Sense of agency disturbances in movement disorders: A comprehensive review

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Highlights

  • Abnormal agency experiences characterize different movement disorders.

  • Agency disturbances are associated with SMA structural and functional abnormalities.

  • Different measures of the sense of agency often provide divergent results.

Abstract

Sense of agency refers to the experience that one’s self-generated action causes an event in the external environment. Here, we review the behavioural and brain evidence of aberrant experiences of agency in movement disorders, clinical conditions characterized by either a paucity or an excess of movements unrelated to the patient’s intention. We show that specific abnormal agency experiences characterize several movement disorders. Those manifestations are typically associated with structural and functional brain abnormalities. However, the evidence is sometimes conflicting, especially when considering results obtained through different agency measures. The present review aims to create order in the existing literature on sense of agency investigations in movement disorders and to provide a coherent overview framed within current neurocognitive models of motor awareness.

Introduction

The sense of agency refers to the feeling that one voluntarily initiates and controls actions, and generates, through them, effects in the external world (P. Haggard, 2017). The sense of agency is altered in several psychiatric and neurological conditions (Moore & Fletcher, 2012). Schizophrenia represents a classic agency disorder. It has been the subject of most of the agency research in pathological conditions. Passivity phenomena in schizophrenia clearly implicate the misattribution of thoughts or actions to an external agent (Synofzik, Thier, Leube, Schlotterbeck, & Lindner, 2010). In the condition of delusion of control, an individual firmly believes that her/his own action has been initiated and controlled by another agent (C. D. Frith, S. Blakemore, & D. M. Wolpert, 2000a). Similarly, the thought insertion symptoms entail thoughts to be perceived as externally generated, as they have been inserted in a patient’s mind without permission (Frith et al., 2000a). However, aberrant experiences of agency are not restricted to schizophrenic patients but can be observed in other clinical conditions, like obsessive–compulsive behaviour (Gentsch, Schütz-Bosbach, Endrass, & Kathmann, 2012), borderline personality disorder (Colle, Hilviu, Rossi, Garbarini, & Fossataro, 2020), and movement disorders (Moore et al., 2010, Saito et al., 2017). This latter condition is the specific topic of the present review.

Movement disorders are clinical syndromes characterized by either a paucity or an excess of movements unrelated to the patient’s intention. They include, among others, Gilles de la Tourette Syndrome, Parkinson’s disease, Huntington's disease, corticobasal syndrome, and other psychogenic conditions, like functional movement disorders.

There are several reasons for expecting an altered sense of agency in movement disorders. First, the neural correlates of the sense of agency partially overlap with the neurofunctional network of voluntary movements, with particular reference to the supplementary and pre-supplementary motor areas (SMA, pre-SMA, Kühn et al., 2013, Moore et al., 2010, Zapparoli et al., 2020). It follows that the sense of agency might be generated by the same sensorimotor system that generates and controls motor execution and is differently compromised in movement disorders. Therefore, it is reasonable to expect that any malfunctioning of the sensorimotor system, particularly involving the SMA/pre-SMA network, may affect the subjective experience of agency to various degrees. Movement disorders might be associated with an impaired agency experience also because of the motoric symptoms. For example, it has been hypothesized that voluntary movements may be hard to distinguish from tics in Gilles de la Tourette’s syndrome patients due to the high level of noise in the sensorimotor system induced by the hyperkinetic production (Ganos et al., 2015). Furthermore, agency disturbances in movement disorders might be either a consequence of the disease or a side-effect of the disease’s pharmacological treatment, as suggested, for instance, for dopaminergic treatment in Parkinson’s disease (Moore, Schneider, et al., 2010). These considerations make movement syndromes particularly interesting for agency studies and have motivated the investigation of the sense of agency in movement disorders over the years. However, to date, a comprehensive understanding of the disturbances of the sense of agency in relation to movement disorders is still missing.

The present review provides a comprehensive overview of the behavioural, structural, and functional brain abnormalities linked to the sense of agency experience in movement disorders patients, framed within current neurocognitive models of motor awareness. We start this review by describing the different theoretical frameworks that address the arising of the sense of agency from a neurocognitive perspective. Then, we introduce the experimental paradigms typically used to measure the agency experience and its neural correlates. In the second part of the review, we analyse the existing literature on the sense of agency in movement disorders. We describe the behavioural and brain evidence that has revealed specific abnormalities in motor awareness in populations affected by movement disorders. We address whether there is a consistency in agency disturbances across different movement disorders or whether specific alterations characterize each condition. We consider if such agency disturbances are coherent across the different measures of the agency experience (i.e., implicit and explicit measures). When possible, we also include the neural correlates of the described sense of agency disturbances. We complemented the revision by discussing how the current neurocognitive models of motor awareness can address these aberrant manifestations.

In social sciences, the term “agency” refers to individuals' ability to act on their own will. Besides the objective facts of agency, linked to motor preparation and action execution, the agency is also a subjective experience, or “sense” (Patrick Haggard & Eitam, 2015). The term “sense of agency” refers to this subjective experience, and typically entails “the experience of controlling one’s own actions and, through them, the course of events in the outside world” (P. Haggard, 2017).

The origins of the sense of agency in the human mind are still under investigation. Several theories have been proposed to address the arising of the sense of agency. These theories imply different levels of description, from the top-down inferential processes to the fine-grained neural mechanisms. These are summarized in Table 1.

The apparent mental causation theory (Wegner, 2003) offers a theoretical explanation of the sense of agency generation as a top-down inferential process. In particular, this theory describes the experience of agency as a retrospective insertion to consciousness or a post-hoc reconstruction of events and their likely causes (Wegner & Wheatley, 1999). Accordingly, the sense of agency would arise from an inferential sense-making process computed after the end of the movement, in accordance with three main principles: priority, consistency, exclusivity. If (1) a thought becomes conscious just before an action (priority), (2) the thought is consistent with the action (consistency) and (3) it is not accompanied by apparent alternative causes of the action (exclusivity), the agent ascribes the generated sensory consequences to one’s own action (Wegner, 2003). This theory is intriguing, but it accounts for a theoretical explanation level that refrains from any explanations of the mechanisms involved in the sense of agency generation.

A mechanistic account of the sense of agency belongs to the so-called Comparator Model (Blakemore et al., 2002, Frith et al., 2000), which is based on concepts from optimal motor control theory (Franklin and Wolpert, 2011, Wolpert and Ghahramani, 2000). Central to this theory is the idea that the motor control system relies on the so-called “internal models”, which represent the motor-to-sensory transformations and how these are implemented in the physical world. Action control mainly depends on the joint activity of these internal models and a series of comparators, namely mechanisms that compare signals and use the result of the comparison to regulate the system. Within this framework, the sense of agency arises from the comparison between predictive signals generated by the internal models during motor planning (the so-called “efference copy”) and the actual sensory effects of one’s action (hence the name “Comparator Model”, Blakemore et al., 2002, Frith et al., 2000). An action is perceived as self-caused when there is a match between the predicted and experienced sensory effects (P. Haggard, 2017). This theory offers a mechanistic explanation of the sense of agency that may seem incompatible with the theoretical proposal of the apparent mental causation theory. While the optimal motor control theory and comparator model highlighted the role of “internal” motor signals in the generation of the agency experience, the apparent mental causation theory seems to favour inferential processes based on “external”, contextual signals. This dichotomy has been solved by a recent proposal that stresses the role of both sources of information in the emergence of the sense of agency (Moore et al., 2009, Synofzik et al., 2008a, Wolpe et al., 2013). Moore et al. (2009) suggested that the sense of agency arises from a weighted integration of internal and external cues, together with prior beliefs. This theory – called “cue integration theory” – also suggested that the relative influence of the different information sources may be linked to their reliability, with the more reliable source of information dominating the agentic experience (Moore et al., 2009).

However, these theories still lack a biologically plausible explanation of the processes of agency in terms of their underlying brain mechanisms. This further level of explanation appeals instead to theories that have tried to link the putative cognitive processes of agency to biologically plausible mechanisms.

Among them, active inference rests upon the idea that the brain uses “internal generative models” to explain the source of the incoming sensory information with the ultimate purpose of minimizing the free energy of the model, its “entropy”, or more simply the “surprise” associated with sensations (Friston, Mattout, & Kilner, 2011). Crucially, active inference proposes that the cerebral cortex, and the larger-scale organization of different brain networks, are hierarchically organized. The upper levels represent abstract, high-level, domain-general, multimodal beliefs. Intermediate levels contain modality-specific beliefs related to sensations. Lower levels address specific predictions for specific sensations, like immediate proprioceptive predictions. There is a set of neurons encoding predictions at each level, and another set encoding prediction errors, which corresponds, in the context of motor control, to the amount to unexpected proprioceptive and exteroceptive sensations contingent on the action.

The fit between model predictions – what it can explain – and sensations is assured in two ways. On the one hand, the brain could update its predictions about the sensory data through perceptual inference. Alternatively, the fit could be optimised by changing the sensory data (Parr & Friston, 2019). This latter purpose can be realised by acting on the world, such that the sensations are more consistent with the model expectations. The mechanism by which the prediction error is resolved (changing predictions or changing sensory evidence through actions) is determined by the relative precision-weighting of predictions and prediction errors, with the more precise source of information dominating the agentic experience. Predictions that initiate a movement prevail when the precision of the current somatosensory state is down-weighted relative to predictions (Brown, Adams, Parees, Edwards, & Friston, 2013). From a neurobiological point of view, the precision is proposed to be encoded by synaptic gain, i.e., the inverse of the variance in the fluctuation of neuronal activity. In turn, these modulations in synaptic gain are thought to underlie the physiological sensory attenuation seen prior to and during the movement in the somatosensory cortex (Brown et al., 2013). This physiological sensory attenuation seen before and during movements should not be confused with the so-called psychophysical (or perceptual) sensory attenuation evoked by the consequences of the generated movements and recorded after the execution of the movement (please see the methods session).

Within the generative model, the sense of agency is implicit in the cycle of active sampling of sensations. Precisely, the sense of agency is thought to emerge from the successful balancing of the precision of prediction errors within the cortical hierarchy for action, and the ability of this balanced hierarchy to converge on the most likely cause of a self-generated sensation, i.e., the agent himself. Thus, active inference approaches the study of the sense of agency by reducing it to an active inference problem (Friston et al., 2013). Precisely, the inference that has to be made by the agent corresponds to the estimation of the probability that one was the agent of the action (“who is the agent that is minimizing the free energy?”) given the sensory attributes of that action (proprioception, sensorimotor feedback, external cues) and the prior probability that the action was executed by the agent (i.e., the probability that the agent was optimal in minimizing the free energy associated with the desired outcomes of its actions). In this way, the active inference framework is able to contain in itself both the theoretical cues from the apparent mental causation theory and the mechanistic explanation of the comparator model, giving at the same time new hints on the neurobiology of the agency generation.

In this paper, we will take advantage of those (neuro)cognitive models to review the several expressions of aberrant experiences of agency in movement disorders by discussing, at the same time, the manifestations that are largely expected and those that escape the current explanations.

In the last twenty years, several experimental paradigms have been designed to capture the subjective experience of agency in experimental settings. These are summarized in Table 2.

Explicit measures of agency rest upon humans’ ability to reflect on their agentic role when directly asked about it. The most widely used task in the research setting is the so-called “action-recognition task.” In a typical example, participants perform specific actions without having the possibility of seeing their movements. Rather, they see feedback through a screen that can refer to either the participant’s movement or a temporal/spatial experimental manipulation of it. Participants are then asked to judge whether the video they are watching is showing their own movements or those of another person (i.e., the experimenter), or the degree of control they experience over the seen scene (Farrer et al., 2008, Farrer et al., 2008).

Implicit measures of agency rely on unconscious behavioural biases that provide indirect clues of our agentic experience. A major one is the intentional binding effect (P. Haggard, Clark, & Kalogeras, 2002). Intentional binding refers to a phenomenon whereby voluntary actions, but not passively induced movements, are perceived as temporally shifted towards their effects (i.e., action-binding effect), and their effects (e.g., a tone) as shifted back towards the actions that caused them (i.e., tone-binding effect). As a result, a time compression between voluntary actions and effects is reported (i.e., overall binding-effect, P. Haggard et al., 2002).

Another implicit marker of the sense of agency is the sensory attenuation phenomenon (or sensory suppression). This phenomenon describes the human tendency to perceive the sensory consequences of voluntary actions as less intense than the same stimuli generated by passive movements (Blakemore et al., 2000, Blakemore et al., 1998). This phenomenon can be observed at both behavioural (e.g., different behavioral responses in the “force-matching type-tasks”, see, for example, Shergill, Samson, Bays, Frith, & Wolpert, 2005) and neural level (e.g., reduced ERPs for action-triggered versus externally triggered stimuli, see, for example, Hughes & Waszak, 2011 for attenuation of visual responses; and Martikainen, Kaneko, & Hari, 2005 for attenuation of auditory responses).

Although explicit and implicit measures of agency are useful in capturing the sense of agency experience in experimental settings, both measures have theoretical and methodological limitations.

Explicit paradigms are undoubtedly intuitive, but they can be vulnerable to cognitive biases, typical of self-report measures. For example, people can overestimate their agency, claiming authorship of actions or consequences that are not their own (see, for example, Wegner & Wheatley, 1999). Moreover, explicit judgments of agency are rare in everyday life. While they might have a significant role in social settings where individuals may be held responsible or liable for the consequences of their behaviour, the everyday experience of agency mostly relies on the implicit background feelings of being in control (Kühn et al., 2013).

Implicit measures have their methodological weaknesses as well. For example, intentional binding is usually observed on a group level, but there is a large variability between subjects. The source of this variability is largely unknown (Wolpe & Rowe, 2014). More importantly, it has been shown that an intentional binding effect can sometimes be also observed even in the absence of intentionality (Buehner, 2012, Suzuki et al., 2019).

Furthermore, the relationship between implicit and explicit measures of agency is still a matter of debate. While it is widely accepted that there are separable, and to some extent independent, agency processing systems (Synofzik et al., 2008a), the two measures sometimes co-occur and sometimes dissociate (Moore, Middleton, Haggard, & Fletcher, 2012).

In the past two decades, both explicit and implicit measures have been extensively used to explore the brain mechanisms underlying the sense of agency through neuroimaging, non-invasive brain stimulation, and electrophysiological studies.

Most of the studies measuring agency with explicit attribution judgments have consistently highlighted the involvement of the parietal cortex, especially the inferior parietal cortex and the angular gyrus, in the sense of agency experience (Farrer et al., 2003, Farrer et al., 2008, Farrer and Frith, 2002, Preston and Newport, 2008; for a meta-analysis of 15 neuroimaging studies see also Sperduti, Delaveau, Fossati, & Nadel, 2011 or Seghezzi, Giannini & Zapparoli, 2019). However, the parietal activations observed in neuroimaging studies seem associated with the perturbed experience of agency, i.e., when the (visual) feedback is judged as externally-generated in the so-called “no-agency condition”. The neural correlates of self-agency attribution are still unclear. Several studies have hypothesized the role of the frontal and prefrontal cortex in the sense of agency generation (see for example Chambon et al., 2013, Renes et al., 2015). Other studies emphasized the role of the parietal cortex (see, for example, Leube, Knoblich, Erb, & Kircher, 2003), insula (see, for example, Farrer et al., 2003, Farrer and Frith, 2002, Leube et al., 2003) and cerebellum (see, for example, Fukushima, Goto, Maeda, Kato, & Umeda, 2013). For a graphical representation of the brain regions that have been associated with the self-agency experience, please see Fig. 1a.

New insights come from studies that explored the brain mechanisms of the sense of agency by taking advantage of the intentional binding phenomenon. Those studies have consistently shown a link between the activity of the supplementary motor area (SMA), with reference to its anterior portion (pre-SMA), and the magnitude of the intentional binding effect (Cavazzana et al., 2015, Kühn et al., 2013, Moore et al., 2010, Seghezzi and Zapparoli, 2020, Zapparoli et al., 2020). For a graphical representation of the brain regions that have been associated with the intentional-binding effect, please see Fig. 1b.

However, it is becoming increasingly clear that such a complex phenomenon like the sense of agency experience is more likely to be associated with the functioning of brain in networks instead of single structures. One hypothesis is that the key neural substrate of the sense of agency lies in the effective connectivity between the pre-SMA that initiates actions and parietal areas that monitors the generating consequences of actions (P. Haggard, 2017).

Section snippets

Sense of agency disturbances in movement disorders

To provide a comprehensive overview of the behavioural, structural, and functional brain abnormalities linked to the sense of agency experience in movement disorders patients, we performed literature research in the PubMed database (https://pubmed.ncbi.nlm.nih.gov).

Specifically, the studies included in this review were retrieved through the following queries: [“Sense of agency] AND [ “Movement disorders” OR “Parkinson’s disease” OR “Gilles de la Tourette” OR “Functional Movement Disorders” OR

Conclusions

An altered sense of agency characterizes several movement disorders. Agency disturbances in Parkinson’s disease were revealed by a reduction of the subjective agency and an altered action-biding in intentional binding paradigms (Saito et al., 2017). Sense of agency disturbances in Gilles de la Tourette syndrome may occur as an inflated subjective experience of agency (Delorme, Salvador, et al., 2016) or as the absence of an overall-binding effect (Zapparoli, Seghezzi, Devoto, et al., 2020).

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgement

None.

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