Beta Waves in Action: Context-Dependent Modulations of Subthalamo-Cortical Synchronization during Rapid Reversals of Movement Direction
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eLife Assessment
This valuable study combined whole-head magnetoencephalography (MEG) and subthalamic (STN) local field potential (LFP) recordings in patients with Parkinson's disease undergoing deep brain stimulation surgery. The paper provides solid evidence that cortical and STN beta oscillations are sensitive to movement context and may play a role in the coordination of movement redirection.
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Abstract
The role of beta band activity in cortico-basal ganglia interactions during motor control has been studied extensively in resting-state and for simple movements, such as button pressing. However, little is known about how beta oscillations change and interact in more complex situations involving rapid changes of movement in various contexts.To close this knowledge gap, we combined magnetoencephalography (MEG) and local field potential recordings from the subthalamic nucleus (STN) in Parkinson’s disease patients to study beta dynamics during initiation, stopping, and rapid reversal of rotational movements. The action prompts were manipulated to be predictable vs. unpredictable.We observed movement-related beta suppression at motor sequence start, and a beta rebound after motor sequence stop in STN power, motor cortical power, and STN-cortex coherence. Despite involving a brief stop of movement, no clear rebound was observed during reversals of turning direction. On the cortical level, beta power decreased bilaterally following reversals, but more so in the hemisphere ipsilateral to movement, due to a floor effect on the contralateral side. In the STN, power modulations varied across patients, with patients revealing brief increases or decreases of high-beta power. Importantly, cue predictability affected these modulations. Event-related changes of STN-cortex beta coherence were generally stronger in the unpredictable than in the predictable condition.In summary, this study reveals the influence of movement context on beta oscillations in basal ganglia-cortex loops when humans change ongoing movements according to external cues. We find that movement scenarios requiring higher levels of caution involve enhanced modulations of subthalamo-cortical beta synchronization. Further, our results confirm that beta oscillations reflect the start and end of motor sequences better than movement changes within a sequence.
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eLife Assessment
This valuable study combined whole-head magnetoencephalography (MEG) and subthalamic (STN) local field potential (LFP) recordings in patients with Parkinson's disease undergoing deep brain stimulation surgery. The paper provides solid evidence that cortical and STN beta oscillations are sensitive to movement context and may play a role in the coordination of movement redirection.
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Reviewer #1 (Public review):
Summary:
Winkler et al. present brain activity patterns related to complex motor behaviour by combining whole-head magnetoencephalography (MEG) with subthalamic local field potential (LFP) recordings from people with Parkinson's disease. The motor task involved repetitive circular movements with stops or reversals associated with either predictable or unpredictable cues. Beta and gamma frequency oscillations are described, and the authors found complex interactions between recording sites and task conditions. For example, they observed stronger modulation of connectivity in unpredictable conditions. Moreover, STN power varied across patients during reversals, which differed from stopping movements. The authors conclude that cortex-STN beta modulation is sensitive to movement context, with potential relevance …
Reviewer #1 (Public review):
Summary:
Winkler et al. present brain activity patterns related to complex motor behaviour by combining whole-head magnetoencephalography (MEG) with subthalamic local field potential (LFP) recordings from people with Parkinson's disease. The motor task involved repetitive circular movements with stops or reversals associated with either predictable or unpredictable cues. Beta and gamma frequency oscillations are described, and the authors found complex interactions between recording sites and task conditions. For example, they observed stronger modulation of connectivity in unpredictable conditions. Moreover, STN power varied across patients during reversals, which differed from stopping movements. The authors conclude that cortex-STN beta modulation is sensitive to movement context, with potential relevance for movement redirection.
Strengths:
This study employs a unique methodology, leveraging the rare opportunity to simultaneously record both invasive and non-invasive brain activity to explore oscillatory networks.
Weaknesses:
It is difficult to interpret the role of the STN in the context of reversals because no consistent activity pattern emerged.
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Reviewer #2 (Public review):
Summary:
This study examines the role of beta oscillations in motor control, particularly during rapid changes in movement direction among patients with Parkinson's disease. The researchers utilized magnetoencephalography (MEG) and local field potential (LFP) recordings from the subthalamic nucleus to investigate variations in beta band activity within the cortex and STN during the initiation, cessation, and reversal of movements, as well as the impact of external cue predictability on these dynamics. The primary finding indicates that beta oscillations more effectively signify the start and end of motor sequences than transitions within those sequences. The article is well-written, clear, and concise.
Strengths:
The use of a continuous motion paradigm with rapid reversals extends the understanding of beta …
Reviewer #2 (Public review):
Summary:
This study examines the role of beta oscillations in motor control, particularly during rapid changes in movement direction among patients with Parkinson's disease. The researchers utilized magnetoencephalography (MEG) and local field potential (LFP) recordings from the subthalamic nucleus to investigate variations in beta band activity within the cortex and STN during the initiation, cessation, and reversal of movements, as well as the impact of external cue predictability on these dynamics. The primary finding indicates that beta oscillations more effectively signify the start and end of motor sequences than transitions within those sequences. The article is well-written, clear, and concise.
Strengths:
The use of a continuous motion paradigm with rapid reversals extends the understanding of beta oscillations in motor control beyond simple tasks. It offers a comprehensive perspective on subthalamo-cortical interactions by combining MEG and LFP.
Weaknesses:
(1) The small and clinically diverse sample size may limit the robustness and generalizability of the findings. Additionally, the limited exploration of causal mechanisms reduces the depth of its conclusions and focusing solely on Parkinson's disease patients might restrict the applicability of the results to broader populations.
(2) The small sample size and variability in clinical characteristics among patients may limit the robustness of the study's conclusions. It would be beneficial for the authors to acknowledge this limitation and propose strategies for addressing it in future research. Additionally, incorporating patient-specific factors as covariates in the ANOVA could help mitigate the confounding effects of heterogeneity.
(3) The author may consider using standardized statistics, such as effect size, that would provide a clearer picture of the observed effect magnitude and improve comparability.
(4) Although the study identifies revelance between beta activity and motor events, it lacks causal analysis and discussion of potential causal mechanisms. Given the valuable datasets collected, exploring or discussing causal mechanisms would enhance the depth of the study.
(5) The study cohort focused on senior adults, who may exhibit age-related cortical responses during movement planning in neural mechanisms. These aspects were not discussed in the study.
(6) Including a control group of patients with other movement disorders who also undergo DBS surgery would be beneficial. Because we cannot exclude the possibility that the observed findings are specific to PD or can be generalized. Additionally, the current title and the article, which are oriented toward understanding human motor control, may not be appropriate.
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Reviewer #3 (Public review):
Summary:
The study highlights how the initiation, reversal, and cessation of movements are linked to changes in beta synchronization within the basal ganglia-cortex loops. It was observed that different movement phases, such as starting, stopping briefly, and stopping completely, affect beta oscillations in the motor system.
It was found that unpredictable cues lead to stronger changes in STN-cortex beta coherence. Additionally, specific patterns of beta and gamma oscillations related to different movement actions and contexts were observed. Stopping movements was associated with a lack of the expected beta rebound during brief pauses within a movement sequence.
Overall, the results underline the complex and context-dependent nature of motor-control and emphasize the role of beta oscillations in managing …
Reviewer #3 (Public review):
Summary:
The study highlights how the initiation, reversal, and cessation of movements are linked to changes in beta synchronization within the basal ganglia-cortex loops. It was observed that different movement phases, such as starting, stopping briefly, and stopping completely, affect beta oscillations in the motor system.
It was found that unpredictable cues lead to stronger changes in STN-cortex beta coherence. Additionally, specific patterns of beta and gamma oscillations related to different movement actions and contexts were observed. Stopping movements was associated with a lack of the expected beta rebound during brief pauses within a movement sequence.
Overall, the results underline the complex and context-dependent nature of motor-control and emphasize the role of beta oscillations in managing movement according to changing external cues.
Strengths:
The paper is very well written, clear, and appears methodologically sound.
Although the use of continuous movement (turning) with reversals is more naturalistic than many previous button push paradigms.
Weaknesses:
The generalizability of the findings is somewhat curtailed by the fact that this was performed peri-operatively during the period of the microlesion effect. Given the availability of sensing-enabled DBS devices now and HD-EEG, does MEG offer a significant enough gain in spatial localizability to offset the fact that it has to be done shortly postoperatively with externalized leads, with an attendant stun effect? Specifically, for paradigms that are not asking very spatially localized questions as a primary hypothesis?
Further investigation of the gamma signal seems warranted, even though it has a slightly lower proportional change in amplitude in beta. Given that the changes in gamma here are relatively wide band, this could represent a marker of neural firing that could be interestingly contrasted against the rhythm account presented.
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