Wrist Joint Proprioceptive Function and Its Corresponding Cortical Neural Activity in Cervical Dystonia

Abstract

Cervical dystonia is associated with abnormal movement and postures in the cervical region. There is evidence of abnormal somatosensory function in dystonia, even in non-affected limbs. This indicates a link between the atypical processing of somatosensory information and the generation of abnormal motor outputs. This study set out to explore this linkage systematically pursuing the following specific aims: First, to document the extent of proprioceptive dysfunction in the non-symptomatic wrist joint in CD during passive and active movement. Second, to investigate how such proprioceptive dysfunction is associated with atypical activity in somatosensory-motor cortical areas. Third, to explore how BOTOX injections, a common symptomatic treatment of dystonia, affect the neural and behavioral measures of proprioception in CD. METHOD: Fifteen CD and 15 control participants were invited. To achieve aim 1, wrist proprioception was evaluated based on: (1) wrist position sense discrimination threshold (examining “pure” proprioceptive function in the contralateral hemisphere); (2) ipsilateral matching error, i.e., the ability to proprioceptively perceive the wrist position of one hand and to match this experienced position by actively moving the same hand to it (examining the integrity of somatosensory function/somatosensory-motor integration in the contralateral hemisphere); and (3) the contralateral matching error, i.e., the ability to proprioceptively perceive wrist position of one hand and to match this experienced position by actively moving the opposite hand to it (examining the integrity of the inter-hemispheric exchange of somatosensory-motor information). To achieve aim 2, the anticipation period prior to ipsilateral/contralateral matching (reflecting cortical processes involved in motor planning) was targeted for studying cortical potentials associated with the proprioceptive function. Derived EEG features include: (1) change in spectral power during motor preparation in relation to rest, and (2) inter-regional spectral coherence during motor preparation. To achieve aim three, measurements of proprioceptive function were compared in the CD group pre- and post-BOTOX injection. RESULTS: In comparison to controls, the wrist position sense discrimination threshold was significantly larger in the CD group, both pre- and post-BOTOX injection. The ipsilateral matching error was significantly larger in the CD group only pre-BOTOX injection. EEG assessment of the ipsilateral matching task revealed a significantly larger beta-band synchronization in the contralateral motor cortex in the CD group. Within the CD group, BOTOX injection was associated with the significant decline of beta power over contralateral somatosensory-motor cortical areas. With respect to the contralateral matching task, patients pre-BOTOX showed a significantly larger somatosensory-motor coherence (1) in the contralateral hemisphere in the gamma band, and (2) in the ipsilateral hemisphere in the theta band. Patients, post-BOTOX, still maintained the significantly higher theta band coherence in the ipsilateral hemisphere. Within the patient group, BOTOX injection corresponded to the significant rise of beta band coherence between bilateral somatosensory areas. DISCUSSION: The behavioral findings confirm that somatosensory impairment to non-dystonic limbs is a feature of cervical dystonia. It is accompanied by excessive intra- and inter-regional cortical synchronization during the preparatory state of movement. They also provide evidence on the modulation of cortical somatosensory-motor activity and wrist proprioceptive performance concurrent with BOTOX injection. This sheds light on the sensory aspect of dystonia and the spread of sensory impairments to non-affected limbs.