Endogenous Action Selection Processes in Dorsolateral Prefrontal Cortex Contribute to Sense of Agency: A Meta-Analysis of tDCS Studies of 'Intentional Binding'

BACKGROUND: Sense of agency is the experience of being in control of one's own actions and their consequences. The role of frontal cortex in this aspect of action control and awareness remains unclear. OBJECTIVE/HYPOTHESIS: Given the role of dorsolateral prefrontal cortex (DLPFC) in action selection, we predicted that DLPFC may contribute to sense of agency when participants select between multiple actions. METHODS: We performed a series of experiments by manipulating a range of task parameters related to action selection and action outcomes while participants were exposed to tDCS stimulation of the left DLPFC. We measured the temporal association between a voluntary action and its outcome using the intentional binding effect, as an implicit measure of sense of agency. RESULTS: Fixed-effect meta-analysis of our primary data showed a trend towards a frontal tDCS, together with considerable heterogeneity between our experiments. Classifying the experiments into subsets of studies, according to whether participants endogenously selected between alternative actions or not, explained 71% of this heterogeneity. Anodal stimulation of DLPFC increased the temporal binding of actions towards tones in the subset of studies involving endogenous action selection, but not in the other studies. CONCLUSIONS: DLPFC may contribute to sense of agency when participants selected between multiple actions. This enhanced feeling of control over voluntary actions could be related to the observed therapeutic effects of frontal tDCS in depression

Neural mechanisms underlying voluntary action control in the human brain

The capacity for voluntary action lies at the heart of human nature. Healthy adults typically feel that they can exercise voluntary control over their actions, and thus change their physical and social environment. This feeling of autonomous control over one’s own action is a foundational concept for most human societies. However, neuromechanistic models of this ubiquitous experience remain unclear. This thesis explores the neural mechanisms underlying voluntary action control in the human brain and the experiences associated with it such as the experience of agency. After operationalizing voluntary action in a novel behavioural paradigm, we show that self-initiated actions are preceded by a specific preparatory process in the brain. Later experiments suggest that the experience of agency might be a metacognitive readout of this precursor process: a study of a patient with anarchic hand syndrome shows that precursor processes for voluntary action contribute to the sense of agency over outcomes of action. We then provide new causal evidence that the experiences of voluntary action could be influenced by modulating specific parts of the brain that may host these precursor processes such as parietal and frontal areas. Finally, we show that by pairing voluntary actions of one hand with involuntary movements of the other hand, key aspects of agency experience can transfer from voluntary to involuntary movements after repeated association. This later finding suggests that the experiences of voluntary action are not hardwired, but could be acquired through associative learning. This thesis concludes by proposing that a dedicated system in the human brain contributes to the preparation and execution of self-initiated voluntary actions and the characteristic subjective experiences associated with it

Social Transmission of Experience of Agency: An Experimental Study

The sense of controlling one’s own actions is fundamental to normal human mental function, and also underlies concepts of social responsibility for action. However, it remains unclear how the wider social context of human action influences sense of agency. Using a simple experimental design, we investigated, for the first time, how observing the action of another person or a robot could potentially influence one’s own sense of agency. We assessed how observing another’s action might change the perceived temporal relationship between one’s own voluntary actions and their outcomes, which has been proposed as an implicit measure of sense of agency. Working in pairs, participants chose between two action alternatives, one rewarded more frequently than the other, while watching a rotating clock hand. They judged, in separate blocks, either the time of their own action, or the time of a tone that followed the action. These were compared to baseline judgements of actions alone, or tones alone, to calculate the perceptual shift of action toward outcome and vice versa. Our design focused on how these two dependent variables, which jointly provide an implicit measure of sense of agency, might be influenced by observing another’s action. In the observational group, each participant could see the other’s actions. Multivariate analysis showed that the perceived time of action and tone shifted progressively toward the actual time of outcome with repeated experience of this social situation. No such progressive change occurred in other groups for whom a barrier hid participants’ actions from each other. However, a similar effect was observed in the group that viewed movements of a human-like robotic hand, rather than actions of another person. This finding suggests that observing the actions of others increases the salience of the external outcomes of action and this effect is not unique to observing human agents. Social contexts in which we see others controlling external events may play an important role in mentally representing the impact of our own actions on the external world

Modulating human sense of agency with non-invasive brain stimulation

Human voluntary actions are accompanied by a distinctive subjective experience termed “sense of agency”. We performed three experiments using transcranial direct current stimulation (tDCS) to modulate brain circuits involved in control of action, while measuring stimulation-induced changes in one implicit measure of sense of agency, namely the perceived temporal relationship between a voluntary action and tone triggered by the action. Participants perceived such tones as shifted towards the action that caused them, relative to baseline conditions with tones but no actions. Actions that caused tones were perceived as shifted towards the tone, relative to baseline actions without tones. This ‘intentional binding’ was diminished by anodal stimulation of the left parietal cortex [targeting the angular gyrus (AG)], and, to a lesser extent, by stimulation targeting the left dorsolateral prefrontal cortex (DLPFC), (Experiment 1). Cathodal AG stimulation had no effect (Experiment 2). Experiment 3 replicated the effect of left anodal AG stimulation for actions made with either the left or the right hand, and showed no effect of right anodal AG stimulation. The angular gyrus has been identified as a key area for explicit agency judgements in previous neuroimaging and lesion studies. Our study provides new causal evidence that the left angular gyrus plays a key role in the perceptual experience of agency

Precursor processes of human self-initiated action

A gradual buildup of electrical potential over motor areas precedes self-initiated movements. Recently, such "readiness potentials" (RPs) were attributed to stochastic fluctuations in neural activity. We developed a new experimental paradigm that operationalised self-initiated actions as endogenous 'skip' responses while waiting for target stimuli in a perceptual decision task. We compared these to a block of trials where participants could not choose when to skip, but were instead instructed to skip. Frequency and timing of motor action were therefore balanced across blocks, so that conditions differed only in how the timing of skip decisions was generated. We reasoned that across-trial variability of EEG could carry as much information about the source of skip decisions as the mean RP. EEG variability decreased more markedly prior to self-initiated compared to externally-triggered skip actions. This convergence suggests a consistent preparatory process prior to self-initiated action. A leaky stochastic accumulator model could reproduce this convergence given the additional assumption of a systematic decrease in input noise prior to self-initiated actions. Our results may provide a novel neurophysiological perspective on the topical debate regarding whether self-initiated actions arise from a deterministic neurocognitive process, or from neural stochasticity. We suggest that the key precursor of self-initiated action may manifest as a reduction in neural noise

Extending experiences of voluntary action by association

“Sense of agency” refers to the experience that links one’s voluntary actions to their external outcomes. It remains unclear whether this ubiquitous experience is hardwired, arising from specific signals within the brain’s motor systems, or rather depends on associative learning, through repeated cooccurrence of voluntary movements and their outcomes. To distinguish these two models, we asked participants to trigger a tone by a voluntary keypress action. The voluntary action was always associated with an involuntary movement of the other hand. We then tested whether the combination of the involuntary movement and tone alone might now suffice to produce a sense of agency, even when the voluntary action was omitted. Sense of agency was measured using an implicit marker based on time perception, namely a shift in the perceived time of the outcome toward the action that caused it. Across two experiments, repeatedly pairing an involuntary movement with a voluntary action induced key temporal features of agency, with the outcome now perceived as shifted toward the involuntary movement. This shift required involuntary movements to have been previously associated with voluntary actions. We show that some key aspects of agency may be transferred from voluntary actions to involuntary movements. An internal volitional signal is required for the primary acquisition of agency but, with repeated association, the involuntary movement in itself comes to produce some key temporal features of agency over the subsequent outcome. This finding may explain how humans can develop an enduring sense of agency in nonnatural cases, like brain–machine interfaces

I could have done otherwise: Availability of counterfactual comparisons informs the sense of agency

Personal control and agency are closely associated with the counterfactual notion that a person could have done otherwise (CDO). In both philosophy and law, this counterfactual evaluation determines responsibility and punishment, yet little is known about its influence on agents' experience during action. We used a risky decision-making task to study how counterfactual evaluations influenced participants' sense of agency. Two factors were manipulated independently: the presence/absence of counterfactual comparisons between actions and the presence/absence of counterfactual comparisons between outcomes of these actions. Perceived agency was highest when both counterfactual comparisons were available. Interestingly, this pattern persisted even when counterfactual information was only revealed after action, suggesting a purely reconstructive evaluation effect. These findings allow a more precise phrasing of the CDO element of personal agency: a person feels most control when she could have performed another action, thereby obtaining another outcome

Differential functional connectivity underlying asymmetric reward-related activity in human and nonhuman primates

The orbitofrontal cortex (OFC) is a key brain region involved in complex cognitive functions such as reward processing and decision making. Neuroimaging studies have reported unilateral OFC response to reward-related variables; however, those studies rarely discussed this observation. Nevertheless, some lesion studies suggest that the left and right OFC contribute differently to cognitive processes. We hypothesized that the OFC asymmetrical response to reward could reflect underlying hemispherical difference in OFC functional connectivity. Using resting-state and reward-related functional MRI data from humans and from rhesus macaques, we first identified an asymmetrical response of the lateral OFC to reward in both species. Crucially, the subregion showing the highest reward-related asymmetry (RRA) overlapped with the region showing the highest functional connectivity asymmetry (FCA). Furthermore, the two types of asymmetries were found to be significantly correlated across individuals. In both species, the right lateral OFC was more connected to the default mode network compared to the left lateral OFC. Altogether, our results suggest a functional specialization of the left and right lateral OFC in primates.</jats:p