Subthalamic low beta bursts differ in Parkinson’s disease phenotypes

Neto, Arnaldo Fim; Luccas, Julia Baldi de; Bianqueti, Bruno Leonardo; Silva, Luiz Ricardo da; Almeida, Tiago P.; Takahata, André K.; Teixeira, Manoel Jacobsen; Figueiredo, Eberval Gadelha; Nasuto, Slawomir J.; Rocha, M. S.; Soriano, Diogo C.; Godinho, Fábio

doi:10.1016/j.clinph.2022.05.013

Cited by 9 publications

(7 citation statements)

References 48 publications

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“…The observed disease-related changes in spontaneous cortical bursts, in the form of a more rapid decrease in burst rate over age for PD patients, could reflect inhibition of these projections along the thalamic-cortical pathways caused by disturbances in the dopamine-dependent structures projecting to the cortex. The association of beta burst duration with midline functions is in line with previous studies reporting that longer bursts in the subthalamic nucleus are associated with the postural-instability and gait disorder (PIGD) motor phenotype of PD 68 , 69 , Freezing of Gait and other gait features 70 . However, we did not find significant group differences in burst duration in the current study—in line with previously reported findings on cortical bursts in PD 14 —supporting the view that the central mechanisms of the cortical bursts are not primarily affected in PD—instead, it is the rate of bursts that is reduced at the cortical level.…”

Section: Discussionsupporting

confidence: 90%

Oscillatory and non-oscillatory features of the magnetoencephalic sensorimotor rhythm in Parkinson’s disease

Vinding,

Waldthaler,

Eriksson

et al. 2024

npj Parkinsons Dis.

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Parkinson’s disease (PD) is associated with changes in neural activity in the sensorimotor alpha and beta bands. Using magnetoencephalography (MEG), we investigated the role of spontaneous neuronal activity within the somatosensory cortex in a large cohort of early- to mid-stage PD patients (N = 78) on Parkinsonian medication and age- and sex-matched healthy controls (N = 60) using source reconstructed resting-state MEG. We quantified features of the time series data in terms of oscillatory alpha power and central alpha frequency, beta power and central beta frequency, and 1/f broadband characteristics using power spectral density. Furthermore, we characterised transient oscillatory burst events in the mu-beta band time-domain signals. We examined the relationship between these signal features and the patients’ disease state, symptom severity, age, sex, and cortical thickness. PD patients and healthy controls differed on PSD broadband characteristics, with PD patients showing a steeper 1/f exponential slope and higher 1/f offset. PD patients further showed a steeper age-related decrease in the burst rate. Out of all the signal features of the sensorimotor activity, the burst rate was associated with increased severity of bradykinesia, whereas the burst duration was associated with axial symptoms. Our study shows that general non-oscillatory features (broadband 1/f exponent and offset) of the sensorimotor signals are related to disease state and oscillatory burst rate scales with symptom severity in PD.

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Section: Discussionsupporting

confidence: 90%

Oscillatory and non-oscillatory features of the magnetoencephalic sensorimotor rhythm in Parkinson’s disease

Vinding,

Waldthaler,

Eriksson

et al. 2024

npj Parkinsons Dis.

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“…For example, patients with more aggressive motor progression may have a lower (residual) long-duration response to levodopa and, consequently, stronger beta oscillatory activity after overnight withdrawal of dopaminergic medication, as in our off medication recordings. A pathophysiological subtype specificity would also be consistent with beta oscillatory activity being stronger in the more aggressive postural-instability and gait disorder phenotype compared to the less aggressive tremor-dominant phenotype (Fim Neto et al, 2022;Godinho et al, 2021;Neuville et al, 2021), although this is not always observed (Telkes et al, 2018). A second possibility is that the causality is reversed in such a way that faster motor progression of the disease may actually be caused by stronger beta oscillatory activity.…”

Section: Clinical Correlationsmentioning

confidence: 82%

Oscillatory vs. non‐oscillatory subthalamic beta activity in Parkinson's disease

Pardo‐Valencia,

Fernández‐García,

Alonso‐Frech

et al. 2023

The Journal of Physiology

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Parkinson's disease is characterized by exaggerated beta activity (13–35 Hz) in cortico‐basal ganglia motor loops. Beta activity includes both periodic fluctuations (i.e. oscillatory activity) and aperiodic fluctuations reflecting spiking activity and excitation/inhibition balance (i.e. non‐oscillatory activity). However, the relative contribution, dopamine dependency and clinical correlations of oscillatory vs. non‐oscillatory beta activity remain unclear. We recorded, modelled and analysed subthalamic local field potentials in parkinsonian patients at rest while off or on medication. Autoregressive modelling with additive 1/f noise clarified the relationships between measures of beta activity in the time domain (i.e. amplitude and duration of beta bursts) or in the frequency domain (i.e. power and sharpness of the spectral peak) and oscillatory vs. non‐oscillatory activity: burst duration and spectral sharpness are specifically sensitive to oscillatory activity, whereas burst amplitude and spectral power are ambiguously sensitive to both oscillatory and non‐oscillatory activity. Our experimental data confirmed the model predictions and assumptions. We subsequently analysed the effect of levodopa, obtaining strong‐to‐extreme Bayesian evidence that oscillatory beta activity is reduced in patients on vs. off medication, with moderate evidence for absence of modulation of the non‐oscillatory component. Finally, specifically the oscillatory component of beta activity correlated with the rate of motor progression of the disease. Methodologically, these results provide an integrative understanding of beta‐based biomarkers relevant for adaptive deep brain stimulation. Biologically, they suggest that primarily the oscillatory component of subthalamic beta activity is dopamine dependent and may play a role not only in the pathophysiology but also in the progression of Parkinson's disease. imageKey points Beta activity in Parkinson's disease includes both true periodic fluctuations (i.e. oscillatory activity) and aperiodic fluctuations reflecting spiking activity and synaptic balance (i.e. non‐oscillatory activity). The relative contribution, dopamine dependency and clinical correlations of oscillatory vs. non‐oscillatory beta activity remain unclear. Burst duration and spectral sharpness are specifically sensitive to oscillatory activity, while burst amplitude and spectral power are ambiguously sensitive to both oscillatory and non‐oscillatory activity. Only the oscillatory component of subthalamic beta activity is dopamine‐dependent. Stronger beta oscillatory activity correlates with faster motor progression of the disease.

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“…In patients with Parkinson’s disease, subthalamic beta activity is hypothesized to be driven by cortex. The most recent multi-modal work 124 (combining MEG, LFP and computational modelling) suggests that cortical high-frequency beta oscillations (20–35 Hz) are propagated to STN, where they are subsequently converted to the more pathological low-frequency (13–20 Hz) rhythm 125 , 126 by the reciprocal connectivity of the STN-GPe network; a phenomenon that may be exacerbated in the hypodopaminergic state. 110 , 123 Importantly, while DBS modulates synchrony between cortex and STN, it does not change directionality of this network that follows the neuroanatomical/axonal orientation of the hyperdirect pathway.…”

Section: Macroscale Circuit Effects: Modulation Of Distributed Neurop...mentioning

confidence: 99%

Neurophysiological mechanisms of deep brain stimulation across spatiotemporal resolutions

Neumann

Steiner

Milosevic

2023

Brain

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Deep brain stimulation is a neuromodulatory treatment for managing the symptoms of Parkinson’s disease and other neurological and psychiatric disorders. Electrodes are chronically implanted in disease-relevant brain regions and pulsatile electrical stimulation delivery is intended to restore neurocircuit function. However, the widespread interest in the application and expansion of this clinical therapy has preceded an overarching understanding of the neurocircuit alterations invoked by deep brain stimulation. Over the years, various forms of neurophysiological evidence have emerged which demonstrate changes to brain activity across spatiotemporal resolutions; from single-neuron, to local field potential, to brain-wide cortical network effects. Though fruitful, such studies have often led to debate about a singular putative mechanism. In this Update we aim to produce an integrative account of complementary instead of mutually exclusive neurophysiological effects to derive a generalizable concept of the mechanisms of deep brain stimulation. In particular, we offer a critical review of the most common historical competing theories, an updated discussion on recent literature from animal and human neurophysiological studies, and a synthesis of synaptic and network effects of DBS across scales of observation, including micro-, meso-, and macroscale circuit alterations.

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Subthalamic low beta bursts differ in Parkinson’s disease phenotypes

Cited by 9 publications

References 48 publications

Oscillatory and non-oscillatory features of the magnetoencephalic sensorimotor rhythm in Parkinson’s disease

Oscillatory and non-oscillatory features of the magnetoencephalic sensorimotor rhythm in Parkinson’s disease

Oscillatory vs. non‐oscillatory subthalamic beta activity in Parkinson's disease

Neurophysiological mechanisms of deep brain stimulation across spatiotemporal resolutions

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