Dorsal visual stream is preferentially engaged during externally guided action selection in Parkinson Disease

Abstract

Objective: In patients with Parkinson Disease (PD), self-initiated or internally cued (IC) actions are thought to be compromised by the disease process, as exemplified by impairments in action initiation. In contrast, externally-cued (EC) actions which are made in response to sensory prompts can restore a remarkable degree of movement capability in PD, particularly alleviating freezing-of-gait. This study investigates the electrophysiological underpinnings of movement facilitation in PD through visuospatial cuing, with particular attention to the dynamics within the posterior parietal cortex (PPC) and lateral premotor cortex (LPMC) axis of the dorsal visual stream.

Methods: Invasive cortical recordings over the PPC and LPMC were obtained during deep brain stimulation lead implantation surgery. Thirteen PD subjects performed an action selection task, which was constituted by left or right joystick movement with directional visual cuing in the EC condition and internally generated direction selection in the IC condition. Time-resolved neural activities within and between the PPC and LPMC were compared between EC and IC conditions.

Results: Reaction times (RT) were significantly faster in the EC condition relative to the IC condition (paired t-test, p = 0.0015). PPC-LPMC inter-site phase synchrony within the β-band (13-35 Hz) was significantly greater in the EC relative to the IC condition. Greater PPC-LPMC β debiased phase lag index (dwPLI) prior to movement onset was correlated with faster reaction times only in the EC condition. Multivariate granger causality (GC) was greater in the EC condition relative to the IC condition, prior to and during movement.

Conclusion: Relative to IC actions, we report relative increase in inter-site phase synchrony and directional PPC to LPMC connectivity in the β-band during preparation and execution of EC actions. Furthermore, increased strength of connectivity is predictive of faster RT, which are pathologically slow in PD patients. Stronger engagement of the PPC-LPMC cortical network by an EC specifically through the channel of β-modulation is implicated in correcting the pathological slowing of action initiation seen in Parkinson's patients.

Significance: These findings shed light on the electrophysiological mechanisms that underlie motor facilitation in PD patients through visuospatial cuing.

Keywords: Action selection; Choice task; Dorsal visual stream; Electrocorticography; Posterior parietal cortex; Premotor cortex.