This study is in favour of the existence of an abnormal sense of agency early in the psychotic illness. Because it is quick and none verbal, motor agency may be a valuable tool to use in complement to classic interviews, especially when investigating complex ineffable experiences that are difficult to explicitly describe.

As reported in the literature for adult controls, healthy adolescents used more efficient force levels in self than in other-imposed collisions. For both UHR and FEP patients, abnormally high levels of grip force were used for self-produced collisions, leading to an absence of difference between self and other. The normalized results revealed that motor agency differentiated patients from controls with a higher level of sensitivity than the more classic neuropsychological test battery.

Thirty-two young symptomatic patients and their age-matched controls participated in the study. 15 of these patients were at ultra high-risk for developing psychosis (UHR), and 17 patients were suffering from first-episode psychosis (FEP). Patients' neurocognitive capacities were assessed through the use of seven neuropsychological tests. A motor agency task was also introduced to obtain an objective indicator of the degree of sense of agency, by contrasting force levels applied during other and self-produced collisions between a hand-held objet and a pendulum.

Early diagnosis of young adults at risk of schizophrenia is essential for preventive approaches of the illness. Nevertheless, classic screening instruments are difficult to use because of the non-specific nature of the signs at this pre-onset phase of illness. The objective of the present contribution was to propose an innovating test that can probe the more specific symptom of psychosis, i.e., the sense of agency, which is defined as being the immediate experience of oneself as the cause of an action. More specifically, we tested whether motor agency is abnormal in early psychosis.

Introduction

Psychosis describes a mental state characterized by distortion or loss of contact with reality and may involve severe disturbances in cognition, behaviour, and emotion. It can be associated to different types of symptoms, one of which may be the positive symptoms that include delusions, hallucinations and thought disorders. Most individuals with schizophrenia, which is the most common of psychosis, experience onset during late adolescence or early adulthood. This initial episode of psychotic disorders can thus be particularly traumatic both for the individuals and their family as it occurs during the key moment in life for the development of identity, relationships and long-term vocational plans. Hence, a particular interest has emerged for the early phase of schizophrenia, including the pre-onset of the illness, i.e., the prodromal period. This is particularly true as more and more evidence show that early clinical intervention, i.e., when the disorder is not yet entrenched, may improve the longer-term outcome of patient [1], [2] and even reduce the duration of untreated psychoses [3].

However, how to provide adequate care to those young adolescences at clinical risk of developing psychosis (Ultra High Risk individuals) remains an unanswered question. This is especially true, as the detection of the emergence of psychosis is rendered difficult by the non-specificity of the prodromal signs and symptoms [4]. The objective of the present contribution was to propose an innovating motor test that might probe the more specific symptom of psychosis, i.e., the sense of agency. This highly sensitive measure could then in a midterm improve the predictive validity of early diagnosis.

Today, the most widely used screening tool for identifying individuals suffering from attenuated psychotic symptoms and thus, at imminent risk for onset of a psychotic disorder is the Comprehensive Assessment of At Risk Mental State (CAARMS) scale [5], [6], [7]. This instrument is based on a “close-in” strategy that combines different risk factors including, e.g., the peak age range for onset of psychotic disorder, the presence of subthreshold psychotic symptoms and signs, family history of psychotic disorders and functional decline [8], [9]. This semi-structured interview provides the means to specify whether an individual meets the Ultra High Risk (UHR) criteria. However, despite the promising identification results obtained with the CAARMS, a recent study investigating the predictive validity of the UHR criteria reported a much lower transition rate (16%) [10] than that reported in the initial cohorts (greater than 40% - for a review see Haroun et al. [11]). More specifically, it was demonstrated that a greater number of “false positive” cases were identified. This may be due to the fact that the questions in the CAARMS do not target the subtle and infraliminary signs that characterise the prodromal phase of psychosis such as basic anomalies in the bodily experiences of self.

Phenomenological studies have argued that the basic sense of self may be one of the earliest and most fundamental features of the abnormal self-disturbance experiences reported in patients suffering from psychosis [12], [13], [14], [15]. This abnormal sense of self would include: (a) a diminished sense of the minimal self, with an inner void and a lack of identity; (b) a distorted first-person perspective, with a pervasive and fluctuating limit between self and the outer-world; (c) an abnormally intensified reflectivity with a circular repetition of thoughts. In UHR individuals, these alterations of the sense of self are rarely of pathological intensity, and it is only during the psychotic transition that they become thematised within the emerging positive symptoms, such as delusions of control and hallucinations. As a consequence, it is difficult to quantify these disturbances at the early stage of the disease, and more particularly through a verbal interview such as the CAARMS, since (1) self- disturbances are so strange, that young patients hesitate to express them, and (2) even in the situations for which patients do try to describe their state, the phenomena are so ineffable that they find themselves short of words.

Explicit reports from patients have described an abnormal sense of self as leading to an artificial distance between the body that is moving, and the experience of being. This alienated self-experience would be expressed through thoughts as well as actions leading to abnormal sense of agency. In this way, it has been proposed that one of the most basic components of the sense of self may be the sense of agency, which has recently been defined by Gallagher [16] as being the immediate experience of oneself as the cause of an action.

Based on the empirical evidence that self-disturbances may be a core feature of schizophrenia and present during the prodromal phase of schizophrenia [15], we have developed the use of a motor agency task [17], [18], [19] to probe the degree of self-disturbances in individuals at clinical risk of developing schizophrenia (UHR individuals). Indeed, we have proposed the use of the collision paradigm [20] because it requires neither reflective responses nor explicit judgments. It provides the means to reveal behaviourally a difference in experiential states between a situation for which the participant is an active agent of the initiation of a collision, and the contrasting situation for which the same participant is passively experiencing collisions that are initiated by someone else. The term “collision” is used because concretely, the subjects' task is to use a hand-held object to resist impacts that are produced as a consequence of the collision between the hand-held object and a pendulum (see Figure 1). The degree of agency is investigated by contrasting two conditions. In the first, the pendulum is released by the experimenter (other-released, task O). In the second, the pendulum is released by the participants themselves (self-released, task S). As described in previous studies, a distorted sense of agency is associated to a low-degree of agency, i.e., similar levels of grip force efficiency are applied on the hand-held object when the pendulum is self released (task S) and when the pendulum release is triggered by someone else (task O). Conversely, a preserved sense of agency is characterised by a significant difference in grip force efficiency between task S and task O.

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larger image TIFF original image Download: Figure 1. Motor agency task. Illustration of the collision paradigm that was used to estimate the degree of sense of agency experienced by each individual for two different types of events. LEFT: other-triggered collisions with a pendulum that was released by the experimenter; RIGHT: self-produced collisions with a pendulum that was released by the participants. Under both conditions, the subjects were required to remain the hand-held objet immobile and to stop the fall of the pendulum. https://doi.org/10.1371/journal.pone.0030449.g001

The originality of this paradigm is to explore the contribution of the pure efferent-based mechanisms by measuring grip force levels at the specific time of impact. Because the duration of the impacts is very short (<30 ms), feedback mechanisms that take a minimum of 90 ms to intervene do not have the time to implement a functional change in grip force adjustments. Thus, we propose that our measure provides the means to probe the participants' immediate experience of being agent or not of that event, without contamination from higher-order cognitive functions mediated through afferent and reflective feedback loops.

Through the use of the collision paradigm, the aim here was first to see whether the sense of agency was indeed perturbed as early as the prodromal phase of psychosis, and to compare these results to those observed in first episode young patients. The second objective was to measure basic motor performances and neurocognitive functions to confirm the none-specificity of general cognitive deficits that are at a sub-pathological intensity. Finally, we aimed at revealing that because it targets the core symptom of psychosis, the motor agency tool is more sensitive than the general neuropsychological battery to detect the emergence of prodromal symptoms.