Predictive neural processing of self-generated hand and tool actions in patients with schizophrenia spectrum disorders and healthy individuals.

Abstract

Schizophrenia spectrum disorders (SSD) have been linked to dysfunctions in the predictive neural suppression of sensory input elicited by one's own actions. Such motor predictions become particularly challenging during tool use and when feedback from multiple sensory modalities is present. In this study, we investigated the neural correlates and potential dysfunctions of action feedback processing in SSD during tool use actions and bimodal sensory feedback presentation. Patients with SSD (N_Total = 42; schizophrenia N_F20 = 34; schizoaffective disorder N_F25 = 6; other N = 2) and healthy controls (HC, N = 27) performed active or passive hand movements with or without a tool and received unimodal (visual; a video of their hand movement) or bimodal (visual and auditory) feedback with various delays (0, 83, 167, 250, 333, 417 ms). Subjects reported whether they detected a delay. A subgroup (N_SSD = 20; N_HC = 20) participated in an identical fMRI experiment. Both groups reported fewer delays in active than passive conditions and exhibited neural suppression in all conditions in occipital and temporoparietal regions, cerebellum, and SMA. Group differences emerged in right cuneus, calcarine, and middle occipital gyrus, with reduced active-passive differences in patients during tool use actions and in bimodal trials during actions performed without a tool. These results demonstrate for the first time that, although patients and HC show similarities in neural suppression, higher-level visual processing areas fail to adequately distinguish between self- and externally generated sensory input in patients, particularly in complex action feedback scenarios involving bimodal action feedback and feedback elicited by tool use actions.