Sense Of 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.

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.

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.

Dysconnectivity of the Agency Network in Schizophrenia: A Functional Magnetic Resonance Imaging Study.

Background: Self-disturbances in schizophrenia have recently been explained by an abnormality in the sense of agency (SoA). The cerebral structures of SoA in healthy people are considered to mainly include the insula and inferior parietal lobule. In contrast, the functional lesion of aberrant SoA in schizophrenia is not yet fully understood. Considering the recent explanation of establishing SoA from the standpoint of associative learning, the “agency network” may include not only the insula and inferior parietal lobule but also the striatum. We hypothesized that aberrant SoA in schizophrenia is based on a deficit in the “agency network.”Methods: Functional magnetic resonance imaging data were acquired while patients with schizophrenia (n = 15) and matched controls (n = 15) performed our adaptation method of agency attribution task on a trial-by-trial basis to assess participants' explicit experience of the temporal causal relationship between an action and an external event with temporal biases. Analysis of functional connectivity was done using the right supramarginal gyrus and the right middle frontal gyrus as seed regions.Results: In healthy controls, analyses revealed increased activation of the right inferior parietal lobule (mainly the supramarginal gyrus), right insula, and right middle frontal gyrus as an activation of the agency condition. We defined activated Brodmann areas shown in the agency condition of healthy controls as the seed region for connectivity analysis. The connectivity analysis revealed lower connectivity between the head of the left caudate nucleus and right supramarginal gyrus in the patients compared to healthy controls.Conclusions: This dysconnectivity of the agency network in schizophrenia may lead to self-disturbance through deficits in associative learning of SoA. These findings may explain why pathological function of the striatum in schizophrenia leads to self-disturbance.

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.

Behavioral evidence of delayed prediction signals during agency attribution in patients with schizophrenia

Self-disturbance, a core feature of schizophrenia, recently has been explained from the standpoint of an abnormal sense of agency (SoA). Previous studies showed that aberrant SoA in schizophrenia arise from imprecise predictions about the sensory consequences of actions. However, the nature of the malfunctioning predictions remains unclear. We examined the temporally “delayed” nature of inadequate predictions. We studied 30 patients with schizophrenia and 30 healthy controls. Our original SoA task evaluates explicit experience of the temporal causal relationship between an intentional action and an effect on a computer screen under the presence of temporal biases. We introduced an adaptation with a “trial-by-trial” method that prolonged or shortened the temporal biases. We hypothesized that delayed prediction signals in schizophrenia could lead to a match in timing between predictions and actual outcomes, resulting in self-agency. The adjustment courses to changing temporal biases were evaluated. Patients with schizophrenia continued to feel self-agency even when the adjusted temporal bias was longer than 1000ms. This result indicated that patient's prediction would be delayed in each trial. Our study empirically showed behavioral evidence for “delayed” prediction signals in a SoA paradigm for the first time.

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.

Reduced sense of agency in chronic schizophrenia with predominant negative symptoms

Self-disturbances in schizophrenia have been regarded as a fundamental vulnerability marker for this disease, and have begun to be studied from the standpoint of an abnormal “sense of agency (SoA)” in cognitive neuroscience. To clarify the nature of aberrant SoA in schizophrenia, it needs to be investigated in various clinical subtypes and stages. The residual type of chronic schizophrenia with predominant negative symptoms (NS) has never been investigated for SoA. Accordingly, we investigated SoA by an original agency attribution task in NS-predominant schizophrenia, and evaluated the dynamic interplay between the predictive and postdictive components of SoA in the optimal cue integration framework. We studied 20 patients with NS-predominant schizophrenia, and compared with 30 patients with paranoid-type schizophrenia and 35 normal volunteers. NS-predominant schizophrenia showed markedly diminished SoA compared to normal controls and paranoid-type schizophrenia, indicating a completely opposite direction in agency attribution compared with excessive SoA demonstrated in paranoid-type schizophrenia. Reduced SoA was detected in experimental studies of schizophrenia for the first time. According to the optimal cue integration framework, these results indicate that there was no increase in compensatory contributions of the postdictive processes despite the existence of inadequate predictions, contrary to the exaggerated postdictive component in paranoid-type schizophrenia.

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.

Altered awareness of action in schizophrenia: a specific deficit in predicting action consequences

Patients suffering from schizophrenia may report unusual experiences of their own actions. They may either feel that external forces are controlling their actions or even their thoughts, or they may feel in control of events that in fact are not caused by their actions. Most theories link these disturbances in the sense of agency to deficits in motor prediction, resulting in a mismatch between predicted and actual sensory feedback at a central comparator mechanism. Such theories therefore can account for situations in which the sense of agency is reduced. However, other experiments as well as clinical observations show an enhanced rather than reduced sense of agency in schizophrenic patients. Here, we distinguish between a predictive and a retrospective mechanism where both contribute to the experience of agency, and show that schizophrenia is associated with a specific impairment to the predictive component. We measured subjective time estimates of self-initiated voluntary action (a key press) that were followed by a sensory effect (a tone). When the voluntary actions had a high probability of causing tones, healthy volunteers showed a predictive shift of the perceptual estimate of the action towards the tone, even on occasional trials where the tone was omitted. No such shift occurred in the absence of the tone on blocks when tones were less frequent. The predictive component of action awareness was calculated as the difference between time estimates on 'action only' trials from blocks with lower and higher tone probabilities. Schizophrenic patients lacked this predictive component of action awareness, showing a shift on 'action only' trials, regardless of the probability of the tone. Importantly, the schizophrenic deficit in predicting the relation between action and effect was strongly correlated with severity of positive psychotic symptoms, specifically delusions and hallucinations. Furthermore, the patients showed an exaggerated retrospective binding between action and tone, shifting the perceived time of action whenever the tone occurred, relative to when it did not occur. Our quantitative, implicit measures show how basic sensory and motor experience may be altered in acute psychosis. The enhanced sense of agency in schizophrenia reflects reliance on retrospection, rather than prediction, to associate actions with external events. The failure to predict the effects of one's own actions may underlie the blurring and confusion in the relationship between the self and the world that characterizes acute psychosis.

Agentivité : se vivre ou se juger agent ?

Composante du self, l’agentivité se définit par le fait de se vivre auteur de nos propres actions. Dans la schizophrénie, les idées d’influence, l’automatisme mental et les hallucinations acoustico-verbales seraient dus à un défaut d’agentivité. Frith a suggéré que l’agentivité reposait sur le système automatique de contrôle de l’action (modèles internes). Selon lui, une mauvaise prédiction de celle-ci, ne correspondant pas à l’action désirée, pourrait être à l’origine d’un trouble de l’agentivité. Les travaux de l’équipe de Jeannerod sur les jugements d’attribution ont nuancé cette théorie en avançant que l’agentivité impliquait également des processus conscients. Dernièrement, les travaux de l’équipe de Frith ont fait suggérer que ce serait l’atténuation du ressenti sensoriel, spécifique de nos propres actions, qui rendrait leur vécu différent de celles d’autrui. Le traitement du contexte social et des conséquences sensorielles secondaires à l’action serait également impliqué. L’évolution du concept d’agentivité s’explique par les différentes méthodologies employées. Deux éléments, en lien avec l’utilisation expérimentale de jugements d’attribution, sont source d’ambiguïtés: la définition même de l’agentivité et l’absence de réfutation des théories alternatives. Des études, permettant de préciser et d’explorer ces deux points, seraient nécessaires pour une meilleure compréhension de la physiopathologie de la schizophrénie. Experiencing oneself as the author of an action defines the sense of agency, which is a component of the self. A deficit affecting this process is thought to cause the principle symptoms characterizing schizophrenia - e.g. delusions of control and auditive hallucinations would exist because patients do not experience themselves as the author of their own actions. To explore this specific problem of the sense of agency in schizophrenia, Frith et al. collected a serie of experimental data that lead them to propose that the sense of agency relied on the automatic motor system, processes that enable the predictive adjustment of action. An impairment in these processes (called « internal models » in the literature) would lead to the problem of dissociation between our own actions and those performed by others. More specifically, the problem would lay in the comparison between the predicted state and the desired state (figure 1) . Jeannerod et al. from Lyon used attribution judgements that suggested that the sense of agency would not depend uniquely on the motor mechanisms but would also involve conscious processes. Recently, Frith et al. have published new data that integrates both preceding models. According to this theory, the sense of agency would depend on the processes involved in the predictive control of action but at a conscious level : the attenuation of the sensory feedback, specific of our own actions. This attenuation would depend on the accuracy of comparison between the predicted state and the actual state. Moreover, the sense of agency would also imply the management of social frame, which normally gives the means to cope with human interaction. The conception of the sense of agency has greatly evolved over the years, mainly because of the various experimental methods employed. The consequences of this are the various theoretical interpretations given to the characteristics of the sense of agency. They can be explained in two main points : a non-unified definition of the sense of agency and an absence of experimental data testing alternative interpretations. First, protocols using attribution judgements have proven to be useful to gain better understanding of the attribution mechanism in schizophrenia. However, findings obtained with these judgments have often been used to conclude on deficits of the sense of agency in schizophrenia, whereas the sense of agency is only a sub component of these judgements. More work must be conducted in order to show that generalization from judgements to self-agency is possible. Secondly, data have not been collected in order to go against the accepted proposition that the sense of agency (1) implies conscious processes, comes (2) secondary to action execution because based on sensory attenuation and (3) has subjective consequences only. Further studies would be useful to explore these points, so as to improve our understanding of the physiopathologyogy of schizophrenia.

A pre-reflective indicator of an impaired sense of agency in patients with Schizophrenia

In schizophrenia, passivity phenomenon are clinically related to an abnormal sense of agency, which has been experimentally studied through self-recognition tasks. However, Tsakiris et al. (Cognition 96(3):215-231, 2005) have recently shown in healthy controls that the sense of agency is distinct from self-recognition abilities. We propose a simple motor task to obtain an implicit indicator of the working status of the pre-reflective sense of agency in schizophrenia. Collision dynamics gave us the means to further dissociate agency from motor prediction. Twenty-four patients and a group of matched controls used a hand-held object to stop the fall of a pendulum that was released either by the Subject (task S) or by the Experimenter (task E). The objective indicator of the sense of agency was taken as the efficiency difference between tasks S and E, before the availability of afferent information from collision. Qualitative feedback was provided to assess the top-down effect of explicit information. Motor prediction was as accurate in patients as in controls in tasks E and S. Controls were more efficient in S than in E. Patients revealed similar efficiency levels in both tasks. Qualitative feedback helped but did not affect the efficiency difference between tasks. Our results suggest an impairment of a pure efferent-driven sense of agency in schizophrenia, which is (1) distinct from motor prediction and (2) not under voluntary control. The abnormal judgments previously reported in schizophrenia for self-recognition abilities might be the consequence of a low order deficit of a pre-reflective sense of agency.