Neuronal Responses to Passive Movement in the Globus Pallidus Internus in Primary Dystonia

Abstract

Abnormal sensory processing has been implicated in the pathophysiology of primary dystonia. In the globus pallidus internus (GPi), the primary output structure of the basal ganglia, many neurons respond to sensory (proprioceptive) stimulation. Here we have characterized GPi neuronal responses to passive movement of the contralateral limbs in 22 patients with primary dystonia undergoing microelectrode recording for placement of deep brain stimulator leads. We plotted coordinates of cells responding to limb movement in a common space. We observed distinct representations of leg and arm movement localized to the dorsal and ventral part of the posterior GPi, respectively. Comparing patients with generalized dystonia versus patients with segmental craniocervical dystonia, there was no difference in the volumes or separations of leg and arm related territories. In contrast to parkinsonism, only a small minority of units were responsive to movement across multiple joints. Abnormally increased directional selectivity was found in units responding to dystonic limbs compared with nondystonic limbs. Some affected GPi neurons therefore appear to have altered proprioceptive tuning for movement direction. There is an apparent preservation of GPi somatotopic organization in dystonia in comparison with prior studies of GPi somatotopic organization in non-human primates and humans with Parkinson's disease.

Pathological basal ganglia activity in movement disorders

“…For instance, altered sensorimotor maps similar to those in cortex, have been identified in the putamen (Delmaire et al, 2005) and thalamic levels (Lenz and Byl, 1999, Lenz et al, 1999). However, such changes were not seen in recent GPi recording studies (Chang et al, 2007, Tang et al, 2007). …”

Pallidal neuronal discharge in Parkinson's disease following intraputamenal fetal mesencephalic allograft

“…Here, in a small number of neurons, we show a consistent pattern of movement-related profound phasic inhibition of pallidal outflow that is not seen in the non-transplanted off-medication or on-medication parkinsonian states. The inhibition was non-topographic, in the sense that it was present in neurons recorded in different subregions of GPi, unlikely to correspond to a normal hand-related area 36. This observation suggests that the striatal allograft ‘overcorrects’ the parkinsonian imbalance in the ratio of inhibited to activated cells.…”

Sensory aspects of movement disorders

“…33–35 Poor recognition of limb displacement has been noted during testing of passive motion in patients with Parkinson’s disease. 36,37 Other kinaesthetic abnormalities include impaired detection of applied force and weight required for single-joint displacement.…”