Brain Advance Access published online on October 24, 2008
Brain, doi:10.1093/brain/awn272
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Influence of basal ganglia on upper limb locomotor synergies. Evidence from deep brain stimulation and L-DOPA treatment in Parkinson's disease
1Institute of Human Physiology I, L.A.M.B. Pierfranco & Luisa Mariani, University of Milan, 2Polo Tecnologico, Fond. Don Carlo Gnocchi ONLUS, IRCCS, Milan, 3Department of Neuroscience, University of Turin, Turin and 4Department of Neuroscience, Ospedale Niguarda Ca’ Granda, Milan, Italy
Correspondence to:
Paolo Crenna, MD, Institute of Human Physiology I, University of Milan, via Mangiagalli32 I-20133, Milan, Italy E-mail: paolo.crenna{at}unimi.it
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.
Key Words: arm swing; subthalamic nucleus; deep brain stimulation; Parkinson's disease; walking
Abbreviations: DBS, deep brain stimulation; ROM, range of motion; STN, subthalamic nucleus
Received April 15, 2008. Revised September 18, 2008. Accepted September 22, 2008.