Altered action awareness in schizophrenia patients with passivity experiences and auditory hallucinations

Abstract

The deficit in motor self-monitoring is suggested to explain the passivity experiences and even auditory verbal hallucinations (AVH). It is proposed that the loss of the sense of agency in these strange experiences originates from abnormalities in the motor control system. When executing an action, the central nervous system sends out the corresponding motor commands for suitable muscular contractions. An efference copy (EC) (a copy of the motor command) will be made, for computing a prediction of motor consequences. Discrepancies between the predicted state and the actual state imply alien interruption, generating possibly the judgments about alien agency's control over the movement. An abnormal occurrence of this discrepancy is thought to be underlying the passivity experiences or even AVH.

Ample evidences have shown that schizophrenia patients performed worse in motor related tasks that requires access to the EC and the predicted state. Patients with passivity experiences or AVH (patients with relevant symptoms) demonstrated even greater anomaly than those without. However, most of the tasks adopted involved complex cognitive processes or required verbal report of experiences. Patients with passivity experiences have poor general cognitive functions and may have an eccentric criterion in making judgment, thus affecting the tasks’ validities.

The current study proposes two paradigms that tried to investigate the abnormalities of EC and predicted state in the motor control system of the patients with relevant symptoms. The two paradigms aimed to measure the direct influences of EC and predicted state in motor performances and are designed to eliminate as much cognitive processes involvement as possible.

In both paradigms, three groups were recruited: (a) schizophrenia patients with clinically significant AVH or passivity experiences; (b) schizophrenia patients without the relevant symptoms and (c) normal controls. Both paradigms focused on the influences of the EC and predicted state of one action on another separate action. The first paradigm focused on the influence of them on a subsequent action and the second paradigm focused on the influence of them on a simultaneous action. The first paradigm required subjects to replicating their previous voluntary movement, which should be more accurate than when replicating a passive movement. The second paradigm required subjects to unload an object on one hand with the other hand. This voluntary action should stabilize the loaded hand when unloading objects comparing to passive unloading, due to an anticipation of movements.

In both paradigms, the performances of the patients with relevant symptoms significantly deviated from the control groups. In the first paradigm, the patients with relevant symptoms replicate their action much worse than controls; in the second paradigm, the patients with relevant symptoms have their hands fluctuated significantly stronger. Unlike the patients with relevant symptoms, both the control groups demonstrated utilization of EC and the predicted states.

The findings strongly suggest that deficit in motor self-monitoring in the predictors process associated strong with passivity experiences and AVH. The link between motor performances and the experience of AH should be highlighted.