Dysfunction of the basal ganglia, but not the cerebellum, impairs kinaesthesia

Precise knowledge about limb position and orientation is essential for the ability of the nervous system to plan and control voluntary movement. While it is well established that proprioceptive signals from peripheral receptors are necessary for sensing limb position and motion, it is less clear which supraspinal structures mediate the signals that ultimately lead to the conscious awareness of limb position (kinaesthesia). Recent functional imaging studies have revealed that the cerebellum, but not the basal ganglia, are involved in sensory processing of proprioceptive information induced by passive and active movements. Yet psychophysical studies have suggested a prominent role of the basal ganglia in kinaesthesia. This study addresses this apparent dichotomy by investigating the contributions of the cerebellum and the basal ganglia to the perception of limb position. Using a passive movement task, we examined the elbow position sense in patients with a dysfunction of the basal ganglia (Parkinson's disease, n=9), patients with cerebellar degeneration [spinocerebellar ataxia (SCA) types 6 and 8, n=6] and age-matched healthy control subjects (n=11). In comparison with healthy control subjects, Parkinson's disease patients, but not SCA patients, were significantly impaired in the ability to detect displacements correctly. A 1degrees forearm displacement was correctly recognized in >75% of trials by control subjects and SCA patients, but only in 55% of Parkinson's disease patients. Only at 6degrees displacement did Parkinson's disease patients exhibit a response rate similar to those of the two other groups. Thresholds for 75% correct responses were 1.03degrees for controls, 1.15degrees for cerebellar patients and 2.10degrees for Parkinson's disease patients. This kinaesthetic impairment significantly correlated with the severity of disease in Parkinson's disease patients, as determined by the Unified Parkinson's Disease Rating Scale (r=-0.7, P=0.03) and duration of disease (r=-0.7, P=0.05). In contrast, there was no significant correlation between performance and the daily levodopa equivalent dose. These results imply that an intact cerebro-basal ganglia loop is essential for awareness of limb position and suggest a selective role of the basal ganglia but not the cerebellum in kinaesthesia.