Was it me or was it you? How the sense of agency originates from ideomotor learning revealed by fMRI

(C) 2009 Elsevier Inc. All rights reserved

Whodunnit? Electrophysiological correlates of agency judgements.

Sense of agency refers to the feeling that "I" am responsible for those external events that are directly produced by one's own voluntary actions. Recent theories distinguish between a non-conceptual "feeling" of agency linked to changes in the processing of self-generated sensory events, and a higher-order judgement of agency, which attributes sensory events to the self. In the current study we explore the neural correlates of the judgement of agency by means of electrophysiology. We measured event-related potentials to tones that were either perceived or not perceived as triggered by participants' voluntary actions and related these potentials to later judgements of agency over the tones. Replicating earlier findings on predictive sensory attenuation, we found that the N1 component was attenuated for congruent tones that corresponded to the learned action-effect mapping as opposed to incongruent tones that did not correspond to the previously acquired associations between actions and tones. The P3a component, but not the N1, directly reflected the judgement of agency: deflections in this component were greater for tones judged as self-generated than for tones judged as externally produced. The fact that the outcome of the later agency judgement was predictable based on the P3a component demonstrates that agency judgements incorporate early information processing components and are not purely reconstructive, post-hoc evaluations generated at time of judgement

New frontiers in the neuroscience of the sense of agency

The sense that I am the author of my own actions, including the ability to distinguish my own from other people's actions, is a fundamental building block of our sense of self, on the one hand, and successful social interactions, on the other. Using cognitive neuroscience techniques, researchers have attempted to elucidate the functional basis of this intriguing phenomenon, also trying to explain pathological abnormalities of action awareness in certain psychiatric and neurological disturbances. Recent conceptual, technological, and methodological advances suggest several interesting and necessary new leads for future research on the neuroscience of agency. Here I will describe new frontiers for the field such as the need for novel and multifactorial paradigms, anatomically plausible network models for the sense of agency, investigations of the temporal dynamics during agentic processing and ecologically valid virtual reality (VR) applications

The influence of group membership on cross-contextual imitation

Research on mimicry has demonstrated that individuals imitate in-group members more strongly than out-group members. In the present study, we tested whether such top-down modulation also applies for more extreme forms of direct mapping, such as for cross-contextual imitation settings, in which individuals imitate others' movements without sharing a common goal or context. Models on self-other control suggest that top-down modulations are based merely on a direct link between social sensory processing and imitation. That is, perceived similarities between oneself and another person is sufficient to amplify a shared representation between own and others' actions, which then trigger imitation. However, motivational accounts explain such findings with the assumption that individuals are motivated to affiliate with others. Because imitation is linked to positive social consequences, individuals should imitate in-group members more strongly than out-group members. We tested these two theoretical accounts against each other by applying a cross-contextual imitation paradigm. The results demonstrate that in-group members are more strongly cross-contextually imitated than out-group members the higher individuals' motivation to affiliate with the in-group is. This supports motivational models but not self-other control accounts. Further theoretical implications are discussed

Investigating social gaze as an action-perception online performance

Gaze represents a major non-verbal communication channel in social interactions. In this respect, when facing another person, one's gaze should not be examined as a purely perceptive process but also as an action-perception online performance. However, little is known about processes involved in the real-time self-regulation of social gaze. The present study investigates the impact of a gaze-contingent viewing window on fixation patterns and the awareness of being the agent moving the window. In face-to-face scenarios played by a virtual human character, the task for the 18 adult participants was to interpret an equivocal sentence which could be disambiguated by examining the emotional expressions of the character speaking. The virtual character was embedded in naturalistic backgrounds to enhance realism. Eye-tracking data showed that the viewing window induced changes in gaze behavior, notably longer visual fixations. Notwithstanding, only half of the participants ascribed the window displacements to their eye movements. These participants also spent more time looking at the eyes and mouth regions of the virtual human character. The outcomes of the study highlight the dissociation between non-volitional gaze adaptation and the self-ascription of agency. Such dissociation provides support for a two-step account of the sense of agency composed of pre-noetic monitoring mechanisms and reflexive processes, linked by bottom-up and top-down processes. We comment upon these results, which illustrate the relevance of our method for studying online social cognition, in particular concerning autism spectrum disorders (ASD) where the poor pragmatic understanding of oral speech is considered linked to visual peculiarities that impede facial exploration

Neural mechanisms of goal-directed behavior: outcome-based response selection is associated with increased functional coupling of the angular gyrus

Goal-directed behavior is based on representations of contingencies between a certain situation (S), a certain (re)action (R) and a certain outcome (O). These S-R-O representations enable flexible response selection in different situations according to the currently pursued goal. Importantly however, the successful formation of such representations is a necessary but not sufficient precondition for goal-directed behavior which additionally requires the actual usage of the contingency information for action control. The present fMRI study aimed at identifying the neural basis of each of these two aspects: representing vs. explicitly using experienced S-R-O contingencies. To this end, we created three experimental conditions: S-R-O contingency present and used for outcome-based response selection, S-R-O contingency present but not used, and S-R-O contingency absent. The comparison between conditions with and without S-R-O contingency revealed that the angular gyrus is relevant for representing S-R-O contingencies. The explicit usage of learnt S-R-O representations in turn was associated with increased functional coupling between angular gyrus and several subcortical (hippocampus, caudate head), prefrontal (lateral orbitofrontal cortex (OFC), rostrolateral prefrontal cortex (RLPFC)) and cerebellar areas, which we suggest represent different explicit and implicit processes of goal-directed action control. Hence, we ascribe a central role to the angular gyrus in associating actions to their sensory outcomes which is used to guide behavior through coupling of the angular gyrus with multiple areas related to different aspects of action control

The influence of action observation on action execution : dissociating the contribution of action on perception, perception on action, and resolving conflict

For more than 15 years, motor interference paradigms have been used to investigate the influence of action observation on action execution. Most research on so-called automatic imitation has focused on variables that play a modulating role or investigated potential confounding factors. Interestingly, furthermore, a number of functional magnetic resonance imaging (fMRI) studies have tried to shed light on the functional mechanisms and neural correlates involved in imitation inhibition. However, these fMRI studies, presumably due to poor temporal resolution, have primarily focused on high-level processes and have neglected the potential role of low-level motor and perceptual processes. In the current EEG study, we therefore aimed to disentangle the influence of low-level perceptual and motoric mechanisms from high-level cognitive mechanisms. We focused on potential congruency differences in the visual N190 - a component related to the processing of biological motion, the Readiness Potential - a component related to motor preparation, and the high-level P3 component. Interestingly, we detected congruency effects in each of these components, suggesting that the interference effect in an automatic imitation paradigm is not only related to high-level processes such as self-other distinction but also to more low-level influences of perception on action and action on perception. Moreover, we documented relationships of the neural effects with (autistic) behavior

Does the brain know who is at the origin of what in an imitative interaction?

Brain correlates of the sense of agency have recently received increased attention. However, the explorations remain largely restricted to the study of brains in isolation. The prototypical paradigm used so far consists of manipulating visual perception of own action while asking the subject to draw a distinction between self- versus externally caused action. However, the recent definition of agency as a multifactorial phenomenon combining bottom-up and top-down processes suggests the exploration of more complex situations. Notably there is a need of accounting for the dynamics of agency in a two-body context where we often experience the double faceted question of who is at the origin of what in an ongoing interaction. In a dyadic context of role switching indeed, each partner can feel body ownership, share a sense of agency and altogether alternate an ascription of the primacy of action to self and to other. To explore the brain correlates of these different aspects of agency, we recorded with dual EEG and video set-ups 22 subjects interacting via spontaneous versus induced imitation (II) of hand movements. The differences between the two conditions lie in the fact that the roles are either externally attributed (induced condition) or result from a negotiation between subjects (spontaneous condition). Results demonstrate dissociations between self- and other-ascription of action primacy in delta, alpha and beta frequency bands during the condition of II. By contrast a similar increase in the low gamma frequency band (38–47 Hz) was observed over the centro-parietal regions for the two roles in spontaneous imitation (SI). Taken together, the results highlight the different brain correlates of agency at play during live interactions

The role of the temporoparietal junction in self-other distinction

Being able to discriminate between what originates from ourselves and what originates from others is critical for efficient interactions with our social environment. However, it remains an open question whether self-other distinction is a domain-general mechanism that is involved in various social-cognitive functions or whether specific 'self-other distinction mechanisms' exist for each of these functions. On the neural level, there is evidence that self-other distinction is related to a specific brain region at the border of the superior temporal and inferior parietal cortex, the temporoparietal junction (TPJ). Demonstrating that the TPJ plays a role in social processes that require self-other distinction would support the idea of a domain-general mechanism of self-other distinction. In the present paper, we review evidence coming from clinical observations, neuroimaging experiments and a meta-analysis indicating the involvement of the TPJ in various cognitive operations requiring self-other distinction. At the perceptual level, we discuss the human ability to identify one's own body and to distinguish it from others. At the action level, we review research on the human ability to experience agency and the control of imitative response tendencies. Finally, at the mental-state level, we discuss the ability to attribute mental states to others. Based on this integrative review, we suggest that the TPJ, and in particular its dorsal part, supports a domain general ability to enhance task-relevant representations when self-related and other-related representations are in conflict. Finally, this conception allows us to propose a unifying architecture for the emergence of numerous socio-cognitive abilities

Feeling in control: Neural correlates of experience of agency.

The ability to control external events through our own actions is a fundamental aspect of human experience. Both the subjective experience of agency, and its neural correlates, remain poorly understood. Previous studies show that the angular gyrus is activated when participants explicitly judge that they lack agency. In contrast, the positive sense of agency over external events is associated with distortions of time perception. Here, we show that the perceived interval between actions and a subsequent tone is shorter than the perceived interval between a physically comparable passive movement and a tone, replicating the 'intentional binding' effect reported previously. We considered this as a potential implicit marker of agency, and investigated its neural basis, by using parametric analyses to identify brain areas whose activation correlated more strongly with the perceived action-tone interval in the action condition, than in the passive condition. Small volume corrections were used to test specific hypotheses about the contribution of the angular gyrus, and of the supplementary motor area (SMA), based on previous literature. We found no correlation between angular gyrus and our temporal measure of sense of agency. In contrast, we found that a lateral, caudal region within the SMA proper was more strongly associated with the perceived action-tone interval than with perception of a control interval following a passive movement. We suggest that the supplementary motor complex contributes to the subjective experience of temporal flow that accompanies goal-directed voluntary actions