Distinct Subthalamic Coupling in the ON State Describes Motor Performance in Parkinson's Disease

Öztürk, Musa; Abosch, Aviva; Francis, D.; Wu, Jianping; Jimenez‐Shahed, Joohi; Ince, Nuri F.

doi:10.1002/mds.27800

Cited by 29 publications

(38 citation statements)

References 48 publications

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“…In particular, the excessive beta peak seen in 8-30 Hz range is suppressed upon dopaminergic medication intake (Brown et al, 2001;Williams et al, 2002;Alonso-Frech et al, 2006;Lopez-Azcarate et al, 2010;Swann et al, 2016;Ozturk et al, 2019). Additionally, the HFO activity seen between 200 and 300 Hz shifts to 300 and 400 Hz frequency range and CFC disappears concurrently (Lopez-Azcarate et al, 2010;van Wijk et al, 2016;Ozturk et al, 2019). LFP peaks in 70-90 Hz range in the STN have also been reported and have been associated with voluntary movement (Cassidy et al, 2002;Cheyne et al, 2008;Thompson et al, 2014) and levodopa-induced dyskinesias (Swann et al, 2016).…”

Section: Introductionmentioning

confidence: 95%

“…The effect of dopaminergic medication on LFP patterns of the STN has been studied through the postoperative recordings from chronic DBS leads (macroelectrodes). In particular, the excessive beta peak seen in 8-30 Hz range is suppressed upon dopaminergic medication intake (Brown et al, 2001;Williams et al, 2002;Alonso-Frech et al, 2006;Lopez-Azcarate et al, 2010;Swann et al, 2016;Ozturk et al, 2019). Additionally, the HFO activity seen between 200 and 300 Hz shifts to 300 and 400 Hz frequency range and CFC disappears concurrently (Lopez-Azcarate et al, 2010;van Wijk et al, 2016;Ozturk et al, 2019).…”

Section: Introductionmentioning

confidence: 98%

“…The spatio-spectral characteristics of local field potentials (LFPs) recorded from the same microelectrodes have also been investigated in the territories of STN (Wang et al, 2014;Telkes et al, 2016;van Wijk et al, 2017). Excessive oscillations discovered in the 8-30 Hz (beta) (Priori et al, 2004;Kühn et al, 2006;Chen et al, 2007;Ray et al, 2008;Eusebio and Brown, 2009) and 200-400 Hz (high frequency oscillations, HFO) bands, and the cross-frequency coupling (CFC) between these bands (Foffani et al, 2003;Lopez-Azcarate et al, 2010;Özkurt et al, 2011;Hirschmann et al, 2016;van Wijk et al, 2017;Telkes et al, 2018;Ozturk et al, 2019), have been shown to correlate with the motor symptoms (van Wijk et al, 2016;Shreve et al, 2017;Ozturk et al, 2019) and subtypes of the disease (Telkes et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

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Subthalamic Single Cell and Oscillatory Neural Dynamics of a Dyskinetic Medicated Patient With Parkinson's Disease

et al. 2020

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Single cell neuronal activity (SUA) and local field potentials (LFP) in the subthalamic nucleus (STN) of unmedicated Parkinson's disease (PD) patients undergoing deep brain stimulation (DBS) surgery have been well-characterized during microelectrode recordings (MER). However, there is limited knowledge about the changes in the firing patterns and oscillations above and within the territories of STN after the intake of dopaminergic medication. Here, for the first time, we report the STN single cell and oscillatory neural dynamics in a medicated patient with idiopathic PD using intraoperative MER. We recorded LFP and SUA with microelectrodes at various depths during bilateral STN-DBS electrode implantation. We isolated 26 neurons in total and observed that tonic and irregular firing patterns of individual neurons predominated throughout the territories of STN. While burst-type firings have been well-characterized in the dorsal territories of STN in unmedicated patients, interestingly, this activity was not observed in our medicated subject. LFP recordings lacked the excessive beta (8-30 Hz) activity, characteristic of the unmedicated state and signal energy was mainly dominated by slow oscillations below 8 Hz. We observed sharp gamma oscillations between 70 and 90 Hz within and above the STN. Despite the presence of a broadband high frequency activity in 200-400 Hz range, no cross-frequency interaction in the form of phase-amplitude coupling was noted between low and high frequency oscillations of LFPs. While our results are in agreement with the previously reported LFP recordings from the DBS lead in medicated PD patients, the sharp gamma peak present throughout the depth recordings and the lack of bursting firings after levodopa intake have not been reported before. The lack of bursting in SUA, the lack of excessive beta activity and cross frequency coupling between HFOs and lower rhythms further validate the link between bursting firing regime of neurons and pathological oscillatory neural activity in PD-STN. Overall, these observations not only validate the existing literature on the PD electrophysiology in healthy/medicated animal models but also provide insights regarding the underlying electro-pathophysiology of levodopa-induced dyskinesias in PD patients through demonstration of multiscale relationships between single cell firings and field potentials.

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Section: Introductionmentioning

confidence: 95%

Section: Introductionmentioning

confidence: 98%

Section: Introductionmentioning

confidence: 99%

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Subthalamic Single Cell and Oscillatory Neural Dynamics of a Dyskinetic Medicated Patient With Parkinson's Disease

et al. 2020

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“…We have also shown that the modulation patterns are specific to the beta band as no significant modulation was present in the bands above or below (8-12 and 30-40 Hz). In addition, our analyses of the low-and high-beta sub-bands (15-20 and 20-30 Hz) produced similar modulation patterns, hence we could not gain any novel insights into the different nature of these bands, although differences in HFA coupling with these bands have been reported previously (Ozturk et al, 2019).…”

Section: Choice Of Frequency Bandsmentioning

confidence: 66%

“…However, intake of dopaminergic medication also resulted in increased coupling between the phase of STN high-beta activity and local HFA in a 300-400 Hz band and was associated with greater motor improvement (Ozturk et al, 2019), suggesting that some forms of beta-HFA PAC can even be beneficial for movement control.…”

Section: Functional Relevance Of Cortico-subcortical Couplingmentioning

confidence: 99%

Basal ganglia high-frequency activity is co-modulated with the phase of motor cortical beta and shifted between the subthalamic nucleus and the internal pallidum during sustained motor control

Fischer

Pogosyan

Green

et al. 2020

Preprint

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Beta oscillations are readily observed in motor cortex and the basal ganglia, but to which extent they are functionally relevant is unclear. To understand how activity transfer between different nodes of the cortico-basal ganglia network is affected by cortical beta oscillations in different behavioural conditions, we recorded local field potentials and electroencephalography (EEG) activity in a low-force motor control task and during rest in Parkinson's patients undergoing deep brain stimulation (DBS) surgery. The patients received DBS of either the subthalamic nucleus (STN) or the internal globus pallidus (GPi), which allowed us to investigate if STN and GPi broad-band high-frequency activity (HFA; >150 Hz) is co-modulated with the phase of motor cortical beta activity. We found significant modulation patterns in the STN and the GPi, which were inverted while patients performed the task, showing that GPi activity fluctuations likely are crafted by other inputs than the direct excitatory STN afferents. We also found that consistent STN modulation disappeared during rest, showing disengagement in this condition, while GPi modulation was maintained, again evidencing that beta-band activity fluctuations in the GPi can be relatively independent of those in the STN. The difference between HFA modulation patterns in the task and rest recordings suggests a potential functional role of beta phase-locked HFA modulation in controlling sustained contractions. Examination of HFA co-modulation patterns at different sites of the cortico-basal ganglia-thalamo-cortical network under different behavioural conditions may provide a tool with which to define the impact of beta synchronization on network communication.

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High‐Frequency Oscillations in the Pallidum: A Pathophysiological Biomarker in Parkinson's Disease?

Johnson

Aman

et al. 2021

Movement Disorders

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A BS TRACT: Background: Abnormal oscillatory neural activity in the beta-frequency band (13-35 Hz) is thought to play a role in Parkinson's disease (PD); however, increasing evidence points to alterations in high-frequency ranges (>100 Hz) also having pathophysiological relevance. Objectives: Studies have found that power in subthalamic nucleus (STN) high-frequency oscillations is increased with dopaminergic medication and during voluntary movements, implicating these brain rhythms in normal basal ganglia function. The objective of this study was to investigate whether similar signaling occurs in the internal globus pallidus (GPi), a nucleus increasingly used as a target for deep brain stimulation (DBS) for PD. Methods: Spontaneous and movement-related GPi field potentials were recorded from DBS leads in 5 externalized PD patients on and off dopaminergic medication, as well as from 3 rhesus monkeys before and after the induction of parkinsonism with the neurotoxin 1-methyl-4-phenyl-1,2,3,6 tetrahydropyridine. Results: In the parkinsonian condition, we identified a prominent oscillatory peak centered at 200-300 Hz that increased during movement. In patients the magnitude of highfrequency oscillation modulation was negatively correlated with bradykinesia. In monkeys, high-frequency oscillations were mostly absent in the naive condition but emerged after the neurotoxin 1-methyl-4-phenyl-1,2,3,6 tetrahydropyridine. In patients, spontaneous high-frequency oscillations were significantly attenuated on-medication. Conclusions: Our findings provide evidence in support of the hypothesis that exaggerated, movementmodulated high-frequency oscillations in the GPi are pathophysiological features of PD. These findings suggest that the functional role(s) of high-frequency oscillations may differ between the STN and GPi and motivate additional investigations into their relationship to motor control in normal and diseased states.

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Distinct Subthalamic Coupling in the ON State Describes Motor Performance in Parkinson's Disease

Cited by 29 publications

References 48 publications

Subthalamic Single Cell and Oscillatory Neural Dynamics of a Dyskinetic Medicated Patient With Parkinson's Disease

Subthalamic Single Cell and Oscillatory Neural Dynamics of a Dyskinetic Medicated Patient With Parkinson's Disease

Basal ganglia high-frequency activity is co-modulated with the phase of motor cortical beta and shifted between the subthalamic nucleus and the internal pallidum during sustained motor control

High‐Frequency Oscillations in the Pallidum: A Pathophysiological Biomarker in Parkinson's Disease?

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