Empathy or Ownership? Evidence from Corticospinal Excitability Modulation during Pain Observation.

Recent studies show that motor responses similar to those present in one's own pain (freezing effect) occur as a result of observation of pain in others. This finding has been interpreted as the physiological basis of empathy. Alternatively, it can represent the physiological counterpart of an embodiment phenomenon related to the sense of body ownership. We compared the empathy and the ownership hypotheses by manipulating the perspective of the observed hand model receiving pain so that it could be a first-person perspective, the one in which embodiment occurs, or a third-person perspective, the one in which we usually perceive the others. Motor-evoked potentials (MEPs) by TMS over M1 were recorded from first dorsal interosseous muscle, whereas participants observed video clips showing (a) a needle penetrating or (b) a Q-tip touching a hand model, presented either in first-person or in third-person perspective. We found that a pain-specific inhibition of MEP amplitude (a significantly greater MEP reduction in the "pain" compared with the "touch" conditions) only pertains to the first-person perspective, and it is related to the strength of the self-reported embodiment. We interpreted this corticospinal modulation according to an "affective" conception of body ownership, suggesting that the body I feel as my own is the body I care more about.

Goal or movement? Action representation within the primary motor cortex.

Although facilitation of the cortico-spinal system during action observation is widely accepted, it remains controversial whether this facilitation reflects a replica of the observed movements or the goal of the observed motor acts. In the present transcranial magnetic stimulation study, we recorded motor evoked potentials from two hand muscles (first dorsal interosseous and abductor digiti minimi) while 22 healthy participants observed a hand reaching towards and grasping a bottle. To test for alternative coding levels (goal vs. movement), three relevant aspects were systematically manipulated: the type of observed movement (precision grip or whole hand grasping), situational context (bottle positioned in front of or behind a wall-like barrier), and processing stage (transcranial magnetic stimulation pulse delivered at the onset of the movement or at the moment of contact between the fingers and the object). At movement onset, motor evoked potential responses reflected the program necessary to achieve the action goal within the situational context. During movement observation, however, the type of observed movement was taken into account and a transition towards a movement-related modulation was observed. These results suggest that, rather than being exclusive alternatives, goal coding and movement coding may relate to different processing stages.

Anticipating the course of an action: evidence from corticospinal excitability.

BACKGROUND: Anticipatory planning, the ability to anticipate future perceptual-motor demands of a goal-oriented action sequence, is essential for flexible, purposeful behavior. Once an action goal has been defined, movement details necessary to achieve that goal can be selected. Here, we investigate if anticipatory planning takes place even when multi-step actions are being carried out. How, we may ask, are the cerebral circuits involved in movement selection influenced by anticipated object-center task demands? Transcranial magnetic stimulation (TMS) was used to investigate how changes in corticospinal excitability (CSE) are dependent on anticipated task variables of intended future actions. Specifically, single- and paired-pulse TMS was used to evaluate corticospinal excitability during the action selection phase preparatory to grasp execution. RESULTS: We found that during the premovement phase, there is an object- and muscle-specific modulation in the intrinsic hand muscle that will be used during a forthcoming grasping action. Depending on whether the participants were instructed to perform a single- or double-step movement sequence, modulation of the corticospinal output to the appropriate hand muscles was dependent on what object was to be grasped and what type of movement was being prepared. No modulation in excitability was observed during one-step movements. CONCLUSIONS: Anticipation of intended task demands plays an important role in controlling multi- step actions during which ongoing behavior may need to be adjusted. This finding supports the notion that the cortico-cortical mechanism involving movement planning is specific for an object's properties as well as for the goal of the movement sequence.

Corticospinal excitability during the observation of social behavior.

Evidence suggests that the observation of an action induces in the observers an enhancement of motor evoked potentials (MEPs) recorded by the observer's muscles corresponding to those involved in the observed action. Although this is a well-studied phenomenon, it remains still unclear how the viewer's motor facilitation is influenced by the social content characterizing the observed scene. In the present study we investigated the facilitation of the corticospinal system during the observation of either an action that does not imply a social interaction (i.e., an actor throwing a ball against a wall), or an action which implies a social interaction (i.e., an actor passing a ball to a partner). Results indicate that MEPs amplitude is enhanced during the observation of a social rather than an individual action. We contend that the increase in MEPs activation might reflect an enhancement of the simulative activity stemming from the mirror system during the observation of social interactions. Altogether these findings show that the human corticospinal system is sensitive to social interactions and may support the role of the mirror neurons system in social cognition.

Grasping with tools: corticospinal excitability reflects observed hand movements.

Although facilitation of the corticospinal system during action observation is widely accepted, it remains controversial whether this facilitation reflects a replica of the observed movements or the goal of the observed motor acts. In the present study, we asked whether, when an object is grasped by using a tool, corticospinal facilitation represents 1) the movements of the hand, 2) the movements of the tool, or 3) the distal goal of the action. To address this question, we recorded motor-evoked potentials (MEPs) to transcranial magnetic stimulation while participants observed a hand reaching and grasping a mothball by using 3 types of pliers, requiring different hand-tool movements to achieve the same goal (grasping the object). We found that MEPs recorded from the opponens pollicis and from the first dorsal interosseous reflected the observed hand movements rather than the movements of the tool or the distal goal of the action. These results suggest that during observation of tool actions, detailed motor matching recruits online the same muscles as those used in the observed action.

The transfer of motor functional strategies via action observation.

When someone is choosing one piece from a bowl full of fruit, many pieces are within reach and visible. Although the desired piece seems to govern the particular pattern and direction of that person's reaching movement, the selection process is not impervious to the presence of task-irrelevant information (i.e. the other fruits). Evidence suggests that the kinematics of reach-to-grasp actions for a desired object integrates the motor features of all the objects which might become potential targets. Transcranial magnetic stimulation (TMS) and motor-evoked potentials (MEPs) were used by us to establish if that motor integration process can be transferred to an onlooker. Our results indicate that observation of hybrid reach-to-grasp movement kinematics is reflected in the observer's pattern of MEP amplitudes. This effect can be defined as a form of motor resonance which operates by 'reading' the kinematics of an observed action. The brain's ability to mirror motor integration processes while observing someone else's action helps an onlooker to understand what the other person is doing and to predict his/her motor alternatives.

Corticospinal excitability is specifically modulated by the social dimension of observed actions.

A large body of research reports that perceiving body movements of other people activates motor representations in the observer's brain. This automatic resonance mechanism appears to be imitative in nature. However, action observation does not inevitably lead to symmetrical motor facilitation: mirroring the observed movement might be disadvantageous for successfully performing joint actions. In two experiments, we used transcranial magnetic stimulation (TMS) to investigate whether the excitability of the corticospinal system was selectively modulated by the social dimension of an observed action. We recorded motor-evoked potentials (MEPs) from right-hand muscles during the observation of an action sequence which, depending on context, might or might not elicit a complementary response. The results demonstrate a differential motor facilitation depending on action context. Specifically, when the context called for a complementary action, the excitability pattern reflected the under-threshold activation of a complementary action, whereas when the context did not imply acting in a complementary manner, the observer's corticospinal activity reflected symmetrical motor resonance. We contend that the mechanisms underlying action observation are flexible and respond to contextual factors that guide the social interaction between individuals beyond emulation.

Visual attention and inhibitory control in children, teenagers and adults with autism without intellectual disability: results of oculomotor tasks from a 2-year longitudinal follow-up study (InFoR).

BACKGROUND: Inhibitory control and attention processing atypicalities are implicated in various diseases, including autism spectrum disorders (ASD). These cognitive functions can be tested by using visually guided saccade-based paradigms in children, adolescents and adults to determine the time course of such disorders. METHODS: In this study, using Gap, Step, Overlap and Antisaccade tasks, we analyzed the oculomotor behavior of 82 children, teenagers and adults with high functioning ASD and their peer typically developing (TD) controls in a two-year follow-up study under the auspices of the InFoR-Autism project. Analysis of correlations between oculomotors task measurements and diagnostic assessment of attentional (ADHD-RS and ADHD comorbidity indices) and executive functioning (BRIEF scales) were conducted in order to evaluate their relationship with the oculomotor performance of participants with ASD. RESULTS: As indicated by the presence of a Gap and Overlap effects in all age groups, the oculomotor performances of ASD participants showed a preserved capability in overt attention switching. In contrast, the difference in performances of ASD participants in the Antisaccade task, compared to their TD peers, indicated an atypical development of inhibition and executive functions. From correlation analysis between our oculomotor data and ADHD comorbidity index, and scores of attention and executive function difficulties, our findings support the hypothesis that a specific dysfunction of inhibition skills occurs in ASD participants that is independent of the presence of ADHD comorbidity. LIMITATIONS: These include the relatively small sample size of the ASD group over the study's two-year period, the absence of an ADHD-only control group and the evaluation of a TD control group solely at the study's inception. CONCLUSIONS: Children and teenagers with ASD have greater difficulty in attention switching and inhibiting prepotent stimuli. Adults with ASD can overcome these difficulties, but, similar to teenagers and children with ASD, they make more erroneous and anticipatory saccades and display a greater trial-to-trial variability in all oculomotor tasks compared to their peers. Our results are indicative of a developmental delay in the maturation of executive and attentional functioning in ASD and of a specific impairment in inhibitory control.

Anxiety-dependent modulation of motor responses to pain expectancy.

The relationship between pain expectancy and motor system plays a crucial role in the human defensive system. Here, we took advantage of the inhibitory modulation of the motor pathway to the muscle of the hand receiving painful stimuli, by recording motor-evoked potentials (MEPs) to Transcranial Magnetic Stimulation (TMS). We employed a classical conditioning paradigm in which neutral (visual and auditory) stimuli were conditioned by pairing either painful or not-painful stimuli (electric shocks) in separated groups. Only the Pain Group showed clear motor responses: i.e. a significant decrease in MEPs amplitude, with respect to the neutral condition, not only in conditioning stimuli, when actual shocks were paired with neutral stimuli, but also in conditioned stimuli, when shocks were only expected. Significant differences between the two groups suggest that the MEPs decrease is specific for pain expectancy and does not pertain to anticipation in general. Furthermore, in the Pain Group, a significant negative correlation between physiological responses to conditioned stimuli and the participants' anxiety traits was found: the lower the MEPs amplitude, the higher the participants' anxiety scores. The present findings suggest that, in order for defensive motor responses to occur, actual pain is not necessary; rather, anxiety-dependent pain expectancy can be sufficient.

Do we feel the same empathy for loved and hated peers?

Empathy allows us to understand and react to other people's feelings and sensations; we can more accurately judge another person's situation when we are aware of his/her emotions. Empathy for pain is a good working model of the behavioral and neural processes involved in empathy in general. Although the influence of perspective-taking processes (notably "Self" vs. "Other") on pain rating has been studied, the impact of the degree of familiarity with the person representing the "Other" perspective has not been previously addressed. In the present study, we asked participants to adopt four different perspectives: "Self", "Other-Most-Loved-Familiar", "Other-Most-Hated-Familiar" and "Other-Stranger". The results showed that higher pain ratings were attributed to the Other-Most-Loved-Familiar perspective than to the Self, Other-Stranger and Other-Most-Hated-Familiar perspectives. Moreover, participants were quicker to rate pain for the Other-Most-Loved-Familiar perspective and the Self-perspective than for the other two perspectives. These results for a perspective-taking task therefore more clearly define the role of familiarity in empathy for pain.

Influence of postural threat on postural responses to aversive visual stimuli.

Recent research has shown that emotion influences postural control. The objective of the present study was to establish whether or not postural threat influences postural and physiological responses to aversive visual stimuli. In order to investigate the coupling between emotional reactions, motivated behavior and postural responses, we studied the displacement of the subject's center of pressure (COP) and the changes in electrodermal activity (EDA), heart rate (HR) and postural muscle activation. Thirty-two participants (15 males, 17 females; mean ± SD age: 21.4 ± 2.3) viewed affective and neutral pictures while standing still on a force platform in the presence or absence of postural threat. The HR and EDA data revealed that the emotional state varied as a function of the postural condition. The mean displacement in the anteroposterior (AP) axis was more rearwards in response to aversive stimuli that in response to neutral stimuli, in both the absence of postural threat (-0.65 mm and +0.90 mm for aversive and neutral stimuli, respectively) and the presence of postural threat (-0.00 mm vs. +0.89 mm, respectively). An aversive stimulus was associated with a shorter AP COP sway path than a neutral stimulus in the presence of a postural threat (167.26 mm vs. 174.66 mm for aversive and neutral stimuli, respectively) but not in the latter's absence (155.85 mm vs. 154.48 mm, respectively). Our results evidenced withdrawal behavior in response to an aversive stimulus (relative to a neutral stimulus) in the absence of postural threat. Withdrawal behavior was attenuated (but nevertheless active) in the presence of a postural threat.

When emulation becomes reciprocity.

It is well known that perceiving another's body movements activates corresponding motor representations in an observer's brain. It is nevertheless true that in many situations simply imitating another's actions would not be an effective or appropriate response, as successful interaction often requires complementary rather than emulative movements. At what point does the automatic tendency to mirror another's actions become the inclination to carry out appropriate, complementary movements? In the present study, single-pulse transcranial magnetic stimulation (TMS) was used to explore corticospinal excitability in participants observing action sequences evoking imitative or complementary movements. TMS was delivered at five time points corresponding to different moments in time when key kinematic landmarks characterizing an observed action occurred. A variation in motor evoked potentials (MEPs) confirmed that the motor system flexibly shifts from imitative to complementary action tendencies. That shift appears to take place very precociously in time. Observers are attuned to advance movement information and can use it to anticipate a future course of action and to prepare for an appropriate, complementary action. Altogether, these findings represent a step forward in research concerning social action-perception coupling mechanisms providing important data to better understand the role of predictive simulation in social contexts.

Motor cortex excitability is tightly coupled to observed movements.

Although facilitation of the corticospinal (CS) system during action observation is a widely accepted phenomenon, it is still controversial if facilitation reflects the replica of observed movement kinematics or the tension to achieve a particular goal. In this study, transcranial magnetic stimulation (TMS)-induced motor evoked potentials (MEPs) were recorded from the abductor digiti minimi (ADM) and the first dorsal interosseus (FDI) muscles while participant-volunteers observed a model grasping a small target eliciting a precision grip or a large target eliciting a whole hand grasp directed toward an isolated object or flanked by different sized objects (i.e., distractor). A detailed movement analysis revealed that the model's kinematics were influenced by the distractor's size. Video clips filming the scene were edited in such a way that the distractor was removed from the scene. Participant-volunteers were asked to observe actions characterized by the same goal but performed using different kinematical patterns. Although the differences in movement kinematics were not noticed by the participant-volunteers, they nonetheless elicited distinct configurations of corticospinal activation. Detailed motor matching seems to recruit the same muscles in the onlooker as in the person actually carrying out the action during observation of grasping actions. These effects appear to be elicited by very subtle, imperceptible aspects of observed actions pointing to a finely tuned mechanism that specifically encodes body parts.

From simulation to reciprocity: the case of complementary actions.

A large body of research reports that perceiving body movements of other people activates motor representations in the observer's brain. This automatic resonance mechanism appears to be imitative in nature. However, action observation does not inevitably lead to symmetrical motor facilitation: Mirroring the observed movement might be disadvantageous for successfully performing joint actions. What remains unknown is how we are to resolve the possible conflict between the automatic tendency to "mirror" and the need to perform different context-related complementary actions. By using single-pulse transcranial magnetic stimulation, we found that observation of a double-step action characterized by an implicit complementary request engendered a shift from symmetrical simulation to reciprocity in the participants' corticospinal activity. Accordingly, differential motor facilitation was revealed for the snapshots evoking imitative and complementary gestures despite the fact that the observed type of grasp was identical. Control conditions in which participants observed the same action sequence but in a context not implying a complementary request were included as well. The results provide compelling evidence that when an observed action calls for a nonidentical complementary action, an interplay between the automatic tendency to resonate with what is observed and to implicitly prepare for the complementary action does emerge. In other words, implicit complementary requests might have the ability to draw attention to specific features of the context affording nonidentical responses.