Influence of basal ganglia on upper limb locomotor synergies. Evidence from deep brain stimulation and l-DOPA treatment in Parkinson's disease

• Published in: Brain (London, England : 1878) Vol. 131; no. 12; pp. 3410 - 3420
• Main Authors: Crenna, P., Carpinella, I., Lopiano, L., Marzegan, A., Rabuffetti, M., Rizzone, M., Lanotte, M., Ferrarin, M.
• Format: Journal Article
• Language: English
• Published: Oxford Oxford University Press 01.12.2008; Oxford Publishing Limited (England)
• Subjects: Aged; Arm - physiopathology; arm swing; Basal Ganglia - drug effects; Basal Ganglia - physiopathology; Biological and medical sciences; Combined Modality Therapy; Deep Brain Stimulation; Degenerative and inherited degenerative diseases of the nervous system. Leukodystrophies. Prion diseases; Exercise Test - methods; Gait Disorders, Neurologic - drug therapy; Gait Disorders, Neurologic - etiology; Gait Disorders, Neurologic - physiopathology; Humans; Levodopa - therapeutic use; Medical sciences; Middle Aged; Neurology; Parkinson Disease - complications; Parkinson Disease - physiopathology; Parkinson Disease - therapy; Parkinson's disease; Primates; Psychomotor Performance; subthalamic nucleus; Thigh - physiopathology; walking; arm swing; Parkinson's disease; subthalamic nucleus; walking; deep brain stimulation; Nervous system diseases; Deep brain stimulation; Central nervous system; Parkinson disease; Basal ganglion; Encephalon; Cerebral disorder; Locomotion; Walking; Treatment; Central nervous system disease; Degenerative disease; Upper limb; Subthalamic nucleus; Levodopa; Extrapyramidal syndrome
• ISSN: 0006-8950; 1460-2156
• DOI: 10.1093/brain/awn272

Clinical evidence of impaired arm swing while walking in patients with Parkinson's disease suggests that basal ganglia and related systems play an important part in the control of upper limb locomotor automatism. To gain more information on this supraspinal influence, we measured arm and thigh kinematics during walking in 10 Parkinson's disease patients, under four conditions: (i) baseline (no treatment), (ii) therapeutic stimulation of the subthalamic nucleus (STN), (iii) l-DOPA medication and (iv) combined STN stimulation and l-DOPA. Ten age-matched controls provided reference data. Under baseline conditions the range of patients’ arm motion was severely restricted, with no correlation with the excursion of the thigh. In addition, the arm swing was abnormally coupled in time with oscillation of the ipsilateral thigh. STN stimulation significantly increased the gait speed and improved the spatio-temporal parameters of arm and thigh motion. The kinematic changes as a function of gait speed changes, however, were significantly smaller for the upper than the lower limb, in contrast to healthy controls. Arm motion was also less responsive after l-DOPA. Simultaneous deep brain stimulation and l-DOPA had additive effects on thigh motion, but not on arm motion and arm–thigh coupling. The evidence that locomotor automatisms of the upper and lower limbs display uncorrelated impairment upon dysfunction of the basal ganglia, as well as different susceptibility to electrophysiological and pharmacological interventions, points to the presence of heterogeneously distributed, possibly partially independent, supraspinal control channels, whereby STN and dopaminergic systems have relatively weaker influence on the executive structures involved in the arm swing and preferential action on those for lower limb movements. These findings might be considered in the light of phylogenetic changes in supraspinal control of limb motion related to primate bipedalism.