Brain Dynamics of Action Monitoring in Higher-Order Motor Control Disorders: The Case of Apraxia

Limb apraxia (LA) refers to a high-order motor disorder characterized by the inability to reproduce transitive actions on commands or after observation. Studies demonstrate that action observation and action execution activate the same networks in the human brain, and provides an onlooker’s motor system with appropriate cognitive, motor and sensory-motor cues to flexibly implementing action-sequences and gestures. Tellingly, the temporal dynamics of action monitoring has never been explored in people suffering from LA. To fill this gap, we studied the electro-cortical signatures of error observation in human participants suffering from acquired left-brain lesions with (LA+) and without (LA–) LA, and in a group of healthy controls (H). EEG was acquired while participants observed from a first-person perspective (1PP) an avatar performing correct or incorrect reach-to-grasp a glass action in an immersive-virtual environment. Alterations of typical EEG signatures of error observation in time (early error positivity; Pe) and time-frequency domain (theta band-power) were found reduced in LA+ compared with H. Connectivity analyses showed that LA+ exhibited a decreased theta phase synchronization of both the frontoparietal and frontofrontal network, compared with H and LA–. Moreover, linear regression analysis revealed that the severity of LA [test of upper LA (TULIA) scores] was predicted by mid-frontal error-related theta activity, suggesting a link between error monitoring capacity and apraxic phenotypes. These results provide novel neurophysiological evidence of altered neurophysiological dynamics of action monitoring in individuals with LA and shed light on the performance monitoring changes occurring in this disorder.