Increased beta synchronization underlies perception-action hyperbinding in functional movement disorders

Brain Commun. 2024 Oct 9;6(5):fcae301. doi: 10.1093/braincomms/fcae301. eCollection 2024.

Abstract

Functional movement disorders are amongst the most common and disabling neurological conditions, placing a significant burden on the healthcare system. Despite the frequency and importance of functional movement disorders, our understanding of the underlying pathophysiology is limited, hindering the development of causal treatment options. Traditionally, functional movement disorders were considered as a psychiatric condition, associated with involuntary movements triggered by psychological stressors. Recent neurophysiological studies have unveiled cognitive alterations in affected individuals, suggesting that functional movement disorders might be better characterized by overarching neural principles governing cognitive functions. For instance, recent research has shown that the retrieval of stimulus-response bindings is altered in patients with functional movement disorders. Building upon these recent findings, our study delves into whether the initial integration of stimulus and response information is also disrupted in patients with functional movement disorders. To accomplish this, we reanalysed previously collected EEG data using refined analysis methods that provide insights into oscillatory activity and functional neuroanatomy associated with the integration of stimulus-response bindings. Our results demonstrate that post-movement beta synchronization (i) predicts behavioural stimulus-response binding and (ii) is significantly increased in patients with functional movement disorders compared to healthy controls. Utilizing beamformer analysis, we localized the difference effect to a cluster centred around the left supplementary motor area and the correlation effect to the right supplementary motor area. Extending beyond recent research that focused on the retrieval of stimulus-response bindings, our present findings reveal that the integration of stimulus and response information is already impaired in patients with functional movement disorders. These results uncover a phenomenon of hyperbinding between perception and action, which may represent a fundamental mechanism contributing to the movement impairments in patients with functional movement disorders.

Keywords: binding and retrieval in action control; functional movement disorder; perception-action integration; post-movement beta oscillations; theory of event coding.