fMRI exploration of the cerebral mechanisms of the perception of pain in others via facial expression

La douleur ressentie entraine des réactions de différents ordres : physique, neurologique, comportemental. L’expression de la douleur sur un visage constitue une de ces réactions, d’ordre comportemental. Cette expression faciale intègre les éléments caractérisant la douleur ressentie et il est possible de l’analyser en tant qu’observateur extérieur. Les travaux d’imagerie cérébrale étudiant la réaction du cerveau à la perception d’une douleur chez autrui ont mis en lumière un chevauchement entre les régions du cerveau réagissant à une douleur personnellement ressentie et celles réagissant à l’observation d’une expression de douleur chez les autres. Dans la première étude présentée ici, la réaction du cerveau à l’expression de la douleur chez autrui a été analysée en établissant dans quelle mesure l’intensité plus ou moins forte de la douleur exprimée pouvait moduler cette réaction. Les résultats de cette étude indiquent que la perception de la douleur chez autrui ne concerne pas seulement certaines régions du cerveau réagissant à la douleur personnellement ressentie mais aussi des régions habituellement impliquées dans le système des neurones miroirs (MNS; « human mirror neuron system ») ainsi que dans des régions associées à la Théorie de l’esprit (‘Theory of Mind’, ToM; ou « mentalizing »). En outre, ce travail montre que l’implication relative de ces différentes régions varie selon que la personne évalue la signification affective de l’expression – la magnitude de la douleur – ou qu’elle discrimine les composantes motrices de l’expression – les mouvements faciaux. Une deuxième étude a donc été réalisée, s’appuyant sur un paradigme combinant l’observation et l’exécution pour vérifier et confirmer la « réponse miroir » observée dans la première étude et pour examiner plus en détail les différences apparentes entre la résonance émotionnelle et la résonance motrice. En confirmation de la première étude, il a été établi que ce sont différentes régions du cerveau qui sont impliquées dans les réactions à l’expression de la douleur selon qu’elles relèvent de la résonance émotionnelle ou de la résonance motrice. En somme, ces résultats montrent que la perception de la douleur chez autrui est un processus complexe qui met en jeu un chevauchement entre les régions réagissant à une douleur personnellement ressentie et à une douleur constatée chez autrui, ainsi que les phénomènes de résonance motrice (« mirroring ») et de « mentalizing », processus plus généraux de la cognition sociale.The pain experience provokes several responses – physical, neural, behavioral. The facial expression of pain is one such behavioral response: it encodes the subjective experience of pain and, as observers, we can decode it. Neuroimaging studies looking at the brain response to the perception of pain in others have identified overlap between brain areas active for the experience of self-pain, and those active during the observation of pain in others. In the first study described below, the brain response to pain in others was investigated using a paradigm that investigated how the intensity of the perceived pain modulated the brain response. The results of this work indicate that the perception of pain in others involves not only certain brain regions involved in self-pain, but also regions previously implicated in the human mirror neuron system (MNS), as well as areas underlying Theory of Mind (i.e. mentalizing). Further, the relative contribution of these areas depended on whether the subject is evaluating the affective meaning of the expression – the pain magnitude – or if they are discriminating the motor components of the expression – the facial movements. A second study was thus designed, using a combined observation and execution paradigm, to confirm the mirroring response observed in the first study, as well as to further explore the hypothesized difference between emotional and motor mirroring. Similarly to the first study, it was found that different brain regions are responsible for mirroring for emotional, versus motor, content of the observed pain expressions. Taken together, these results reveal the perception of pain in others to be a complex process that involves overlap between self and other affective pain areas, as well as mirroring and mentalizing – more general processes of social cognition

Perceiving Pain in Others: Automatic and Controlled Mechanisms

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Pain mirrors: Neural correlates of observing self or others' facial expressions of pain

Facial expressions of pain are able to elicit empathy and adaptive behavioral responses in the observer. An influential theory posits that empathy relies on an affective mirror mechanism, according to which emotion recognition relies upon the internal simulation of motor and interoceptive states triggered by emotional stimuli. We tested this hypothesis comparing representations of self or others' expressions of pain in nineteen young healthy female volunteers by means of functional magnetic resonance imaging (fMRI). We hypothesized that one's own facial expressions are more likely to elicit the internal simulation of emotions, being more strictly related to self. Video-clips of the facial expressions of each volunteer receiving either painful or non-painful mechanical stimulations to their right hand dorsum were recorded and used as stimuli in a 2 × 2 (Self/Other; Pain/No-Pain) within-subject design. During each trial, a 2 s video clip was presented, displaying either the subject's own neutral or painful facial expressions (Self No-Pain, SNP; Self Pain, SP), or the expressions of other unfamiliar volunteers (Others' No-Pain, ONP; Others' Pain, OP), displaying a comparable emotional intensity. Participants were asked to indicate whether each video displayed a pain expression. fMRI signals were higher while viewing Pain than No-Pain stimuli in a large bilateral array of cortical areas including middle and superior temporal, supramarginal, superior mesial and inferior frontal (IFG) gyri, anterior insula (AI), anterior cingulate (ACC), and anterior mid-cingulate (aMCC) cortex, as well as right fusiform gyrus. Bilateral activations were also detected in thalamus and basal ganglia. The Self vs. Other contrast showed signal changes in ACC and aMCC, IFG, AI, and parietal cortex. A significant interaction between Self and Pain [(SP vs. SNP) > (OP vs. ONP)] was found in a pre-defined region of aMCC known to be also active during noxious stimulation. These findings demonstrate that the observation of one's own and others' facial expressions share a largely common neural network, but self-related stimuli induce generally higher activations. In line with our hypothesis, selectively greater activity for self pain-related stimuli was found in aMCC, a medial-wall region critical for pain perception and recognition

The role of anterior insular cortex in social emotions

Functional neuroimaging investigations in the fields of social neuroscience and neuroeconomics indicate that the anterior insular cortex (AI) is consistently involved in empathy, compassion, and interpersonal phenomena such as fairness and cooperation. These findings suggest that AI plays an important role in social emotions, hereby defined as affective states that arise when we interact with other people and that depend on the social context. After we link the role of AI in social emotions to interoceptive awareness and the representation of current global emotional states, we will present a model suggesting that AI is not only involved in representing current states, but also in predicting emotional states relevant to the self and others. This model also proposes that AI enables us to learn about emotional states as well as about the uncertainty attached to events, and implies that AI plays a dominant role in decision making in complex and uncertain environments. Our review further highlights that dorsal and ventro-central, as well as anterior and posterior subdivisions of AI potentially subserve different functions and guide different aspects of behavioral regulation. We conclude with a section summarizing different routes to understanding other people's actions, feelings and thoughts, emphasizing the notion that the predominant role of AI involves understanding others' feeling and bodily states rather than their action intentions or abstract belief

The role of the right tempoparietal junction in the elicitation of vicarious experiences and detection accuracy while observing pain and touch

This study investigated the effects of observing pain and touch in others upon vicarious somatosensory experiences and the detection of subtle somatosensory stimuli. Furthermore, transcranial direct current stimulation (tDCS) was used to assess the role of the right temporoparietal junction (rTPJ), as this brain region has been suggested to be involved in perspective taking and self-other distinction. Undergraduates (N = 22) viewed videos depicting hands being touched, hands being pricked, and control scenes (same approaching movement as in the other video categories but without the painful/touching object), while experiencing vibrotactile stimuli themselves on the left, right, or both hands. Participants reported the location at which they felt a somatosensory stimulus. Vibrotactile stimuli and visual scenes were applied in a congruent or incongruent way. During three separate testing sessions, excitability of the rTPJ was modulated with tDCS (cathodal, anodal, or sham). We calculated the proportion of correct responses and false alarms (i.e., number of trials in which a vicarious somatosensory experience was reported congruent to the site of the visual information). Pain-related scenes facilitated the correct detection of tactile stimuli and augmented the number of vicarious somatosensory experiences compared with observing touch or control videos. Stimulation of the rTPJ had no reliable influence upon detection accuracy or the number of vicarious errors. This study indicates that the observation of pain-related scenes compared to the observation of touch or control videos increases the likelihood that a somatosensory stimulus is detected. Contrary to our expectations, the rTPJ did not modulate detection accuracy

Visualization of Painful Experiences Believed to Trigger the Activation of Affective and Emotional Brain Regions in Subjects with Low Back Pain

In the management of clinical low back pain (LBP), actual damage to lower back areas such as muscles, intervertebral discs etc. are normally targeted for therapy. However, LBP may involve not only sensory pain, but also underlying affective pain which may also play an important role overall in painful events. Therefore we hypothesized that visualization of a painful event may trigger painful memories, thus provoking the affective dimension of pain. The present study investigated neural correlates of affect processing in subjects with LBP (n = 11) and subjects without LBP (n = 11) through the use of virtual LBP stimuli. Whole brain functional magnetic resonance imaging (MRI) was performed for all subjects while they were shown a picture of a man carrying luggage in a half-crouching position. All subjects with LBP reported experiencing discomfort and 7 LBP subjects reported experiencing pain. In contrast to subjects without LBP, subjects with LBP displayed activation of the cortical area related to pain and emotions: the insula, supplementary motor area, premotor area, thalamus, pulvinar, posterior cingulate cortex, hippocampus, fusiform, gyrus, and cerebellum. These results suggest that the virtual LBP stimuli caused memory retrieval of unpleasant experiences and therefore may be associated with prolonged chronic LBP conditions

Mirroring Pain in the Brain: Emotional Expression versus Motor Imitation

Perception of pain in others via facial expressions has been shown to involve brain areas responsive to self-pain, biological motion, as well as both performed and observed motor actions. Here, we investigated the involvement of these different regions during emotional and motor mirroring of pain expressions using a two-task paradigm, and including both observation and execution of the expressions. BOLD responses were measured as subjects watched video clips showing different intensities of pain expression and, after a variable delay, either expressed the amount of pain they perceived in the clips (pain task), or imitated the facial movements (movement task). In the pain task condition, pain coding involved overlapping activation across observation and execution in the anterior cingulate cortex, supplementary motor area, inferior frontal gyrus/anterior insula, and the inferior parietal lobule, and a pain-related increase (pain vs. neutral) in the anterior cingulate cortex/supplementary motor area, the right inferior frontal gyrus, and the postcentral gyrus. The 'mirroring' response was stronger in the inferior frontal gyrus and middle temporal gyrus/superior temporal sulcus during the pain task, and stronger in the inferior parietal lobule in the movement task. These results strongly suggest that while motor mirroring may contribute to the perception of pain expressions in others, interpreting these expressions in terms of pain content draws more heavily on networks involved in the perception of affective meaning

Vicarious facilitation of facial responses to pain

Introduction: Observing facial expressions of pain has been shown to lead to increased subjective, neural and autonomic pain responses. Surprisingly, these vicarious facilitation effects on its corresponding response channel, namely facial responses to pain have mostly been neglected. We aim to examine whether the prior exposure to facial expressions of pain leads to a facilitation of facial responses to experimental pain; and whether this facilitation is linked to the valence (pain vs. neutral expression) or also linked to specific motor-features of the facial pain expressions (different facial muscle movements). Method: Subjective (intensity and unpleasantness ratings) and facial responses (Facial Action Coding System) of 64 participants (34 female) to painful and non-painful heat stimuli were assessed. Before each heat stimulus, video clips of computer-generated facial expressions (three different pain expressions and a neutral expression) were presented. Results: The prior exposure to facial expressions of pain led to increased subjective and facial responses to pain. Further, vicarious pain facilitation of facial responses was significantly correlated with facilitation of unpleasantness ratings. We also found evidence that this vicarious facilitation of facial responses was not only linked to the presentation of pain versus neutral expressions but also to specific motor-features of the pain cue (increase in congruent facial muscle movements). Discussion: Vicarious pain facilitation was found for subjective and facial responses to pain. The results are discussed with reference to the motivational priming hypothesis as well as with reference to motor priming. Significance: Our study uncovers evidence that facial pain responses are not only influenced by motivational priming (similar to other types of pain responses), but also by motor-priming. These findings shed light on the complexity -ranging from social, affective and motor mechanisms -underling vicarious facilitation of pain