Dataset Information

Parkinson's Disease Exhibits Amplified Intermuscular Coherence During Dynamic Voluntary Action.

ABSTRACT: Parkinson's disease (PD) is typically diagnosed and evaluated on the basis of overt motor dysfunction, however, subtle changes in the frequency spectrum of neural drive to muscles have been reported as well. During dynamic actions, coactive muscles of healthy adults often share a common source of 6-15 Hz (alpha-band) neural drive, creating synchronous alpha-band activity in their EMG signals. Individuals with PD commonly exhibit kinetic action tremor at similar frequencies, but the potential relationship between the intermuscular alpha-band neural drive seen in healthy adults and the action tremor associated with PD is not well-understood. A close relationship is most tenable during voluntary dynamic tasks where alpha-band neural drive is strongest in healthy adults, and where neural circuits affected by PD are most engaged. In this study, we characterized the frequency spectrum of EMG synchronization (intermuscular coherence) in 16 participants with PD and 15 age-matched controls during two dynamic motor tasks: (1) rotation of a dial between the thumb and index finger, and (2) dynamic scaling of isometric precision pinch force. These tasks produce different profiles of coherence between the first dorsal interosseous and abductor pollicis brevis muscles. We sought to determine if alpha-band intermuscular coherence would be amplified in participants with PD relative to controls, if such differences would be task-specific, and if they would correlate with symptom severity. We found that relative to controls, the PD group displayed amplified, but similarly task-dependent, coherence in the alpha-band. The magnitude of coherence during the rotation task correlated with overall symptom severity as per the UPDRS rating scale. Finally, we explored the potential for our coherence measures, with no additional information, to discriminate individuals with PD from controls. The area under the Receiver Operating Characteristic curve (AUC) indicated a clear separation between groups (AUC = 0.96), even though participants with PD were on their typical medication and displayed only mild-moderate symptoms. We conclude that a task-dependent, intermuscular neural drive within the alpha-band is amplified in PD. Its quantification via intermuscular coherence analysis may provide a useful tool for detecting the presence of PD, or assessing its progression.

SUBMITTER: Laine CM

PROVIDER: S-EPMC7145888 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Parkinson's Disease Exhibits Amplified Intermuscular Coherence During Dynamic Voluntary Action.

Laine Christopher M CM Valero-Cuevas Francisco J FJ

Frontiers in neurology 20200403

Parkinson's disease (PD) is typically diagnosed and evaluated on the basis of overt motor dysfunction, however, subtle changes in the frequency spectrum of neural drive to muscles have been reported as well. During dynamic actions, coactive muscles of healthy adults often share a common source of 6-15 Hz (alpha-band) neural drive, creating synchronous alpha-band activity in their EMG signals. Individuals with PD commonly exhibit kinetic action tremor at similar frequencies, but the potential rel ...[more]

PMID: 32308641

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Project description:Tourette syndrome is characterized by 'unvoluntary' tics, which are compulsive, yet often temporarily suppressible. The inferior frontal gyrus is implicated in motor control, including inhibition of pre-potent actions through influences on downstream subcortical and motor regions. Although tic suppression in Tourette syndrome also engages the inferior frontal gyrus, it is unclear whether such prefrontal control of action is also dysfunctional: Tic suppression studies do not permit comparison with control groups, and neuroimaging studies of motor inhibition can be confounded by the concurrent expression or suppression of tics. Here, patients with Tourette syndrome were directly compared to control participants when performing an intentional inhibition task during functional MRI. Tic expression was recorded throughout for removal from statistical models. Participants were instructed to make a button press in response to Go cues, withhold responses to NoGo cues, and decide whether to press or withhold to 'Choose' cues. Overall performance was similar between groups, for both intentional inhibition rates (% Choose-Go) and reactive NoGo inhibition commission errors. A subliminal face prime elicited no additional effects on intentional or reactive inhibition. Across participants, the task activated prefrontal and motor cortices and subcortical nuclei, including pre-supplementary motor area, inferior frontal gyrus, insula, caudate nucleus, thalamus and primary motor cortex. In Tourette syndrome, activity was elevated in the inferior frontal gyrus, insula and basal ganglia, most notably within the right inferior frontal gyrus during voluntary action and inhibition (Choose-Go and Choose-NoGo), and reactive inhibition (NoGo-correct). Anatomically, the locus of this inferior frontal gyrus hyperactivation during control of voluntary action matched that previously reported for tic suppression. In Tourette syndrome, activity within the caudate nucleus was also enhanced during both intentional (Choose-NoGo) and reactive (NoGo-correct) inhibition. Strikingly, despite the absence of overt motor behaviour, primary motor cortex activity increased in patients with Tourette syndrome but decreased in controls during both reactive and intentional inhibition. Additionally, severity of premonitory sensations scaled with functional connectivity of the pre-supplementary motor area to the caudate nucleus, globus pallidus and thalamus when choosing to respond (Choose-Go). Together, these results suggest that patients with Tourette syndrome use equivalent prefrontal mechanisms to suppress tics and withhold non-tic actions, but require greater inferior frontal gyrus engagement than controls to overcome motor drive from hyperactive downstream regions, notably primary motor cortex. Moreover, premonitory sensations may cue midline motor regions to generate tics through interactions with the basal ganglia.

Dataset Information

Parkinson's Disease Exhibits Amplified Intermuscular Coherence During Dynamic Voluntary Action.

Publications

Parkinson's Disease Exhibits Amplified Intermuscular Coherence During Dynamic Voluntary Action.

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