Aberrant sense of agency in patients with schizophrenia: Forward and backward over-attribution of temporal causality during intentional action
Introduction
Alterations of self-experience have long been noted as a core feature of schizophrenia. Such disturbances are generally referred to as “self-disturbances” and are characterized by diminished self-affection, which is defined as a weakened sense of existing as a vital and self-coinciding source of awareness and action (Sass and Parnas, 2003). The First Rank Symptoms consist of obvious self-disturbances including passivity experiences or delusions of control where patients feel their own thoughts and actions are influenced or controlled by others (Schneider, 1950). Furthermore, these self-disturbances might be present in the early stages of schizophrenia and have been regarded as a fundamental trait or vulnerability marker for schizophrenia (Parnas and Handest, 2003, Sass and Parnas, 2003, Nelson et al., 2008, Nelson et al., 2009).
The nature of these self-disturbances is hardly studied in neuroscience, because self-disturbances represent subjective experiences and can only be described from the first-person perspective of the patient. However, in recent years, focus has shifted to self-consciousness in cognitive neuroscience, and especially to the “sense of agency” (Gallagher, 2000, Haggard, 2005, Tsakiris et al., 2007, Moore and Haggard, 2008), which is the feeling that a person is causing and controlling his/her own actions and their effects in the outside world. Self-disturbances in schizophrenia have begun to be explained and studied from the standpoint of an abnormal sense of agency (Georgieff and Jeannerod, 1998, Frith et al., 2000, Stephens and Graham, 2000). Two types of tasks for evaluating the sense of agency exist (Haggard, 2006) and have been used in patients with schizophrenia. The agency attribution task is an explicit measure of the sense of agency in which people verbally report how much they feel a sense of control over an event or their own body. In contrast, a test investigating the temporal relation between an action and an effect by subjective time estimates is an implicit measure of sense of agency.
Previous studies using explicit agency-attribution tasks based on visual feedback with temporal or spatial distortion of body movements reported inaccurate agency judgments in patients with schizophrenia; patients were shown to have a stronger tendency to attribute what they saw to their own agency, which is termed over-attribution of agency (Daprati et al., 1997, Franck et al., 2001, Synofzik et al., 2010). In these tasks, patients were shown a visual image corresponding to an action performed by the patient, for example, a video of a hand making a manual gesture (Daprati et al., 1997), or a computerized image of a hand holding a joy stick, that is, a realistic virtual hand (Franck et al., 2001). Explicit agency attribution for patients' body movement was evaluated by asking “Was it your own hand?” (Daprati et al., 1997) or “Did the movement you saw on the screen exactly correspond to the movement you made with your hand?” (Franck et al., 2001). A sense of agency has to be distinguished from a sense of ownership of body movement, which is the sense that one's own body is moving or is causing the movement (Gallagher, 2000, Tsakiris et al., 2007). However, these studies evaluated the mixture of a sense of agency and a sense of ownership of body movement instead of evaluating the sense of agency alone (Synofzik et al., 2008). This separation of the agency from the ownership is important because the sense of agency is more likely to deteriorate than the sense of ownership in patients with schizophrenia (Waters and Badcock, 2010). In the case of delusions of control, for example, patients experience that their bodies are moving, but that they do not have a sense of controlling the movement and they feel they are being controlled by external agents. Patients with schizophrenia should be examined by an unmixed and distinct sense of agency task. In the present study, we devised a new method to measure the sense of agency that was not contaminated by any aspect of the sense of body ownership.
In contrast to an explicit measure, an implicit measure of the sense of agency is evaluated by the “intentional binding” effect in subjective time experience during an intentional action (Haggard et al., 2002, Haggard, 2006). In this experiment, subjects pressed a key and their voluntary actions were followed 250 ms later by an auditory tone. The task was to judge the time at which they were aware of pressing a key and the time at which they were aware of hearing the tone (the Libet-clock method) (Libet et al., 1983). Even in healthy individuals, a temporal binding effect exists, where a voluntary action and a sensory consequence following that action temporally bind each other. Because no such temporal attraction or compression occurs for involuntary movements evoked by trans-cranial magnetic stimulation, this effect was called an “intentional binding” effect (Haggard et al., 2002). This temporal attraction enhances our experience of agency, and was regarded as an implicit measure of sense of agency. These binding effects were shown to be much stronger in patients with schizophrenia (Haggard et al., 2003, Voss et al., 2010), and the hyper-binding effect corresponded to an excessive sense of agency. Accordingly, patients with schizophrenia may experience their actions as having excessive causal effects on the external world. From a clinical standpoint, these phenomena may explain schizophrenic symptoms including delusions of reference, Schädigungswahn, or Omnipotenzerlebnis (Conrad, 1958), where patients have the strong tendency to “bind” external events to their actions and feel they cause all external phenomena around them. These delusions of reference are found even when external events precede intentional actions in patients with schizophrenia. Therefore, it is worthwhile to investigate whether excessive causal effects would be demonstrated even in conditions where external events precede their intentional actions, and thus we introduced those “event prior to action (EPA)” conditions in our experiment.
In this study, we devised an extremely simple task without any confounding from the sense of ownership of body movements, and compared findings between patients with schizophrenia and normal controls. Our experiment introduced temporal biases between actions and sensory consequences in visual feedback on the computer screen, and evaluated how much subjects explicitly felt a sense of control over external events. We supposed that an excessive sense of agency would be revealed even in our genuine agency-attribution task. Moreover, we expected that an enhanced sense of agency would also be found in “EPA” conditions where sensory consequences of actions were programmed to precede subjects’ intentional actions, indicating both forward and backward exaggerated causal efficacy in intentional actions and critical confusion of temporal causality in patients with schizophrenia.
Section snippets
Participants
We recruited 30 patients (21 males and 9 females) with schizophrenia from Sakuragaoka Memorial Hospital in a suburb of Tokyo. All patients had chronic paranoid-type schizophrenia and were clinically stable at the time of testing. The first author (TM) diagnosed all subjects according to the DSM-IV criteria. To clarify the clinical status of patients, we used the Positive and Negative Syndrome Scale (PANSS) (Kay, 2007) and the Global Assessment of Functioning (GAF) score.
Exclusion criteria
Action-linked condition
The mean number of yes responses decreased as the temporal bias increased in both groups. Compared with findings in normal subjects, the slope of the curve of agency judgment was completely different in patients with schizophrenia. The normal control group showed a sharp decrease, on the other hand, whereas the patient group showed a gentle decrease (Fig. 3 right). Patients with schizophrenia had a tendency to give more yes responses than control subjects, indicating that they showed
Discussion
We demonstrated that the sense of agency, which was not confounded by the sense of ownership, was disordered in patients with schizophrenia compared with normal controls. Patients with schizophrenia relatively showed an excessive sense of agency compared to healthy subjects, indicating that these patients over-associate their actions with subsequent events. Neuroleptics were not considered to affect agency judgment in our task. These findings are consistent with the results of previous explicit
Acknowledgments
This study was supported by a Grant-in-Aid for Scientific Research on Priority Areas “Emergence of Adaptive Motor Function through Interaction between Body, Brain and Environment (Area #454)” from the Japanese Ministry of Education, Culture, Sports, Science and Technology to MK.
The authors thank Dr. T Satoh, Dr. M Kashiwakura, Dr. H Kato and Dr. Y Taniguchi of Sakuragaoka Memorial Hospital for their assistance.
References (43)
- et al.
Distributed neural systems for temporal production: a functional MRI study
Brain Research Bulletin
(2003) - et al.
Abnormalities in the awareness of action
Trends in Cognitive Science
(2002) - et al.
Looking for the agent: an investigation into consciousness of action and self-consciousness in schizophrenic patients
Cognition
(1997) - et al.
Explaining the symptoms of schizophrenia: abnormalities in the awareness of action
Brain Research Reviews
(2000) Philosophical conceptions of the self: implications for cognitive science
Trends in Cognitive Science
(2000)- et al.
Beyond consciousness of external reality: a “who” system for consciousness of action and self-consciousness
Consciousness and Cognition
(1998) Conscious intention and motor cognition
Trends in Cognitive Science
(2005)- et al.
Altered sense of agency in schizophrenia and the putative psychotic prodrome
Psychiatry Research
(2011) - et al.
Sense of agency is altered in patients with a putative psychotic prodrome
Schizophrenia Resesarch
(2011) - et al.
Disorders of agency in schizophrenia correlate with an inability to compensate for the sensory consequences of actions
Current Biology
(2005)
Awareness of action: inference and prediction
Consciousness and Cognition
A disturbed sense of self in the psychosis prodrome: linking phenomenology and neurobiology
Neuroscience and Biobehavioral Reviews
Dysfunctional supplementary motor area implication during attention and time estimation tasks in schizophrenia: a PET-O15 water study
Neuroimage
Functional neural networks of time perception: challenge and opportunity for schizophrenia research
Schizophrenia Research
Phenomenology of anomalous self experience in early schizophrenia
Comprehensive Psychiatry
Beyond the comparator model: a multifactorial two step account of agency
Consciousness and Cognition
Me or not me — an optimal integration of agency cues?
Consciousness and Cognition
On agency and body-ownership: phenomenological and neurocognitive reflections
Consciousness and Cognition
Relations between the central nervous system and peripheral organs
The British Journal of Animal Behaviour
The perception of self-produced sensory stimuli in patients with auditory hallucinations and passivity experiences : evidence for a breakdown in self-monitoring
Psychological Medicine
What makes us tick? Functional and neural mechanisms of interval timing
Nature Reviews Neuroscience
Cited by (68)
Aberrant heartbeat-evoked potential in schizophrenia
2024, Progress in Neuro-Psychopharmacology and Biological PsychiatryMetacognition and sense of agency
2023, CognitionPredictive waves in the autism-schizophrenia continuum: A novel biobehavioral model
2022, Neuroscience and Biobehavioral ReviewsVocalizing and singing reveal complex patterns of corollary discharge function in schizophrenia
2021, International Journal of Psychophysiology