Left hemisphere dominance for bilateral kinematic encoding in the human brain

Merrick, Christina; Dixon, Tanner C; Breska, Assaf; Lin, Jack J.; Chang, Edward F.; King-Stephens, David; Laxer, Kenneth D.; Weber, Peter B.; Carmena, Jose M.; Knight, Robert T.; Ivry, Richard B

doi:10.7554/elife.69977

Cited by 29 publications

(22 citation statements)

References 67 publications

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“…We also found increased M1 beta power at rest in patients with PD with versus without dystonia, where other groups have used TMS to identify abnormal short‐term plasticity in patients with both primary dystonia and PD 44 . Notably, we found increases in hfb power during hand movements only, which confirms placement of the ECoG strip over the hand area of the motor cortex 45,46 (Fig. 3).…”

Section: Discussionsupporting

confidence: 80%

Cortical and Subthalamic Nucleus Spectral Changes During Limb Movements in Parkinson's Disease Patients with and Without Dystonia

et al. 2022

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Background Dystonia is an understudied motor feature of Parkinson's disease (PD). Although considerable efforts have focused on brain oscillations related to the cardinal symptoms of PD, whether dystonia is associated with specific electrophysiological features is unclear. Objective The objective of this study was to investigate subcortical and cortical field potentials at rest and during contralateral hand and foot movements in patients with PD with and without dystonia. Methods We examined the prevalence and distribution of dystonia in patients with PD undergoing deep brain stimulation surgery. During surgery, we recorded intracranial electrophysiology from the motor cortex and directional electrodes in the subthalamic nucleus (STN) both at rest and during self‐paced repetitive contralateral hand and foot movements. Wavelet transforms and mixed models characterized changes in spectral content in patients with and without dystonia. Results Dystonia was highly prevalent at enrollment (61%) and occurred most commonly in the foot. Regardless of dystonia status, cortical recordings display beta (13–30 Hz) desynchronization during movements versus rest, while STN signals show increased power in low frequencies (6.0 ± 3.3 and 4.2 ± 2.9 Hz peak frequencies for hand and foot movements, respectively). Patients with PD with dystonia during deep brain stimulation surgery displayed greater M1 beta power at rest and STN low‐frequency power during movements versus those without dystonia. Conclusions Spectral power in motor cortex and STN field potentials differs markedly during repetitive limb movements, with cortical beta desynchronization and subcortical low‐frequency synchronization, especially in patients with PD with dystonia. Greater knowledge on field potential dynamics in human motor circuits can inform dystonia pathophysiology in PD and guide novel approaches to therapy. © 2022 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society

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Section: Discussionsupporting

confidence: 80%

Cortical and Subthalamic Nucleus Spectral Changes During Limb Movements in Parkinson's Disease Patients with and Without Dystonia

et al. 2022

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“…We also found increased M1 beta power at rest in PD patients with versus without dystonia, where other groups have used TMS to identify abnormal short-term plasticity in patients with both primary dystonia and PD [44]. Of note, we found increases in high frequency broadband power during hand movements only, which confirms placement of the electrocorticography strip over the hand area of motor cortex [45, 46] ( Figure 3 ).…”

Section: Discussionsupporting

confidence: 80%

Cortical and STN spectral changes during limb movements in PD patients with and without dystonia

Nakhmani

Olson

Irwin

et al. 2022

Preprint

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Background: Dystonia is a prevalent yet under-studied motor feature of Parkinson disease (PD). Although considerable efforts have focused on brain oscillations related to the cardinal symptoms of PD, whether dystonia is associated with specific electrophysiological features is unclear. Objectives: To investigate subcortical and cortical field potentials at rest and during contralateral hand and foot movements in PD patients with versus without dystonia. Methods: We examined the prevalence and somatotopy of dystonia in PD patients undergoing deep brain stimulation (DBS) surgery. We recorded intracranial electrophysiology from sensorimotor cortex and directional DBS electrodes in subthalamic nucleus (STN), during both rest and voluntary contralateral limb movements. We used wavelet transforms and linear mixed models to characterize spectral content in patients with and without dystonia (n=25). Results: Dystonia was highly prevalent at enrollment (61%) and most common in the foot (78%). PD patients with dystonia display greater subthalamic theta and alpha power during movement (p < 0.05) but not at rest. Regardless of dystonia status, cortical recordings display prominent beta desynchronization (13-30 Hz) during movement, whereas STN signals show increases in spectral power at lower frequencies (4-20 Hz), with peaks at 6.0 +/- 3.3 and 4.2 +/- 2.9 Hz during hand and foot movements, respectively (p < 0.03). Conclusions: Whereas cortex was characterized by beta desynchronization during hand and foot movements similarly, STN showed limb-specific low frequency activity which was increased in PD patients with dystonia. These findings may help elucidate why PD-related dystonia is most common in the foot and help guide future closed-loop DBS devices.

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“…Human neuroimaging studies show that parietofrontal cortex is bilaterally activated by unilateral reaches, but with a preference for the contralateral limb (Bernier & Grafton, 2010; Cappadocia et al, 2017; Cavina-Pratesi et al, 2010; Connolly et al, 2003; Filimon et al, 2009; Gallivan, McLean, Smith, et al, 2011; Gallivan & Wood, 2009; Medendorp et al, 2003; Prado et al, 2005). Likewise, the monkey ‘parietal reach region’, which spans the medial intraparietal sulcus and area V6A and probably corresponds to mIPS/SPOC (Passarelli et al, 2021) shows some ipsilateral signals (Chang et al, 2008; Merrick et al, 2022) but is primarily modulated by reaches of the contralateral limb (Chang et al, 2008).…”

Section: Discussionmentioning

confidence: 99%

Parieto-frontal Oscillations Show Hand Specific Interactions with Top-Down Movement Plans

Blohm

Cheyne

Crawford

2022

Preprint

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To generate a hand-specific reach plan, the brain must integrate hand-specific signals with the desired movement strategy. Although various neurophysiology / imaging studies have investigated hand-target interactions in simple reach-to-target tasks, the whole-brain timing and distribution of this process remain unclear, especially for more complex, instruction-dependent motor strategies. Previously, we showed that a pro/anti-pointing instruction influences magnetoencephalographic (MEG) signals in frontal cortex that then propagate recurrently through parietal cortex (Blohm et al., 2019). Here, we contrasted left versus right hand pointing in the same task to investigate 1) which cortical regions of interest show hand specificity, and 2) which of those areas interact with the instructed motor plan. Eight bilateral areas – the parietooccipital junction (POJ), superior parietooccipital cortex (SPOC), supramarginal gyrus (SMG), middle / anterior interparietal sulcus (mIPS/aIPS), primary somatosensory / motor cortex (S1/M1), and dorsal premotor cortex (PMd) – showed hand-specific changes in beta band power, with four of these (M1, S1, SMG, aIPS) showing robust activation before movement onset. M1, SMG, SPOC, and aIPS showed significant interactions between contralateral hand specificity and the instructed motor plan, but not with bottom-up target signals. Separate hand / motor signals emerged relatively early and lasted through execution, whereas hand-motor interactions only occurred close to movement onset. Taken together with our previous results, these findings show that instruction-dependent motor plans emerge in frontal cortex and interact recurrently with hand-specific parietofrontal signals before movement onset to produce hand-specific motor behaviors.Impact StatementThe brain must generate different motor signals, depending which hand is used. The distribution and timing of hand use / instructed motor plan integration is not understood at the whole-brain level. Using whole-brain MEG recordings we show that different sub-networks involved in action planning code for hand usage (alpha and beta frequencies) and integrating hand use information into a hand-specific motor plan (beta band). The timing of these signals indicates that frontal cortex first creates a general motor plan and then integrates hand-specific frontoparietal information to produce a hand-specific motor plan.

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Left hemisphere dominance for bilateral kinematic encoding in the human brain

Cited by 29 publications

References 67 publications

Cortical and Subthalamic Nucleus Spectral Changes During Limb Movements in Parkinson's Disease Patients with and Without Dystonia

Cortical and Subthalamic Nucleus Spectral Changes During Limb Movements in Parkinson's Disease Patients with and Without Dystonia

Cortical and STN spectral changes during limb movements in PD patients with and without dystonia

Parieto-frontal Oscillations Show Hand Specific Interactions with Top-Down Movement Plans

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