Effects of subthalamic nucleus DBS on haptic perception and sensorimotor control in Parkinson's disease

Abstract

Parkinson’s disease (PD) is a neurodegenerative disease that affects the basal ganglia-thalamocortical pathway resulting in a progressive decline in motor function. An established treatment for the motor symptoms of PD is deep brain stimulation (DBS) of the subthalamic nucleus (STN). Mounting evidence suggests that PD is also associated with somatosensory deficits, specifically a loss of kinaesthetic and haptic precision, yet the effect of STN-DBS on sensory processing is largely unknown. Thus, this study investigated whether STN-DBS affects somatosensory processing by systematically examining the precision of haptic perception of object size. Without vision, 11 PD patients with implanted STN-DBS and 9 healthy controls haptically explored the heights of two successively presented three-dimensional blocks using a precision grip. In each trial, a 6cm reference block was judged against a comparison block (heights: 5.2-6.8 cm). Participants verbally indicated which block was taller (perceptual judgment). While still grasping the comparison block, they then matched its perceived size by opening the non-probing hand accordingly (motor judgment). Patients were tested during ON and OFF stimulation, following a 12-hour medication wash-out period. Based on their verbal responses haptic discrimination thresholds (DT) at the 75% correct response level and areas of uncertainty were derived. Based on the hand kinematic data collected by a motion capture system, a grip aperture error (difference between grip aperture and actual block height) was calculated. The main results were: First, with their stimulators OFF, PD patients showed deficits in both perceptual and motor judgments compared to controls as measured by increased DT and aperture errors. When PD patients used their more affected hand to probe the block, DT was elevated by 233% (PD: 0.37 cm; controls: 0.11 cm) and mean aperture error increased by 97% (PD: 1.48 cm; controls: 0.75 cm). Second, DBS improved the precision of both perceptual and motor judgments. In the ON state, DT of the more affected hand decreased by 30% with respect to OFF state, while aperture error decreased by 15%. Third, probing with the motorically more affected hand resulted in less precise perceptual and motor judgments than probing with the less affected hand. This study offers first evidence that STN-DBS improves haptic precision. Results of this study speak to the notion that deficits seen in PD are not simply motor based, but rather a function of deficits in proprioceptive processing. We conclude that DBS-related improvements in movement accuracy are not explained by improvements in motor function alone, but rather by improved somatosensory processing.