigate brain regions involved in the detection of mechanical and intentional contingencies. Using a factorial design we manipulated the 'animacy' and 'contingency' of stimulus movement, and the subject's attention to the contingencies. The detection of mechanical contingency between shapes whose movement was inanimate engaged the middle temporal gyrus and right intraparietal sulcus. The detection of intentional contingency between shapes whose movement was animate activated superior parietal networks bilaterally. These activations were unaffected by attention to contingency. Additional regions, the right middle frontal gyrus and left superior temporal sulcus, became activated by the animate-contingent stimuli when subjects specifically attended to the contingent nature of the stimuli. Our results help to clarify neural networks previously associated with 'theory of mind' and agency detection. In particular, the results suggest that low-level perception of agency in terms of objects reacting to other objects at a distance is processed by parietal networks. In contrast, the activation of brain regions traditionally associated with theory of mind tasks appears to require attention to be directed towards agency and contingency.

Modulating the experience of agency: a positron emission tomography study.

This study investigated agency, the feeling of being causally involved in an action. This is the feeling that leads us to attribute an action to ourselves rather than to another person. We were interested in the effects of experimentally modulating this experience on brain areas known to be involved in action recognition and self-recognition. We used a device that allowed us to modify the subject's degree of control of the movements of a virtual hand presented on a screen. Four main conditions were used: (1) a condition where the subject had a full control of the movements of the virtual hand, (2) a condition where the movements of the virtual hand appeared rotated by 25 degrees with respect to the movements made by the subject, (3) a condition where the movements of the virtual hand appeared rotated by 50 degrees, and (4) a condition where the movements of the virtual hand were produced by another person and did not correspond to the subject's movements. The activity of two main brain areas appeared to be modulated by the degree of discrepancy between the movement executed and the movement seen on the screen. In the inferior part of the parietal lobe, specifically on the right side, the less the subject felt in control of the movements of the virtual hand, the higher the level of activation. A reverse covariation was observed in the insula. These results demonstrate that the level of activity of specific brain areas maps onto the experience of causing or controlling an action. The implication of these results for understanding pathological conditions is discussed.

[Naturalizing empathy]. / Naturaliser l'empathie.

Empathy is the ability to share emotions with others. It is acknowledged to be a powerful means of tacit communication, a key ingredient in any therapeutic relationship as well as in psychotherapy. Empathy is the cornerstone in the humanist perspective (Ego-psychology) in clinical psychology. This approach is often considered as poorly grounded on scientific and objective evidence. It is however acknowledged that empathetic therapists are more effective than less empathetic therapists. I shall argue that this paradox, i.e. it is the least scientific and the less validated psychotherapeutic approach that is the most efficient, can be eliminated if one considers the nature of empathy, its biological foundation, its evolutionary origin and its cognitive architecture. In this paper I will suggest that empathy is based on specific information processing modules which have been designed by natural selection to cope with social regularities in expressing and reading emotional states. This has provided adaptive benefits to individuals living in large groups bestowing them with mechanisms for cooperativity, altruism and more generally various aspects of prosocial behaviour. The capacity to express emotions, and to read and understand emotions of others also ensures implicit communication with others and may be at the root of intersubjectivity. This perspective on empathy is then articulated with two concurrent hypotheses regarding theory of mind (the simulation and the theory-theory) which aim to explain the human capacity to understand that the behaviors of other intelligent agents are caused by intentions, desires and beliefs. In this context, empathy can be considered as a simulation (or analogical) process that is necessary to understand but not sufficient to interpret other people. This last issue is relevant to clinical practice.

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.

Is perceptual anticipation a motor simulation? A PET study.

A large body of psychophysical evidence suggests that perception of human movement is constrained by the observer's motor competence. PET measurements of regional cerebral blood flow were performed in eight healthy subjects who were requested, in a forced-choice paradigm, to anticipate the outcome of a single moving dot trajectory depicting the beginning of either mechanical, pointing, or writing movements. Selective activation of the left premotor cortex and of the right intraparietal sulcus was associated with visual anticipation of pointing movements while the left frontal operculum and superior parietal lobule were found to be activated during anticipation of writing movements. These results are discussed in the perspective that the motor system is part of a simulation network, which is used to interpret perceived actions.

How the brain perceives causality: an event-related fMRI study.

Detection of the causal relationships between events is fundamental for understanding the world around us. We report an event-related fMRI study designed to investigate how the human brain processes the perception of mechanical causality. Subjects were presented with mechanically causal events (in which a ball collides with and causes movement of another ball) and non-causal events (in which no contact is made between the balls). There was a significantly higher level of activation of V5/MT/MST bilaterally, the superior temporal sulcus bilaterally and the left intraparietal sulcus to causal relative to non-causal events. Directing attention to the causal nature of the stimuli had no significant effect on the neural processing of the causal events. These results support theories of causality suggesting that the perception of elementary mechanical causality events is automatically processed by the visual system.

Different brain correlates for watching real and virtual hand actions.

We investigated whether observation of actions reproduced in three-dimensional virtual reality would engage perceptual and visuomotor brain processes different from those induced by the observation of real hand actions. Participants were asked to passively observe grasping actions of geometrical objects made by a real hand or by hand reconstructions of different quality in 3D virtual reality as well as on a 2D TV screen. We found that only real actions in natural environment activated a visuospatial network including the right posterior parietal cortex. Observation of virtual-reality hand actions engaged prevalent visual perceptual processes within lateral and mesial occipital regions. Thus, only perception of actions in reality maps onto existing action representations, whereas virtual-reality conditions do not access the full motor knowledge available to the central nervous system.

Effect of subjective perspective taking during simulation of action: a PET investigation of agency.

Perspective taking is an essential component in the mechanisms that account for intersubjectivity and agency. Mental simulation of action can be used as a natural protocol to explore the cognitive and neural processing involved in agency. Here we took PET measurements while subjects simulated actions with either a first-person or a third-person perspective. Both conditions were associated with common activation in the SMA, the precentral gyrus, the precuneus and the MT/V5 complex. When compared to the first-person perspective, the third-person perspective recruited right inferior parietal, precuneus, posterior cingulate and frontopolar cortex. The opposite contrast revealed activation in left inferior parietal and somatosensory cortex. We suggest that the right inferior parietal, precuneus and somatosensory cortex are specifically involved in distinguishing self-produced actions from those generated by others.

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.