Proprioceptive Modulation of Pallidal Physiology in Cervical Dystonia

Abstract

BackgroundThere is a growing body of evidence suggesting that botulinum toxin can alter proprioceptive feedback and modulate the muscle‐spindle output for the treatment of dystonia. However, the mechanism for this modulation remains unclear.MethodsWe conducted a study involving 17 patients with cervical dystonia (CD), seven of whom had prominent CD and 10 with generalized dystonia (GD) along with CD. We investigated the effects of neck vibration, a form of proprioceptive modulation, on spontaneous single‐neuron responses and local field potentials (LFPs) recorded from the globus pallidum externus (GPe) and internus (GPi).ResultsOur findings demonstrated that neck vibration notably increased the regularity of neck‐sensitive GPi neurons in focal CD patients. Additionally, in patients with GD and CD, the vibration enhanced the firing regularity of non‐neck‐sensitive neurons. These effects on single‐unit activity were also mirrored in ensemble responses measured through LFPs. Notably, the LFP modulation was particularly pronounced in areas populated with burst neurons compared to pause or tonic cells.ConclusionThe results from our study emphasize the significance of burst neurons in the pathogenesis of dystonia and in the efficacy of proprioceptive modulation for its treatment. Moreover, we observed that the effects of vibration on focal CD were prominent in the α band LFP, indicating modulation of pallido‐cerebellar connectivity. Moreover, the pallidal effects of vibration in GD with CD involved modulation of cerebro‐pallidal θ band connectivity. Our analysis provides insight into how vibration‐induced changes in pallidal activity are integrated into the downstream motor circuit. © 2023 International Parkinson and Movement Disorder Society.