Agency In Schizophrenia Research Articles

Hierarchical analysis of the sense of agency in schizophrenia: motor control, control detection, and self-attribution

The sense of agency refers to the feeling of initiating and controlling one’s actions and their resulting effects on the external environment. Previous studies have uncovered behavioral evidence of excessive self-attribution and, conversely, a reduction in the sense of agency in patients with schizophrenia. We hypothesize that this apparent paradox is likely to result from impairment in lower-level processes underlying the sense of agency, combined with a higher-level compensational bias. The present study employed three behavioral tasks utilizing the same stimuli and experimental design to systematically evaluate multiple factors that influence the sense of agency, including motor control, sensorimotor processing, and self-attribution. Participants’ real-time mouse movements were combined with prerecorded motions of others in ratios of 30/70, 55/45, or 80/20, with an additional angular bias of either 0° or 90°. Twenty-six patients with schizophrenia and 27 health control volunteers participated in the three tasks. Patients with schizophrenia performed significantly worse in the reaching and control detection tasks than healthy controls. However, their self-attribution in the control judgment task was comparable to that of the healthy controls. Patients with schizophrenia were impaired in motor control components and in the detection of control using sensorimotor information, but their evaluation of agency remained relatively less affected. This underscores the importance of distinguishing between different subcomponents when addressing the abnormal sense of agency in patients with schizophrenia. Subsequent cluster analysis revealed that the combined task performance accurately distinguished between the patients and healthy control participants.

Altered sense of agency in schizophrenia: the aberrant effect of cardiac interoceptive signals.

Schizophrenia (SZ) is characterized by abnormalities in self-representation, including a disturbed sense of agency (SoA). The continuous processing of sensory information concerning the internal state of the body (interoception) is argued to be fundamental to neural representations of the self. We, therefore, tested if aberrant interoception underpins disturbances in SoA in SZ, focusing on cardiac interoceptive signaling. Forty-two SZ and 29 non-clinical participants (healthy controls; HC) performed an intentional binding task to measure SoA during concurrent heartbeat recording. The effect of cardiac interoceptive signals on SoA was measured by the difference in intentional binding effect during systole and diastole. This measure was standardized based on the overall intentional binding effect to control for non-cardiac factors, and then compared between SZ and HC. Our study revealed a significant difference between SZ and HC groups, with opposite effects of cardiac systole on SoA. Specifically, cardiac systole disrupted SoA in SZ, contrasting with the enhanced SoA in HC. Across the SZ group, the extent to which SoA was disrupted by cardiac systole correlated significantly with a clinical proxy for symptom instability, namely the number of hospital admissions for hallucinations and delusions. Furthermore, the disruption was particularly observed in patients with severe hallucinations. This study revealed a disturbance in the impact of cardiac interoceptive signals on an implicit index of SoA in schizophrenia. This supports the notion that pathophysiological disruption of the central integration of interoceptive information increases vulnerability to disturbances in self-representation and the associated expression of schizophrenic symptoms.

Impaired perception of temporal contiguity between action and effect is associated with disorders of agency in schizophrenia

Delusions of control in schizophrenia are characterized by the striking feeling that one's actions are controlled by external forces. We here tested qualitative predictions inspired by Bayesian causal inference models, which suggest that such misattributions of agency should lead to decreased intentional binding. Intentional binding refers to the phenomenon that subjects perceive a compression of time between their intentional actions and consequent sensory events. We demonstrate that patients with delusions of control perceived less self-agency in our intentional binding task. This effect was accompanied by significant reductions of intentional binding as compared to healthy controls and patients without delusions. Furthermore, the strength of delusions of control tightly correlated with decreases in intentional binding. Our study validated a critical prediction of Bayesian accounts of intentional binding, namely that a pathological reduction of the prior likelihood of a causal relation between one's actions and consequent sensory events-here captured by delusions of control-should lead to lesser intentional binding. Moreover, our study highlights the import of an intact perception of temporal contiguity between actions and their effects for the sense of agency.

Sense of body ownership and body agency in schizophrenia

Recent research suggests that embodiment sensations (sense of body ownership and sense of body agency) are altered in schizophrenia. Using a mirror box illusion setup, we tested if the anomalous embodiment experience depends on deficient processing of visuomotor synchrony, disrupted processing of movement mode, or both. The task required participants to press a lever with their index while looking at the image of the experimenter’s hand moving on a similar lever. The illusion of embodiment could arise because looking toward the direction of their own hand the participant saw the reflection of the experimenter’s hand visually superimposed to his own one through a mirror. During the illusion induction, we systematically varied visuomotor asynchrony (4 delays were imposed on the movement of the experimenter’s hand) and the mode of movement (the participant could perform active vs. passive movements). The strength of the illusion of embodiment of the external hand was assessed with explicit judgments of ownership and agency. Patients’ data showed an anomalous modulation of ownership with respect to visuomotor synchrony manipulation and an altered modulation of agency with respect to both visuomotor synchrony and movement mode manipulations. Results from the present study suggest that impairments affecting both the processing of temporal aspects of visuomotor signals and the processing of type of movement underlie anomalous embodiment sensations in schizophrenia. Hypotheses about potential deficits accounting for our results are proposed.

Neural correlates of disturbance in the sense of agency in schizophrenia: An fMRI study using the ‘enfacement’ paradigm

An altered sense of self-awareness and agency has been proposed to underlie symptoms of schizophrenia. In this study, we used the enfacement illusion paradigm – in which perception of another person's face leads to changes in perception of one's own peri-personal space – to examine the brain correlates of the sense of agency and its potential disruption in schizophrenia. Thirty-three schizophrenic patients and 27 healthy controls underwent fMRI scanning during performance of a task designed to elicit the enfacement illusion. Activations were examined using whole-brain analysis and also in an a priori identified region of interest (ROI) in the temporoparietal junction (TPJ), a region that has been described as involved in self/other differentiation and sense of agency. Both groups showed a pattern of cortical activation involving the pre and postcentral cortex, Rolandic operculum, insula, parietal, temporal and occipital cortex bilaterally as well as TPJ (but only right-side in patients). Examination of the TPJ ROI revealed significantly reduced activation on the left in the patients that was associated with poorer insight. The findings suggest brain functional abnormality in schizophrenia related to the formation or maintenance of processes related to self and/or agency. Decreased function in the TPJ may have a role in the impaired insight seen in patients with the disorder.

Schizotypy and the vicarious experience of agency.

Sense of agency is the experience of initiating and controlling an action in order to influence one’s environment. It is widely accepted that various different sources of information contribute to sense of agency, including sensorimotor signals and external situational information. Moreover, it has been suggested that atypical experiences in sense of agency in schizophrenia are linked to changes in the relative influence of these agency cues, with external cues being more dominant. This study tests this hypothesis in a non-clinical population by investigating the relationship between schizotypy and performance on the vicarious agency task (a classic demonstration of the effect of external cues on sense of agency). We found that increased susceptibility to the vicarious agency illusion (i.e. an increased feeling of controlling someone else’s action) was linked to higher schizotypy scores. This supports the idea that aberrant experiences of agency in schizophrenia are linked to an increased sensitivity to external agency cues.

Embodied Predictions, Agency, and Psychosis.

Psychotic symptoms, i.e., hallucinations and delusions, involve gross departures from conscious apprehension of consensual reality; respectively, perceiving and believing things that, according to same culture peers, do not obtain. In schizophrenia, those experiences are often related to abnormal sense of control over one's own actions, often expressed as a distorted sense of agency (i.e., passivity symptoms). Cognitive and computational neuroscience have furnished an account of these experiences and beliefs in terms of the brain's generative model of the world, which underwrites inferences to the best explanation of current and future states, in order to behave adaptively. Inference then involves a reliability-based trade off of predictions and prediction errors, and psychotic symptoms may arise as departures from this inference process, either an over- or under-weighting of priors relative to prediction errors. Surprisingly, there is empirical evidence in favor of both positions. Relatedly, there is evidence for both an enhanced and a diminished sense of agency in schizophrenia. How can this be? We argue that there is more than one generative model in the brain, and that ego- and allo-centric models operate in tandem. In brief, ego-centric models implement corollary discharge signals that cancel out the effects of self-generated actions while allo-centric models compare several hypothesis regarding the causes of sensory inputs (including the self among the potential causes). The two parallel hierarchies give rise to different levels of agency, with ego-centric models subserving “feelings of agency” and allo-centric predictions giving rise to “judgements of agency.” Those two components are weighted according to their reliability and combined, generating a higher-level “sense of agency.” We suggest that in schizophrenia a failure of corollary discharges to suppress self-generated inputs results in the absence of a “feeling of agency” and in a compensatory enhancement of allo-centric priors, which might underlie hallucinations, delusions of control but also, under certain circumstances, the enhancement of “judgments of agency.” We discuss the consequences of such a model, and potential courses of action that could lead to its falsification.

What Makes Action and Outcome Temporally Close to Each Other: A Systematic Review and Meta-Analysis of Temporal Binding

Temporal binding refers to the subjective compression of the temporal interval between a voluntary action and its external sensory consequences. While empirical evidence and theoretical accounts have indicated the potential linkage between temporal binding and action outcome prediction mechanisms, several questions regarding the underlying processes and the fundamental nature of temporal binding remain unanswered. Based on the sophisticated classification of predictive processes proposed by Hughes et al. (2013), we conducted a systematic, quantitative review of the binding effect as measured with two representative procedures, i.e., Libet clock procedure and interval estimation procedure. Although both procedures were designed to measure the same phenomenon, we revealed a larger effect size and higher sensitivity to perceptual moderators in binding observed with the clock procedure than with the interval estimation. Moreover, in the former, we observed different characteristics for the two perceptual shifts that comprise temporal binding. Action shifts depended more on whether one can control outcome onsets with voluntary actions. In contrast, outcome shifts depended more on the degree to which participants could predict, rather than control, the action outcome onset. These results indicate that action shift occurs based on the activation of learned action–outcome associations by planning and executing actions, while outcome shift occurs based on comparing predicted and observed outcomes. By understanding the nature of each experimental procedure and each shift, future research can use optimal methods depending on the goal. We discuss, as an example, the implications for the underlying disorders of agency in schizophrenia.

Reduced transfer of visuomotor adaptation is associated with aberrant sense of agency in schizophrenia

One deficit associated with schizophrenia (SZ) is the reduced ability to distinguish self-caused sensations from those due to external sources. This reduced sense of agency (SoA, subjective awareness of control over one’s actions) is hypothesized to result from a diminished utilization of internal monitoring signals of self-movement (i.e., efference copy) which subsequently impairs forming and utilizing sensory prediction errors (differences between the predicted and actual sensory consequences resulting from movement). Another important function of these internal monitoring signals is the facilitation of higher-order mechanisms related to motor learning and control. Current predictive-coding models of adaptation postulate that the sensory consequences of motor commands are predicted based on internal action-related information, and that ownership and control of motor behavior is modified in various contexts based on predictive processing. Here, we investigated the connections between SoA and motor adaptation. Schizophrenia patients (SZP, N=30) and non-psychiatric control subjects (HC, N=31) adapted to altered movement visual feedback and applied the motor recalibration to untested contexts (i.e., the spatial generalization). Although adaptation was similar for SZP and controls, the extent of generalization was significantly less for SZP; movement trajectories made by patients to the furthest untrained target (135o) before and after adaptation were largely indistinguishable. Interestingly, deficits in generalization were correlated with positive symptoms of psychosis in SZP (e.g., hallucinations). Generalization was also associated with measures of SoA across both SZP and HC, emphasizing the role action awareness plays in motor behavior, and suggesting that misattributing agency, even in HC, manifests in abnormal motor performance.

Bodily Experience in Schizophrenia: Factors Underlying a Disturbed Sense of Body Ownership.

Emerging evidence is now challenging the view that patients diagnosed with schizophrenia experience a selective deficit in their sense of agency. Additional disturbances seem to exist in their sense of body ownership. However, the factors underlying this disturbance in body ownership remain elusive. Knowledge of these factors, and increased understanding of how body ownership is related to other abnormalities seen in schizophrenia, could ultimately advance development of new treatments. Research on body ownership in schizophrenia has mainly been investigated with the rubber hand illusion (RHI). Schizophrenia patients show higher susceptibility to the RHI, which may be explained by a stronger reliance on multisensory information over weaker stored body representations. This review shows that a coherent sense of body ownership arises from the integration of both bottom-up sensory processes and higher order, top-down bodily- and perceptual representations. Multisensory integration, temporal binding, anticipation, intention and efferent signals all partly modulate the complex experience of body ownership. Specifically, we propose that patients with schizophrenia have weaker stored body representations, and rely to a greater extent on external stimuli, such as visual information, due to imprecise or highly variable internal predictions. Moreover, the reduced sense of agency in schizophrenia may additionally contribute to the disturbed sense of body ownership, as evidence from healthy participants suggests that agency and body ownership are interrelated. Vice versa, a reduced sense of body ownership may also contribute to a reduced sense of agency. Future studies should explicitly target the precise relationship between the two in schizophrenia.

Disrupted Saccadic Corollary Discharge in Schizophrenia.

According to the World Health Organization, acute schizophrenia carries more disability weight than any other disease, but its etiology remains unknown. One promising theory of schizophrenia highlights alterations in a sense of self, in which self-generated thoughts or actions are attributed externally. Disruptions in corollary discharge (CD), motor signals sent to sensory areas that allow for the prediction of impending sensations, are proposed to underlie these symptoms. Direct physiological evidence, however, is limited. In nonhuman primates, inactivation of mediodorsal thalamic neurons disrupts CD associated with eye movements. Using the same task, we show similar impairments in schizophrenia patients, consistent with disrupted CD. These findings allow us to link clinical phenomenology to primate neurophysiology and interpret findings within a biological framework.

Deficits in agency in schizophrenia, and additional deficits in body image, body schema, and internal timing, in passivity symptoms.

Individuals with schizophrenia, particularly those with passivity symptoms, may not feel in control of their actions, believing them to be controlled by external agents. Cognitive operations that contribute to these symptoms may include abnormal processing in agency as well as body representations that deal with body schema and body image. However, these operations in schizophrenia are not fully understood, and the questions of general versus specific deficits in individuals with different symptom profiles remain unanswered. Using the projected-hand illusion (a digital video version of the rubber-hand illusion) with synchronous and asynchronous stroking (500 ms delay), and a hand laterality judgment task, we assessed sense of agency, body image, and body schema in 53 people with clinically stable schizophrenia (with a current, past, and no history of passivity symptoms) and 48 healthy controls. The results revealed a stable trait in schizophrenia with no difference between clinical subgroups (sense of agency) and some quantitative (specific) differences depending on the passivity symptom profile (body image and body schema). Specifically, a reduced sense of self-agency was a common feature of all clinical subgroups. However, subgroup comparisons showed that individuals with passivity symptoms (both current and past) had significantly greater deficits on tasks assessing body image and body schema, relative to the other groups. In addition, patients with current passivity symptoms failed to demonstrate the normal reduction in body illusion typically seen with a 500 ms delay in visual feedback (asynchronous condition), suggesting internal timing problems. Altogether, the results underscore self-abnormalities in schizophrenia, provide evidence for both trait abnormalities and state changes specific to passivity symptoms, and point to a role for internal timing deficits as a mechanistic explanation for external cues becoming a possible source of self-body input.

A new comparator account of auditory verbal hallucinations: how motor prediction can plausibly contribute to the sense of agency for inner speech.

The comparator account holds that processes of motor prediction contribute to the sense of agency by attenuating incoming sensory information and that disruptions to this process contribute to misattributions of agency in schizophrenia. Over the last 25 years this simple and powerful model has gained widespread support not only as it relates to bodily actions but also as an account of misattributions of agency for inner speech, potentially explaining the etiology of auditory verbal hallucination (AVH). In this paper we provide a detailed analysis of the traditional comparator account for inner speech, pointing out serious problems with the specification of inner speech on which it is based and highlighting inconsistencies in the interpretation of the electrophysiological evidence commonly cited in its favor. In light of these analyses we propose a new comparator account of misattributed inner speech. The new account follows leading models of motor imagery in proposing that inner speech is not attenuated by motor prediction, but rather derived directly from it. We describe how failures of motor prediction would therefore directly affect the phenomenology of inner speech and trigger a mismatch in the comparison between motor prediction and motor intention, contributing to abnormal feelings of agency. We argue that the new account fits with the emerging phenomenological evidence that AVHs are both distinct from ordinary inner speech and heterogeneous. Finally, we explore the possibility that the new comparator account may extend to explain disruptions across a range of imagistic modalities, and outline avenues for future research.

The crisis of minimal self-awareness in schizophrenia: A meta-analytic review

Disturbances of the minimal self, characterized by abnormal sense of the body, body ownership and agency have been proposed as the phenomenological phenotype of schizophrenia. However, self-disturbances have not been extensively investigated, in part, due to the subjective nature of such processes, and the associated difficulty of studying these phenomena using empirical methodology.Of 115 potential studies on self-awareness in schizophrenia, a total of 25 studies met the inclusion criteria for the meta-analysis comprising 690 patients with schizophrenia and 979 healthy controls. We calculated Hedge's g to obtain a better estimate for the standardized mean difference in small samples.We identified significant basic self-disturbance in schizophrenia, as compared with healthy controls (25 studies, effect size=0.51). Additional comparison of three sub-categories of the sense of body ownership (4 studies, effect size=0.91), the sense of agency (15 studies, effect size=0.49), and self-reported subjective experiences (6 studies, effect size=0.57) also confirmed group differences. The complete set of 25 studies, and the studies in the sub-categories showed the statistical homogeneity of the characteristics. After a correction for potential publication bias using the trim-and-fill method, the main findings for all studies combined remained significant.Overall, patients with schizophrenia showed deficits in the sense of the minimal self, driven by abnormal sense of body ownership and sense of agency. Interestingly, the disturbed sense of agency in schizophrenia suggests an exaggerated self-consciousness rather than a diminished sense of self. Further research that utilizes sophisticated study designs is needed to examine the nature of self-disturbances in schizophrenia.

Attenuation of auditory N1 results from identity‐specific action‐effect prediction

The auditory N1 event-related potential has previously been observed to be attenuated for tones that are triggered by human actions. This attenuation is thought to be generated by motor prediction mechanisms and is considered to be important for agency attribution. The present study was designed to rigorously test the notion of action prediction-based sensory attenuation. Participants performed one of four voluntary actions on each trial, with each button associated with either predictable or unpredictable action effects. In addition, actions with each hand could result in action effects that were either congruent or incongruent with hand-specific prediction. We observed no significant differences in N1 amplitude between predictable and unpredictable tones. When contrasting action effects that were congruent or incongruent with hand-specific prediction, we observed significant attenuation for prediction-congruent compared to prediction-incongruent action-effects. These novel findings suggest that accurate action-effect prediction drives sensory attenuation of auditory stimuli. These findings have important implications for understanding the mechanisms of action-effect prediction and sensory attenuation, and may have clinical implications for studies investigating action awareness and agency in schizophrenia.

Mechanisms of intentional binding and sensory attenuation: The role of temporal prediction, temporal control, identity prediction, and motor prediction.

Sensory processing of action effects has been shown to differ from that of externally triggered stimuli, with respect both to the perceived timing of their occurrence (intentional binding) and to their intensity (sensory attenuation). These phenomena are normally attributed to forward action models, such that when action prediction is consistent with changes in our environment, our experience of these effects is altered. Although much progress has been made in recent years in understanding sensory attenuation and intentional binding, a number of important questions regarding the precise nature of the predictive mechanisms involved remain unanswered. Moreover, these mechanisms are often not discussed in empirical papers, and a comprehensive review of these issues is yet to appear. This review attempts to fill this void. We systematically investigated the role of temporal prediction, temporal control, identity prediction, and motor prediction in previous published reports of sensory attenuation and intentional binding. By isolating the individual processes that have previously been contrasted and incorporating these experiments with research in the related fields of temporal attention and stimulus expectation, we assessed the degree to which existing data provide evidence for the role of forward action models in these phenomena. We further propose a number of avenues for future research, which may help to better determine the role of motor prediction in processing of voluntary action effects, as well as to improve understanding of how these phenomena might fit within a general predictive processing framework. Furthermore, our analysis has important implications for understanding disorders of agency in schizophrenia.

Agency: its nature and role in recovery from severe mental illness

Agency: its nature and role in recovery from severe mental illness

Judgements of agency in schizophrenia: an impairment in autonoetic metacognition

We investigated judgements of agency in participants with schizophrenia and healthy controls. Participants engaged in a computer game in which they attempted to touch downward falling Xs and avoid touching Os. On some trials, participants were objectively in perfect control. On other trials, they were objectively not in complete control because the movement of the cursor on the screen was distorted with respect to the position of the mouse by random noise (turbulence), or it was lagged by 250 or 500 ms. Participants made metacognitive judgements of agency as well as judgements of performance. Control participants' judgements of agency were affected by the turbulence and lag variables-indicating that they knew they were objectively not in control in those conditions, and they were also influenced by their assessments of performance. The patients also used their assessments of performance but neither turbulence nor lag affected their judgements of agency. This indicated an impairment in agency monitoring. The patients, unlike the healthy controls, used only publically available external cues about performance in making judgements of 'agency' and did not rely on any additional access to internal self-relevant cues that were diagnostic in indicating whether or not they were, in fact, in control.

Misattributions of agency in schizophrenia are based on imprecise predictions about the sensory consequences of one's actions

Misattributions of agency in schizophrenia are based on imprecise predictions about the sensory consequences of one's actions

Altered sense of agency in schizophrenia and the putative psychotic prodrome

The mechanisms underlying distortions in sense of agency, i.e. the experience of controlling one's own actions and their consequences, in schizophrenia are not fully understood and have barely been investigated in patients classified as being in a putative psychotic prodrome. This study aims to expound the contribution of early and late illness-related processes. Thirty schizophrenia patients, 30 putatively prodromal patients and 30 healthy controls were instructed to reproduce a computer-generated series of drum sounds on a drum pad. While tapping, subjects heard either their self-produced tones or a computer-controlled reproduction of the drum tone series that used either exactly the same, an accelerated or decelerated tempo. Subjects had to determine the source of agency. Results show similar significant impairments in assigning the source of agency under ambiguous conditions in schizophrenia and putatively prodromal patients and an exaggerated self-attribution bias, both of which were significantly correlated with increased (ego-)psychopathology. Patient groups, however, benefited significantly more than controls from additional sensorimotor cues to agency. Sensorimotor input seems to be a compensatory mechanism involved in correctly attributing agency. We deduce that altered awareness of agency may hold promise as an additional risk factor for psychosis.