Synergy as a new and sensitive marker of basal ganglia dysfunction: A study of asymptomatic welders

Abstract

Background Multi-digit synergies, a recently developed, theory-based method to quantify stability of motor action, are shown to reflect basal ganglia dysfunction associated with parkinsonian syndromes. In this study, we tested the hypothesis that multi-digit synergies may capture early and subclinical basal ganglia dysfunction. We chose asymptomatic welders to test the hypothesis because the basal ganglia are known to be most susceptible to neurotoxicity caused by welding-related metal accumulation (such as manganese and iron). Methods Twenty right-handed welders and 13 matched controls were invited to perform single- and multi-finger pressing tasks using the fingers of the right or left hand. United Parkinson’s Disease Rating Scale and Grooved Pegboard scores were used to gauge gross and fine motor dysfunction, respectively. High-resolution (3T) T1-weighted, T2-weighted, T1 mapping, susceptibility, and diffusion tensor MRIs were obtained to reflect manganese, iron accumulation, and microstructural changes in basal ganglia. The synergy index stabilizing total force and anticipatory synergy adjustments were computed, compared between groups, and correlated with estimates of basal ganglia manganese [the pallidal index, R1 (1/T1)], iron [R2* (1/T2*)], and microstructural changes [fractional anisotropy and mean diffusivity]. Results There were no significant differences in Unified Parkinson’s Disease Rating Scale (total or motor subscale) or Grooved Pegboard test scores between welders and controls. The synergy index during steady-state accurate force production was decreased significantly in the left hand of welders compared to controls (p=0.004) but did not reach statistical significance in the right hand (p=0.16). Anticipatory synergy adjustments, however, were not significantly different between groups. Among welders, higher synergy indices in the left hand were associated significantly with higher fractional anisotropy values in the left globus pallidus (R=0.731, p<0.001) but not with the pallidal index, R1, or R2* values in the basal ganglia. Conclusions These data suggest that multi-digit synergy metrics may serve as preclinical markers for basal ganglia dysfunction in welders and other populations at risk for neurodegenerative diseases involving parkinsonian symptoms. This finding may have important clinical, scientific, and public/occupational health implications.

Long-term effects of mild traumatic brain injuries to oculomotor tracking performances and reaction times to simple environmental stimuli

“…The application of principles of sensory-motor integration in laboratory settings is not new, but recent technical developments have caused these techniques to become more sensitive and reliable 15 – 17 . For example, the use of these principles has allowed the detection of subtle balance impairments in long-term mTBI survivors 18 and abnormalities in coordination of multi-finger force production and control in Parkinson’s disease 19 , 20 . Studies utilizing indices of oculomotor performance have been no exception; however, its application to cases of mTBI has yielded conflicting outcomes 8 , 21 , 22 .…”

Individual preferences in motor coordination seen across the two hands: relations to movement stability and optimality

“…Note that patients with various neurological disorders show significant impairments of action stability (Latash and Huang 2015). For example, this is true for patients with Parkinson’s disease at very early stages of the disorder when they are tested on optimal medication (Park et al 2012) and even for healthy persons who are at high risk for basal ganglia-related disorders, such as professional welders (Lewis et al 2016). Studies in patients with multiple sclerosis have shown a significant reduction in the synergy index (Δ V ), which was due to a nearly two-fold drop in the seemingly irrelevant component of inter-trial variance ( V UCM ), whereas the component that affected performance ( V ORT ), showed no difference between the patients and control subjects (Jo et al 2017).…”

Motor equivalence and structure of variance: multi-muscle postural synergies in Parkinson’s disease

“…In contrast, ASAs are reduced and decreased in magnitude in patients with both cortical and subcortical disorders (Park et al 2012; Jo et al 2016). Indices of synergic control are sensitive to very early stages of PD; they can be seen in the apparently non-involved hands of patients at HY stage-I (Park et al 2012, 2014) and even in asymptomatic persons at elevated risk for parkinsonism, such as professional welders (Lewis et al 2016). …”

“…Second, the approach has proven its specificity to subcortical neurological disorders (reviewed in Latash and Huang 2015) in support of the idea of distributed processing modules involving loops through the cerebellum and the basal ganglia (Houk 2005). Third, the approach is highly sensitive to very early stages of disorders (such as PD subjects in HY stage-I, Park et al 2012, 2013, 2014) and even to subclinical changes in persons at elevated risk for parkinsonism (Lewis et al 2016). Other mentioned approaches are typically computational, use behavioral indices with no clear links to physics and physiology, and/or are not as sensitive to disease-related changes.…”