Synchrony of rest tremor in multiple limbs in Parkinson's disease: evidence for multiple oscillators

Ben‐Pazi, Hilla; Bergman, Hagai; Goldberg, Joshua A.; Giladi, Nir; Hansel, David; Reches, Avinoam; Simon, Ely S.

doi:10.1007/s007020170074

Cited by 65 publications

(37 citation statements)

References 21 publications

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“…Our observation is consistent with previous reports showing that neuronal oscillations in the globus pallidus are not always coherent with the tremulous limb (Hurtado et al 1999;Lemstra et al 1999;Raz et al 2000), although their oscillation frequency is similar to the frequency of the limb tremor (Hutchison et al 1997). Several studies of multilimb EMG recordings in PD patients also indicated that tremor in different limbs is largely uncorrelated (Ben-Pazi et al 2001;Hurtado et al 2000;Raethjen et al 2000). These studies, together with the fact that only half of the tremorfrequency neurons fire coherently with the LFP, support the earlier hypothesis that independent oscillatory circuits may underlie parkinsonian tremor in different extremities (Alberts et al 1969).…”

Section: Tremor-frequency Neuronal Activity: Relation To Tremorsupporting

confidence: 92%

“…It was originally suggested by Alberts et al (1969) that PD tremor is generated by segregated parallel networks, each involving a different limb. This idea was supported by studies showing that different limbs oscillate independently of each other (Ben-Pazi et al 2001;Hurtado et al 2000;Raethjen et al 2000). A recent study has further confirmed this hypothesis by showing that tremor-related activity in the globus pallidus can be coherent with one tremulous limb but not with the other (Hurtado et al 2005).…”

Section: Introductionmentioning

confidence: 76%

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Increased Gamma Oscillatory Activity in the Subthalamic Nucleus During Tremor in Parkinson's Disease Patients

Weinberger¹,

Hutchison²,

Lozano³

et al. 2009

Journal of Neurophysiology

127

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. Rest tremor is one of the main symptoms in Parkinson's disease (PD), although in contrast to rigidity and akinesia, the severity of the tremor does not correlate well with the degree of dopamine deficiency or the progression of the disease. Studies suggest that akinesia in PD patients is related to abnormal increased beta (15-30 Hz) and decreased gamma (35-80 Hz) synchronous oscillatory activity in the basal ganglia. Here we investigated the dynamics of oscillatory activity in the subthalamic nucleus (STN) during tremor. We used two adjacent microelectrodes to simultaneously record neuronal firing and local field potential (LFP) activity in nine PD patients who exhibited resting tremor during functional neurosurgery. We found that neurons exhibiting oscillatory activity at tremor frequency are located in the dorsal region of STN, where neurons with beta oscillatory activity are observed, and that their activity is coherent with LFP oscillations in the beta frequency range. Interestingly, in 85% of the 58 sites examined, the LFP exhibited increased oscillatory activity in the low gamma frequency range (35-55 Hz) during periods with stronger tremor. Furthermore, in 17 of 26 cases where two LFPs were recorded simultaneously, their coherence in the gamma range increased with increased tremor. When averaged across subjects, the ratio of the beta to gamma coherence was significantly lower in periods with stronger tremor compared with periods of no or weak tremor. These results suggest that resting tremor in PD is associated with an altered balance between beta and gamma oscillations in the motor circuits of STN.

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Section: Tremor-frequency Neuronal Activity: Relation To Tremorsupporting

confidence: 92%

Section: Introductionmentioning

confidence: 76%

Increased Gamma Oscillatory Activity in the Subthalamic Nucleus During Tremor in Parkinson's Disease Patients

Weinberger¹,

Hutchison²,

Lozano³

et al. 2009

Journal of Neurophysiology

127

View full text Add to dashboard Cite

show abstract

“…This phenomenon is occasionally observed in human patients (Vidailhet et al, 1999) and may be attributed to tremor masking by severe akinesia and rigidity. As in human studies (Hurtado et al, 2000;Raethjen et al, 2000;Ben-Pazi et al, 2001), the DRT states were characterized by a low coherence level between the tremor of the limbs even in Off states; however, in the levodopa-naive state, limb tremor was highly coherent. These results indicate (in line with the electrophysiological studies discussed below) that DRT causes major changes in the functional organization of the basal ganglia.…”

Section: Tremor Analysismentioning

confidence: 58%

Dopamine Replacement Therapy Does Not Restore the Full Spectrum of Normal Pallidal Activity in the 1-Methyl-4-Phenyl-1,2,3,6-Tetra-Hydropyridine Primate Model of Parkinsonism

et al. 2006

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Current physiological studies emphasize the role of neuronal oscillations and synchronization in the pathophysiology of Parkinson's disease; however, little is known about their specific roles in the neuronal substrate of dopamine replacement therapy (DRT). We investigated oscillatory activity and correlations throughout the different states of levodopa-naive parkinsonism as well as "Off-On" and dyskinetic states of DRT in the external globus pallidum (GPe) of tremulous (vervet) and rigid-akinetic (macaque) monkeys and in the internal globus pallidum (GPi) of the vervet monkey. We found that, although oscillatory activity of cells and interneuronal correlation in both pallidal segments increases after induction of parkinsonism with 1-methyl-4-phenyl-1,2,3,6-tetra-hydropyridine (MPTP) and decreases in response to DRT, important differences exist between the two pallidal segments. In the GPi, the fraction of oscillatory cells and relative power of oscillations were significantly higher than in the GPe, and the dominant frequency was within the range of 7.5-13.5 Hz compared with a range of 4.5-7.5 Hz within the GPe. The interneuronal correlations were mostly oscillatory in the GPi, whereas at least half are non-oscillatory in the GPe. We demonstrate that the tremor characteristics after exposure to DRT do not resemble those of the normal or the levodopa-naive state. Moreover, although DRT reverses the MPTP-induced neuronal changes (rate, pattern, and pairwise correlations), the balance between GPe and GPi fails to restore. We therefore suggest that this imbalance reflects additional abnormal organization of the basal ganglia networks in response to dopamine replacement and may constitute the physiological substrate of the limitations and side effects of chronic DRT.

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“…Parkinsonian tremor appears to be generated by oscillatory neuronal activity in the theta band (3-7 Hz) in segregated networks associated with different limbs shaking with time-varying phase and frequency differences [39][40][41][42][43][44]. Tremor-related theta band oscillations are typically no pronounced feature in LFP recordings, presumably since different neuronal subpopulations belonging to different limbs oscillate with time varying phase and frequency relationships [41,43,44].…”

Section: Discussionmentioning

confidence: 99%

Suppression of spontaneous oscillations in high-frequency stimulated neuron models

Pyragas¹,

Tass²

2017

Lith. J. Phys.

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We analyze the influence of high-frequency current stimulation on spontaneous neuronal activity and show that it may cause a death of spontaneous low-frequency oscillations. We demonstrate the universality of this effect for typical neuron models such as FitzHugh-Nagumo, Morris-Lecar, and Hodgkin-Huxley neurons as well as for the normal form of the supercritical Hopf bifurcation. Using a multiple scale method we separate the solutions of the neuron equations into slow and fast components and derive averaged equations for the slow components. The mechanism of suppression of neuronal activity is explained by an analysis of the bifurcations in the averaged equations governing the dynamics of the slow motion. Our results may contribute to the understanding of therapeutic effects of high-frequency deep brain stimulation, the golden standard for the treatment of medically refractory patients suffering from Parkinson's disease. Furthermore, our study enables hypotheses concerning possible improvements of high-frequency deep brain stimulation.

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Synchrony of rest tremor in multiple limbs in Parkinson's disease: evidence for multiple oscillators

Cited by 65 publications

References 21 publications

Increased Gamma Oscillatory Activity in the Subthalamic Nucleus During Tremor in Parkinson's Disease Patients

Increased Gamma Oscillatory Activity in the Subthalamic Nucleus During Tremor in Parkinson's Disease Patients

Dopamine Replacement Therapy Does Not Restore the Full Spectrum of Normal Pallidal Activity in the 1-Methyl-4-Phenyl-1,2,3,6-Tetra-Hydropyridine Primate Model of Parkinsonism

Suppression of spontaneous oscillations in high-frequency stimulated neuron models

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