Explicit Agency in Patients with Cervical Dystonia: Altered Recognition of Temporal Discrepancies between Motor Actions and Their Feedback

Abstract

BackgroundAbnormalities in the cognitive processing of movement have been demonstrated in patients with dystonia. The sense of agency, which is the experience of initiating and controlling one’s own actions, has never before been studied in these patients.ObjectivesWe investigated whether the sense of agency is altered in patients with cervical dystonia.MethodsWe used an explicit metacognitive agency task in which participants had to catch targets with a cursor by moving a computer’s mouse. The task included several conditions in which the control over the cursor could be disrupted by adding a spatial or a temporal discrepancy between the mouse and the cursor’s movements. Participants had to acknowledge these discrepancies and reflect them in metacognitive judgements of agency.ResultsTwenty cervical dystonia patients and 20 matched controls were included in the study. Despite performing equally well as the matched controls, cervical dystonia patients did not fully recognize alterations of agency when a temporal lag was added between their movement and the visual feedback. Moreover, they relied predominantly on their perceived performance to provide judgements of agency and less on their objective degree of controls. There was no correlation between agency scores and clinical severity of dystonia measured by the Toronto Western Spasmodic Torticollis Rating Scale.ConclusionWe demonstrated an abnormal processing of agency in cervical dystonia patients, even for motor actions not affected by dystonia. The exact contribution of abnormal agency to dystonia pathophysiology remains to be clarified.

New measures of agency from an adaptive sensorimotor task

“…Self-agency refers to the feeling that one is the cause of their behaviors [1]. Impairments in self-agency have been observed in multiple psychological and neurological disorders, such as functional movement disorders (FMDs) [2], Parkinson’s disease [3], alien hand syndrome [4], schizophrenia [5], and dystonia [6]. However, existing measurements of agency are rarely applied in diagnosis due to concerns of unreliability [7-9].…”

Reduced Global-Brain Functional Connectivity and Its Relationship With Symptomatic Severity in Cervical Dystonia

“…GFC values in these areas could correctly identify patients from healthy controls with good sensitivity, specificity, and accuracy. Previous studies indicate that dystonia is a disorder of motor organization, programming, execution, and sensorimotor integration (36). The precentral gyrus (as the M1), located between the central sulcus and anterior central sulcus on the dorsolateral side of the frontal lobe, is closely related to motor preparation and execution.…”

Motor sequence awareness is impaired in dystonia despite normal performance

“…Reduced awareness of the motor response in dystonia may be related to abnormal proprioception. 8 Abnormal proprioception can manifest as abnormalities in a sense of agency (i.e., awareness of initiating and controlling movements), 4 tactile discrimination, 24–27 impaired cognition of hand movements, 28,29 and enlargement and overlap or cortical receptive fields. 26 Proprioception plays an important role in motor learning and sequence performance.…”

“…Dystonia is associated with a reduced sense of agency, meaning that people with dystonia are not always aware that they are controlling their own movements. 4 This is likely related to the well-described impairment in sensorimotor integration, 5,6 with specific deficits in spatial and temporal discrimination 7 or proprioception. 8 There is evidence that performance monitoring is abnormal in dystonia.…”