Pallidal low β-low γ phase-amplitude coupling inversely correlates with Parkinson disease symptoms

Tsiokos, Christos; Malekmohammadi, Mahsa; AuYong, Nicholas; Pouratian, Nader

doi:10.1016/j.clinph.2017.08.001

Cited by 40 publications

(56 citation statements)

References 52 publications

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“…Interestingly, it is not clear whether the situation is similar in the GPi. Thus, in a study of LFP PAC in GPi, Tsiokos and colleagues reported an inverse relationship between PAC and parkinsonian signs, suggesting that a high level of PAC could be a normal feature of GPi physiology …”

Section: Parkinsonism As Dysfunction Of the Basal Ganglia Thalamocortmentioning

confidence: 99%

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: Parkinsonism As Dysfunction Of the Basal Ganglia Thalamocortmentioning

confidence: 99%

Changing views of the pathophysiology of Parkinsonism

Wichmann

2019

Movement Disorders

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“…This is in contrast to local oscillatory power in PD, which is sometimes reported as increased at baseline and suppressed with therapy and other times reported as neither abnormally elevated nor modulated by therapy (Kühn et al 2006b;Weinberger et al 2006;Ray et al 2008;Kühn et al 2009;de Hemptinne et al 2015;Swann et al 2015;Weiss et al 2015). In addition, as recent studies suggest functional dissociations between low (~12-20hz) and high (~20-35hz) beta bands in the BGTC network (van Wijk et al 2016;Tsiokos et al 2017), we also examined whether movement specificity is differentially represented in specific sub-bands within the alpha/beta range.…”

Section: Introductionmentioning

confidence: 92%

“…In BGTC network, coupling between alpha/beta phase and gamma amplitude is modulated by movement (Yanagisawa et al 2012;de Hemptinne et al 2013;Kato et al 2016;Kondylis et al 2016;Tsiokos et al 2017;AuYong et al 2018) and we therefore focused on these frequency bands. To calculate the dPAC, instantaneous phase angles were extracted as the angle of the analytic signal at the frequencies of interest for phase (4-40Hz) and corresponding instantaneous amplitudes were extracted as the squared absolute value of the analytic signal at the frequencies of interest for amplitude (30-300 Hz).…”

Section: Neurophysiologic Signal Processingmentioning

confidence: 99%

“…Alpha and beta oscillations in the BGTC are often referred to as "anti-kinetic" signals, because they are prominent when the motor system is idling or maintaining a motor state (Engel and Fries 2010;van Wijk et al 2012;Stolk et al 2019). The association of suppression in alpha and beta power with de Hemptinne et al 2015;Oswal et al 2016;Tsiokos et al 2017;Malekmohammadi et al 2018a;Malekmohammadi et al 2018b). This is in contrast to local oscillatory power in PD, which is sometimes reported as increased at baseline and suppressed with therapy and other times reported as neither abnormally elevated nor modulated by therapy (Kühn et al 2006b;Weinberger et al 2006;Ray et al 2008;Kühn et al 2009;de Hemptinne et al 2015;Swann et al 2015;Weiss et al 2015).…”

Section: Introductionmentioning

confidence: 99%

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Movement-related changes in pallidocortical synchrony differentiate action execution and observation in humans

Cross

Malekmohammadi

Choi

et al. 2020

Preprint

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Suppression of local and network alpha (8)(9)(10)(11)(12) and beta oscillations in the human basal ganglia-thalamocortical (BGTC) circuit is a prominent feature of movement. Local alpha/beta power, cross-region beta phase coupling, and phase-amplitude coupling (PAC) have all been shown to be suppressed during movement in multiple nodes of the BGTC. However, the specificity of these various movement-related changes to actual movement execution remains poorly understood. To differentiate signals that are specifically related to movement execution, we compared changes in globus pallidus internus (GPi) and motor cortical local oscillatory activity and coupling (cross-region phase coupling and local PAC) during movement execution and movement observation in 12 patients with Parkinson disease undergoing deep brain stimulator implantation. We hypothesized that network coupling is more directly related to movement execution than local power changes, given the putative role of pathological network coupling in movement disorders such as Parkinson disease. We observed suppression of alpha/beta power during action observation and execution in the globus pallidus and motor cortex during both action execution and action observation. In contrast, pallidocortical coherence and GPi and motor cortical alpha/beta-gamma PAC were significantly suppressed only during action execution. Our results demonstrate a functional dissociation within the BG-cortical network during action execution and observation in which suppression of BG-cortical functional connectivity and local phase amplitude coupling are features specifically of overt movement, suggesting a particularly important role in motor execution. This has implications for identification and use of intracranial signals for closed loop brain stimulation therapies.

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“…Despite the fact that the internal globus pallidus (GPi) is increasingly being targeted for DBS in PD patients, there are relatively few reports exploring LFP activity in the pallidum (Priori et al, 2002;Silberstein et al, 2003;Tsiokos et al, 2013Tsiokos et al, , 2017AuYong et al, 2018;Aman et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

High-frequency oscillations in the internal globus pallidus: a pathophysiological biomarker in Parkinson's disease?

Johnson

Aman

et al. 2020

Preprint

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Abnormal oscillatory neural activity in the basal ganglia is thought to play a pathophysiological role in Parkinson's disease. Many patient studies have focused on beta frequency band local field potential activity in the subthalamic nucleus, however increasing evidence points to alterations in neural oscillations in high frequency ranges (>100 Hz) having pathophysiological relevance. Prior studies have found that power in subthalamic high frequency oscillations (HFOs) is positively correlated with dopamine tone and increased during voluntary movements, implicating these brain rhythms in normal basal ganglia function. Contrary to this idea, in the current study we present a combination of clinical and preclinical data that support the hypothesis that HFOs in the internal globus pallidus (GPi) are a pathophysiological feature of Parkinson's disease. Spontaneous and movement-related pallidal field potentials were recorded from deep brain stimulation (DBS) leads targeting the GPi in five externalized Parkinson's disease patients, on and off dopaminergic medication. We identified a prominent oscillatory peak centered at 200-300 Hz in the off-medication rest recordings in all patients. High frequency power increased during movement, and the magnitude of modulation was negatively correlated with bradykinesia.Moreover, high frequency oscillations were significantly attenuated in the on-medication condition, suggesting they are a feature of the parkinsonian condition. To further confirm that GPi high frequency oscillations are characteristic of dopamine depletion, we also collected field potentials from DBS leads chronically implanted in three rhesus monkeys before and after the induction of parkinsonism with the neurotoxin 1-methyl-4-phenyl-1,2,3,6 tetrahydropyridine (MPTP). High frequency oscillations and their modulation during movement were not prominent in the normal condition but emerged in the parkinsonian condition in the monkey model. These data provide the first evidence demonstrating that exaggerated, movement-modulated high frequency oscillations in the internal globus pallidus are a pathophysiological feature of Parkinson's disease, and motivate additional investigations into the functional roles of high frequency neural oscillations across the basal ganglia-thalamocortical motor circuit and their relationship to motor control in normal and diseased states. These findings also provide rationale for further exploration of these signals for electrophysiological biomarker-based device programming and stimulation strategies in patients receiving deep brain stimulation therapy.

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Pallidal low β-low γ phase-amplitude coupling inversely correlates with Parkinson disease symptoms

Cited by 40 publications

References 52 publications

Changing views of the pathophysiology of Parkinsonism

Changing views of the pathophysiology of Parkinsonism

Movement-related changes in pallidocortical synchrony differentiate action execution and observation in humans

High-frequency oscillations in the internal globus pallidus: a pathophysiological biomarker in Parkinson's disease?

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