Pallidal deep brain stimulation modulates excessive cortical high β phase amplitude coupling in Parkinson disease

Malekmohammadi, Mahsa; AuYong, Nicholas; Ricks-Oddie, Joni; Bordelon, Yvette; Pouratian, Nader

doi:10.1016/j.brs.2018.01.028

Cited by 57 publications

(65 citation statements)

References 63 publications

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“…Together with beta-band power, and corticocortical and basal ganglia/ cortical coherence, cortical PAC was associated with bradykinesia and rigidity 78 and lowered by therapeutically beneficial DBS in the STN or GPi. [79][80][81] As is true for other oscillatory activities (see above), increased cortical PAC is not specific for PD, but also occurs in patients with (isolated) dystonia 82 or essential tremor. 83 Studies of subcortical PAC in parkinsonian patients have focused on LFP recordings from the STN and GPi.…”

Section: Altered Firing Patterns and Oscillationsmentioning

confidence: 84%

“…In studies of ECoG and EEG signals from PD patients, the amplitude of gamma‐band oscillations was found to be abnormally coupled to the phase of ongoing beta‐band oscillations in a process called phase‐amplitude coupling (PAC). Together with beta‐band power, and corticocortical and basal ganglia/cortical coherence, cortical PAC was associated with bradykinesia and rigidity and lowered by therapeutically beneficial DBS in the STN or GPi . As is true for other oscillatory activities (see above), increased cortical PAC is not specific for PD, but also occurs in patients with (isolated) dystonia or essential tremor …”

Section: Parkinsonism As Dysfunction Of the Basal Ganglia Thalamocortmentioning

confidence: 92%

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Changing views of the pathophysiology of Parkinsonism

Wichmann

2019

Movement Disorders

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Studies of the pathophysiology of parkinsonism (specifically akinesia and bradykinesia) have a long history and primarily model the consequences of dopamine loss in the basal ganglia on the function of the basal ganglia/thalamocortical circuit(s). Changes of firing rates of individual nodes within these circuits were originally considered central to parkinsonism. However, this view has now given way to the belief that changes in firing patterns within the basal ganglia and related nuclei are more important, including the emergence of burst discharges, greater synchrony of firing between neighboring neurons, oscillatory activity patterns, and the excessive coupling of oscillatory activities at different frequencies. Primarily focusing on studies obtained in nonhuman primates and human patients with Parkinson's disease, this review summarizes the current state of this field and highlights several emerging areas of research, including studies of the impact of the heterogeneity of external pallidal neurons on parkinsonism, the importance of extrastriatal dopamine loss, parkinsonism‐associated synaptic and morphologic plasticity, and the potential role(s) of the cerebellum and brainstem in the motor dysfunction of Parkinson's disease. © 2019 International Parkinson and Movement Disorder Society

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Section: Altered Firing Patterns and Oscillationsmentioning

confidence: 84%

Section: Parkinsonism As Dysfunction Of the Basal Ganglia Thalamocortmentioning

confidence: 92%

Changing views of the pathophysiology of Parkinsonism

Wichmann

2019

Movement Disorders

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“…Once again thalamic DBS and GPi DBS showed a similar pattern, but DBS to the GPe did not. Recent work has shown that GPi DBS has a similar effect on beta oscillations as STN DBS (Malekmohammadi et al, 2018). There are no accounts of the effect of human GPe DBS on beta-band activity in the brain, and while the presence of such oscillations can also be an aspect of healthy physiological brain activity, this demonstrates the ability of DBS via STN, GPi or thalamus to suppress beta frequency oscillations, and hypothesizes that GPe DBS may act via a different mechanism as previously suggested (Vitek et al, 2012).…”

Section: Discussionmentioning

confidence: 99%

A Population Model of Deep Brain Stimulation in Movement Disorders From Circuits to Cells

Yousif

Bain

Nandi

et al. 2020

Front. Hum. Neurosci.

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For more than 30 years, deep brain stimulation (DBS) has been used to target the symptoms of a number of neurological disorders and in particular movement disorders such as Parkinson's disease (PD) and essential tremor (ET). It is known that the loss of dopaminergic neurons in the substantia nigra leads to PD, while the exact impact of this on the brain dynamics is not fully understood, the presence of beta-band oscillatory activity is thought to be pathological. The cause of ET, however, remains uncertain, however pathological oscillations in the thalamocortical-cerebellar network have been linked to tremor. Both of these movement disorders are treated with DBS, which entails the surgical implantation of electrodes into a patient's brain. While DBS leads to an improvement in symptoms for many patients, the mechanisms underlying this improvement is not clearly understood, and computational modeling has been used extensively to improve this. Many of the models used to study DBS and its effect on the human brain have mainly utilized single neuron and single axon biophysical models. We have previously shown in separate models however, that the use of population models can shed much light on the mechanisms of the underlying pathological neural activity in PD and ET in turn, and on the mechanisms underlying DBS. Together, this work suggested that the dynamics of the cerebellar-basal ganglia thalamocortical network support oscillations at frequency range relevant to movement disorders. Here, we propose a new combined model of this network and present new results that demonstrate that both Parkinsonian oscillations in the beta band and oscillations in the tremor frequency range arise from the dynamics of such a network. We find regions in the parameter space demonstrating the different dynamics and go on to examine the transition from one oscillatory regime to another as well as the impact of DBS on these different types of pathological activity. This work will allow us to better understand the changes in brain activity induced by DBS, and allow us to optimize this clinical therapy, particularly in terms of target selection and parameter setting.

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“…Converging evidence suggests that PAC is elevated in untreated PD patients compared to treated Swann et al, 2015;Malekmohammadi et al, 2018). It also emerges during the induction of severe parkinsonian symptoms in non-human primate models, and is related to disease severity (Devergnas et al, 2017).…”

Section: Mechanisms Of Waveform Shape Asymmetry and Pacmentioning

confidence: 99%

“…While conventional signal processing measures, such as beta power, have failed to reliably differentiate PD as a function of severity or diagnosis at the cortex (Stoffers et al, 2007;de Hemptinne et al, 2013;George et al, 2013;de Hemptinne et al, 2015;Swann et al, 2015;Malekmohammadi et al, 2018), novel metrics such as phase-amplitude correlations between beta and broadband gamma (50-150 Hz) (phase-amplitude coupling, PAC) have proven more promising. Specifically, PAC over motor cortex detected using electrocorticography (ECoG) is elevated in PD compared to other groups (de Hemptinne et al, 2013) and is reduced with DBS in a clinically-relevant manner Malekmohammadi et al, 2018). Interestingly, following characterization of PAC with ECoG, it was demonstrated that elevated PAC can also be detected non-invasively with scalp electroencephalography (EEG) .…”

Section: Introductionmentioning

confidence: 99%

Characteristics of Beta Waveform Shape in Parkinson’s Disease Detected with Scalp Electroencephalography

Jackson

Cole²,

Voytek

et al. 2019

Preprint

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Neural activity in the beta frequency range (13-30 Hz) is excessively synchronized in Parkinson's Disease (PD). Previous work using invasive intracranial recordings and non-invasive scalp electroencephalography (EEG) has shown that correlations between beta phase and broadband gamma amplitude (i.e., phase-amplitude coupling) are elevated in PD, perhaps a reflection of this synchrony. Recently, it has also been shown, in invasive human recordings, that nonsinusoidal features of beta oscillation shape also characterize PD. Here we show that these features of beta waveform shape also distinguish PD patients on and off medication using noninvasive recordings in a dataset of 15 PD patients with resting scalp EEG. Specifically, beta oscillations over sensorimotor electrodes in PD patients off medication had greater sharpness asymmetry and steepness asymmetry than on medication (sign rank, p=0.006, p=0.003 respectively). We also showed that beta oscillations over sensorimotor cortex most often had a canonical shape and that using this prototypical shape as an inclusion criterion increased the effect size of our findings. Together our findings suggest that novel ways of measuring beta synchrony that incorporate waveform shape could improve detection of PD pathophysiology in non-invasive recordings.

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Pallidal deep brain stimulation modulates excessive cortical high β phase amplitude coupling in Parkinson disease

Abstract: Similar to STN-DBS, GPi-DBS reduces motor cortical β-γ PAC, like that also reported with dopaminergic mediations, suggesting it is a generalizable symptom biomarker in PD, independent of therapeutic target or proximity to the hyperdirect pathway.

Cited by 57 publications

References 63 publications

Changing views of the pathophysiology of Parkinsonism

Changing views of the pathophysiology of Parkinsonism

A Population Model of Deep Brain Stimulation in Movement Disorders From Circuits to Cells

Characteristics of Beta Waveform Shape in Parkinson’s Disease Detected with Scalp Electroencephalography

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