To what extent do we share the pain of others? Insight from the neural bases of pain empathy.
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Biomedical subjects
Publications and source records attributed to Philip L Jackson.
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Is it important to adopt the perspective of the model when learning a new skill? Is the "mirror system" equally involved when the teacher is facing or side-by-side with students? In this functional MRI study, we measured the cerebral hemodynamic changes in participants who watched video-clips depicting simple hand or foot actions. The participants either watched passively or imitated these actions. Half the video-clips depicted actions filmed from the perspective of the participant (1st-person perspective) and half from a frontal view as if watching someone else (3rd-person perspective). Behavioral results showed that latency to imitate was significantly shorter for the 1st-person perspective than the 3rd-person perspective. Functional imaging results demonstrate that the observation of intransitive actions engaged primary visual and extrastriate visual areas, but not the premotor cortex. Imitation vs. observation of actions yielded enhanced signal in the contralateral somatosensory and motor cortices, cerebellum, left inferior parietal lobule and superior parietal cortex, and left ventral premotor cortex. Activity in the lateral occipital cortex around the extrastriate body area was significantly enhanced during imitation, as compared to observation of actions confirming that this region involvement reaches beyond the perception of body parts. Moreover, comparisons of the two visual perspectives showed more activity in the left sensory-motor cortex for 1st-person, even during observation alone, and in the lingual gyrus for 3rd-person perspective. These findings suggest that the 1st-person perspective is more tightly coupled to the sensory-motor system than the 3rd-person perspective, which requires additional visuospatial transformation.
Perspective-taking is a stepping stone to human empathy. When empathizing with another individual, one can imagine how the other perceives the situation and feels as a result. To what extent does imagining the other differs from imagining oneself in similar painful situations? In this functional magnetic resonance imaging experiment, participants were shown pictures of people with their hands or feet in painful or non-painful situations and instructed to imagine and rate the level of pain perceived from different perspectives. Both the Self's and the Other's perspectives were associated with activation in the neural network involved in pain processing, including the parietal operculum, anterior cingulate cortex (ACC; BA32) and anterior insula. However, the Self-perspective yielded higher pain ratings and involved the pain matrix more extensively in the secondary somatosensory cortex, the ACC (BA 24a'/24b'), and the insula proper. Adopting the perspective of the Other was associated with specific increase in the posterior cingulate/precuneus and the right temporo-parietal junction. These results show the similarities between Self- and Other-pain representation, but most interestingly they also highlight some distinctiveness between these two representations, which is a crucial aspect of human empathy. It may be what allows us to distinguish empathic responses to others versus our own personal distress. These findings are consistent with the view that empathy does not involve a complete Self-Other merging.
To what extent do we share feelings with others? Neuroimaging investigations of the neural mechanisms involved in the perception of pain in others may cast light on one basic component of human empathy, the interpersonal sharing of affect. In this fMRI study, participants were shown a series of still photographs of hands and feet in situations that are likely to cause pain, and a matched set of control photographs without any painful events. They were asked to assess on-line the level of pain experienced by the person in the photographs. The results demonstrated that perceiving and assessing painful situations in others was associated with significant bilateral changes in activity in several regions notably, the anterior cingulate, the anterior insula, the cerebellum, and to a lesser extent the thalamus. These regions are known to play a significant role in pain processing. Finally, the activity in the anterior cingulate was strongly correlated with the participants' ratings of the others' pain, suggesting that the activity of this brain region is modulated according to subjects' reactivity to the pain of others. Our findings suggest that there is a partial cerebral commonality between perceiving pain in another individual and experiencing it oneself. This study adds to our understanding of the neurological mechanisms implicated in intersubjectivity and human empathy.
Accumulative empirical evidence has been reviewed in support of the notion that the production and perception of action as well as the interpretation of others' actions are functionally connected, and indeed, rely on common distributed neural systems in the premotor and parietal cortices. We suggest that these neural systems sustain shared representations between self and other that are crucial in social interactions. The inferior parietal cortex plays a special role in the sense of agency, which is a fundamental aspect to navigate within this neural network. The role of other brain areas that implement and regulate these shared representations remains to be specified.
Cooperation and competition are two basic modes of social cognition that necessitate monitoring of both one's own and others' actions, as well as adopting a specific mental set. In this fMRI, study individuals played a specially designed computer game, according to a set of predefined rules, either in cooperation with or in competition against another person. The hemodynamic response during these conditions was contrasted to that of the same subjects playing the game independently. Both cooperation and competition stances resulted in activation of a common frontoparietal network subserving executive functions, as well as the anterior insula, involved in autonomic arousal. Moreover, distinct regions were found to be selectively associated with cooperation and competition, notably the orbitofrontal cortex in the former and the inferior parietal and medial prefrontal cortices in the latter. This pattern reflects the different mental frameworks implicated in being cooperative versus competitive with another person. In accordance with evidence from evolutionary psychology as well as from developmental psychology, we argue that cooperation is a socially rewarding process and is associated with specific left medial orbitofrontal cortex involvement.
OBJECTIVE: To investigate the effect of mental practice on the learning of a sequential task for the lower limb in a patient with a hemiparesis resulting from a stroke. DESIGN: A single-case study. SETTING: Research laboratory of a university-affiliated rehabilitation center. PATIENT: A right-handed 38-year-old man who had suffered a left hemorrhagic subcortical stroke 4 months prior. INTERVENTION: The patient practiced a serial response time task with the lower limb in 3 distinct training phases over a period of 5 weeks: 2 weeks of physical practice, 1 week of combined physical and mental practice, and then 2 weeks of mental practice alone. MAIN OUTCOME MEASURES: Performance on the task measured through errors and response times. Imagery abilities measured through questionnaires. RESULTS: The patient's average response time improved significantly during the 1st 5 days of physical practice (26%) but then failed to show further improvement during the following week of physical practice. The combination of mental and physical practice during the 3rd week yielded additional improvement (10.3%), whereas the following 2 weeks of mental practice resulted in a marginal increase in performance (2.2%). CONCLUSION: The findings show that mental practice, when combined with physical practice, can improve the performance of a sequential motor skill in people who had a stroke, and suggest that mental practice could play a role in the retention of newly acquired abilities.
Empathy accounts for the naturally occurring subjective experience of similarity between the feelings expressed by self and others without loosing sight of whose feelings belong to whom. Empathy involves not only the affective experience of the other person's actual or inferred emotional state but also some minimal recognition and understanding of another's emotional state. In light of multiple levels of analysis ranging from developmental psychology, social psychology, cognitive neuroscience, and clinical neuropsychology, this article proposes a model of empathy that involves parallel and distributed processing in a number of dissociable computational mechanisms. Shared neural representations, self-awareness, mental flexibility, and emotion regulation constitute the basic macrocomponents of empathy, which are underpinned by specific neural systems. This functional model may be used to make specific predictions about the various empathy deficits that can be encountered in different forms of social and neurological disorders.
Positron emission tomography (PET) was used to study the involvement of supraspinal structures in human locomotion. Six right-handed adults were scanned in four conditions while imagining locomotor-related tasks in the first person perspective: Standing (S), Initiating gait (IG), Walking (W) and Walking with obstacles (WO). When these conditions were compared to a rest (control) condition to identify the neural structures involved in the imagination of locomotor-related tasks, the results revealed a common pattern of activations, which included the dorsal premotor cortex and precuneus bilaterally, the left dorsolateral prefrontal cortex, the left inferior parietal lobule, and the right posterior cingulate cortex. Additional areas involving the pre-supplementary motor area (pre-SMA), the precentral gyrus, were activated during conditions that required the imagery of locomotor movements. Further subtractions between the different locomotor conditions were then carried out to determine the cerebral regions associated with the simulation of increasingly complex locomotor functions. These analyses revealed increases in rCBF activity in the left cuneus and left caudate when the W condition was compared to the IG condition, suggesting that the basal ganglia plays a role in locomotor movements that are automatic in nature. Finally, subtraction of the W from the WO condition yielded increases in activity in the precuneus bilaterally, the left SMA, the right parietal inferior cortex and the left parahippocampal gyrus. Altogether, the present findings suggest that higher brain centers become progressively engaged when demands of locomotor tasks require increasing cognitive and sensory information processing.
The goal of the present study was to examine, via positron emission tomography, the functional changes associated with the learning of a sequence of foot movements through mental practice with motor imagery (MI). Following intensive MI training over several days, which led to a modest but significant improvement in performance, healthy subjects showed an increase in activity restricted to the medial aspect of the orbitofrontal cortex (OFC), and a decrease in the cerebellum. These main results are largely consistent with those found in a previous study of sequence learning performed in our laboratory after physical practice of the same task [NeuroImage 16 (2002) 142]. Further analyses showed a positive correlation between the blood flow increase in the OFC and the percentage of improvement on the foot sequence task. Moreover, the increased involvement of the medial OFC revealed a modality specific anatomo-functional organization, as imagination of the sequential task after MI practice activated a more posterior region than its execution. These results demonstrate that learning a sequential motor task through motor imagery practice produces cerebral functional changes similar to those observed after physical practice of the same task. Moreover, the findings are in accord with the hypothesis that mental practice with MI, at least initially, improves performance by acting on the preparation and anticipation of movements rather than on execution per se.
The aim of the present positron emission tomography study was to measure the dynamic changes in cerebral activity before and after practice of an explicitly known sequence of foot movements when executed physically and to compare them to those elicited during motor imagery of the same movements. Nine healthy volunteers were scanned while performing both types of movement at an early phase of learning and after a 1-h training period of a sequence of dorsiflexions and plantarflexions with the left foot. These experimental conditions were compared directly, as well as to a perceptual control condition. Changes in regional cerebral blood flow associated with physical execution of the sequence early in the learning process were observed bilaterally in the dorsal premotor cortex and cerebellum, as well as in the left inferior parietal lobule. After training, however, most of these brain regions were no longer significantly activated, suggesting that they are critical for establishing the cognitive strategies and motor routines involved in executing sequential foot movements. By contrast, after practice, an increased level of activity was seen bilaterally in the medial orbitofrontal cortex and striatum, as well as in the left rostral portion of the anterior cingulate and a different region of the inferior parietal lobule, suggesting that these structures play an important role in the development of a long lasting representation of the sequence. Finally, as predicted, a similar pattern of dynamic changes was observed in both phases of learning during the motor imagery conditions. This last finding suggests that the cerebral plasticity occurring during the incremental acquisition of a motor sequence executed physically is reflected by the covert production of this skilled behavior using motor imagery.