Does Vestibular Motion Perception Correlate with Axonal Pathways Stimulated by Subthalamic Deep Brain Stimulation in Parkinson’s Disease?

• Published in: Cerebellum (London, England) Vol. 23; no. 2; pp. 554 - 569
• Main Authors: Beylergil, Sinem Balta, Noecker, Angela M., Kilbane, Camilla, McIntyre, Cameron C., Shaikh, Aasef G.
• Format: Journal Article
• Language: English
• Published: New York Springer US 01.04.2024; Springer Nature B.V
• Subjects: Basal ganglia; Biomedical and Life Sciences; Biomedicine; Cerebellum; Correlation analysis; Deep brain stimulation; Deep Brain Stimulation - methods; Electrical stimuli; Hemispheric laterality; Humans; Information processing; Locomotion; Motion detection; Motion Perception; Movement disorders; Neurobiology; Neurodegenerative diseases; Neurology; Neurosciences; Parkinson Disease - therapy; Parkinson's disease; Perception; Pontine nuclei; Solitary tract nucleus; Substantia alba; Subthalamic nucleus; Subthalamic Nucleus - physiology; Thalamus; Vestibular system; Parkinsonism; Cerebellum; Motion-perception; Basal ganglia; Neurodegeneration; Movement disorders
• ISSN: 1473-4230; 1473-4222; 1473-4230
• DOI: 10.1007/s12311-023-01576-8

Perception of our linear motion — heading — is critical for postural control, gait, and locomotion, and it is impaired in Parkinson’s disease (PD). Deep brain stimulation (DBS) has variable effects on vestibular heading perception, depending on the location of the electrodes within the subthalamic nucleus (STN). Here, we aimed to find the anatomical correlates of heading perception in PD. Fourteen PD participants with bilateral STN DBS performed a two-alternative forced-choice discrimination task where a motion platform delivered translational forward movements with a heading angle varying between 0 and 30° to the left or to the right with respect to the straight-ahead direction. Using psychometric curves, we derived the heading discrimination threshold angle of each patient from the response data. We created patient-specific DBS models and calculated the percentages of stimulated axonal pathways that are anatomically adjacent to the STN and known to play a major role in vestibular information processing. We performed correlation analyses to investigate the extent of these white matter tracts’ involvement in heading perception. Significant positive correlations were identified between improved heading discrimination for rightward heading and the percentage of activated streamlines of the contralateral hyperdirect, pallido-subthalamic, and subthalamo-pallidal pathways. The hyperdirect pathways are thought to provide top-down control over STN connections to the cerebellum. In addition, STN may also antidromically activate collaterals of hyperdirect pathway that projects to the precerebellar pontine nuclei. In select cases, there was strong activation of the cerebello-thalamic projections, but it was not consistently present in all participants. Large volumetric overlap between the volume of tissue activation and the STN in the left hemisphere positively impacted rightward heading perception. Altogether, the results suggest heavy involvement of basal ganglia cerebellar network in STN-induced modulation of vestibular heading perception in PD.