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

Abstract

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.

Coordination between upper- and lower-limb movements is different during overground and treadmill walking

“…The latter parameter was computed as the time delay between the positive peak of arm angle (maximum forward inclination) and the negative peak of the ipsilateral thigh angle (maximum backward inclination), identified between 20 and 80% of the stride cycle. When the upper limb produced two oscillations per stride at low walking speeds, point estimates of relative phase were computed using the first positive peak of arm oscillation and the negative peak of the ipsilateral thigh angle (Crenna et al 2008;Ford et al 2007).…”

Dopaminergic Modulation of Arm Swing During Gait Among Parkinson's Disease Patients

“…Related research has highlighted upper-limb gait asymmetry and coordination deficits as a common and relatively early feature of PD [10–12]. Biomechanically, several lines of evidence suggest that impaired arm swing may arise from wrongly timed activation of the shoulder flexors or extensors [13], axial rigidity [14, 15], and/or loss of trunk rotation during ambulation [16–18]. The relationship between dopamine deficits and these upper-limb gait changes in PD, however, remain unknown.…”

“…First, using [ 123 I] N-ω-fluoropropyl-2β-carbomethoxy-3β-(4-iodophenyl)-tropane (FP-CIT) and single-photon computed tomography, Isaias et al [19] reported that asymmetric dopaminergic terminal labeling in the striatum correlates strongly with upper-limb gait asymmetry in PD subjects. Second, combined dopaminergic medication and bilateral subthalamic nucleus (STN) stimulation have been shown to ameliorate reduced walking arm swing amplitude among PD patients [16, 17]. …”

A data mining methodology for predicting early stage Parkinson's disease using non-invasive, high-dimensional gait sensor data

“…While the current study was limited by sample size, our results are in agreement with previous characterizations of gait impairment in early PD. Specifically, several studies have suggested that gait impairment in early PD may involve reduced swing of the upper limbs during ambulation (Huang et al 2012; Lewek et al 2010; Isaias et al 2012; Crenna et al 2008; Carpinella et al 2007; Roggendorf et al 2012). Moreover, the agreement of our results with previous studies supports the notion that whole-body data mining techniques may be used to reveal novel markers of gait dysfunction.…”