Persistent suppression of subthalamic beta-band activity during rhythmic finger tapping in Parkinson’s disease

Joundi, Raed A.; Brittain, John-Stuart; Green, Alex L.; Aziz, Tipu Z.; Brown, Peter; Jenkinson, Ned

doi:10.1016/j.clinph.2012.07.029

Cited by 61 publications

(39 citation statements)

References 55 publications

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“…At pacing rates near to and above 2 Hz the pattern of desynchronization-synchronization was markedly attenuated and there was a persistent suppression of alpha and beta oscillations below baseline levels. Although this transition in MRO pattern from lower (< 2 Hz) to higher rate (> 2 Hz) movements has been described for both scalp surface EEG recordings in healthy adults (Toma et al, 2002) and local field potential recordings of the subthalamic nucleus (STN) in patients with PD (Joundi et al, 2013), this study is the first to show distinct differences between participants with PD and matched control participants. The principal difference in MROs between PD and control groups was the mean level of power relative to baseline (rest) in both the alpha and beta bands.…”

Section: Discussionmentioning

confidence: 60%

“…At pacing rates near 2 Hz, movements become out of phase with the cue and cortical activity transitions to a pattern of near continuous desynchronization (Toma et al, 2002; Muthukumaraswamy, 2010). Local field potential recordings from deep brain stimulation electrodes implanted in the subthalamic nucleus (STN) of persons with PD have shown a similar pattern of changes in desynchronization-synchronization when transitioning from low to higher rate movements (Androulidakis et al, 2008; Hebb et al, 2012; Joundi et al, 2013). Movements near 2 Hz were associated with a reduction in beta band modulation and a concomitant worsening of finger tapping performance, suggesting that alterations in the capacity to modulate beta oscillations was linked to impairment (Androulidakis et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

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Motor cortical oscillations are abnormally suppressed during repetitive movement in patients with Parkinson’s disease

Stegemöller

Allen

Simuni

et al. 2016

Clinical Neurophysiology

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Objective Impaired repetitive movement in persons with Parkinson's disease (PD) is associated with reduced amplitude, paradoxical hastening and hesitations or arrest at higher movement rates. This study examined the effects of movement rate and medication on movement-related cortical oscillations in persons with PD. Methods Nine participants with PD were studied off and on medication and compared to nine control participants. Participants performed index finger movements cued by tones from 1 to 3 Hz. Movement-related oscillations were derived from electroencephalographic recordings over the region of the contralateral senorimotor cortex (S1/M1) during rest, listening, or synchronized movement. Results At rest, spectral power recorded over the region of the contralateral S1/M1 was increased in the alpha band and decreased in the beta band in participants with PD relative to controls. During movement, the level of alpha and beta band power relative to baseline was significantly reduced in the PD group, off and on medication, compared to controls. Reduced movement amplitude and hastening at movement rates near 2 Hz was associated with abnormally suppressed and persistent desynchronization of oscillations in alpha and beta bands. Conclusion Motor cortical oscillations in the alpha and beta bands are abnormally suppressed in PD, particularly during higher rate movements. Significance These findings contribute to the understanding of mechanisms underlying impaired repetitive movement in PD.

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Section: Discussionmentioning

confidence: 60%

Section: Introductionmentioning

confidence: 99%

Motor cortical oscillations are abnormally suppressed during repetitive movement in patients with Parkinson’s disease

Stegemöller

Allen

Simuni

et al. 2016

Clinical Neurophysiology

View full text Add to dashboard Cite

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“…Modulation of beta range activity in association with movement has been extensively explored in the basal ganglia of PD patients and its significance remains a subject of ongoing interest (Cassidy et al, 2002;Doyle et al, 2005;Florin et al, 2013;Foffani et al, 2005a;Hirschmann et al, 2013;Jenkinson and Brown, 2011;Joundi et al, 2013;Kempf et al, 2007;Kuhn et al, 2004;Priori et al, 2002;Wingeier et al, 2006). The exaggerated high beta/low gamma activity in the SNpr of the hemiparkinsonian rats appears most prominent during periods when the rats are executing repetitive movements, such as walking or grooming.…”

Section: Discussionmentioning

confidence: 99%

Functional correlates of exaggerated oscillatory activity in basal ganglia output in hemiparkinsonian rats

Brazhnik¹,

Novikov²,

McCoy³

et al. 2014

Experimental Neurology

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Exaggerated beta range (13–30 Hz) synchronized activity is observed in the basal ganglia of Parkinson’s disease (PD) patients during implantation of deep brain stimulation electrodes and is thought to contribute to the motor symptoms of this disorder. To explore the translational potential of similar activity observed in a rat model of PD, local field potentials (LFP) and spiking activity in basal ganglia output were characterized in rats with unilateral dopamine cell lesion during a range of behaviors. A circular treadmill was used to assess activity during walking; hemiparkinsonian rats could maintain a steady gait when oriented ipsiversive to the lesioned hemisphere, but were less effective at walking when oriented contraversive to lesion. Dramatic increases in substantia nigra pars reticulata (SNpr) LFP oscillatory activity and spike-LFP synchronization were observed within the beta/low gamma range (12–40 Hz) in the lesioned hemisphere, relative to the non-lesioned hemisphere, with the dominant frequency of spike-LFP entrainment and LFP power varying with behavioral state. At 3 weeks post-lesion, the mean dominant entrainment frequency during ipsiversive treadmill walking and grooming was 34 Hz. Other behaviors were associated with lower mean entrainment frequencies: 27–28 Hz during alert non-walking and REM, 17 Hz during rest and 21 Hz during urethane anesthesia with sensory stimulation. SNpr spike-LFP entrainment frequency was stable during individual treadmill walking epochs, but increased gradually over weeks post-lesion. In contrast, SNpr LFP power in the 25–40 Hz range was greatest at the initiation of each walking epoch, and decreased during walking to stabilize by 6 min at 49% of initial values. Power was further modulated in conjunction with the 1.5 s stepping rhythm. Administration of L-dopa improved contraversive treadmill walking in correlation with a reduction in SNpr 25–40 Hz LFP power and spike synchronization in the dopamine cell lesioned hemisphere. These effects were reversed by the serotonergic 1A agonist, 8-OH-DPAT. While the prominent spike-LFP phase locking observed during ongoing motor activity in the hemiparkinsonian rats occurs at frequencies intriguingly higher than in PD patients, the synchronized activity in the SNpr of this animal model has much in common with oscillatory activity recorded from the basal ganglia of the PD patients. Results support the potential of this model for providing insight into relationships between synchronization of basal ganglia output induced by loss of dopamine and motor symptoms in PD.

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“…Patients are not commonly engaged in motor activity as vigorous as treadmill walking while being recorded. Although motor activity is increasingly being taken into consideration in studies with PD patients [60], it is still not clear exactly how firing patterns in the basal ganglia would be affected during effort to overcome difficulties in gait.…”

Section: Introductionmentioning

confidence: 99%

Oscillatory activity in basal ganglia and motor cortex in an awake behaving rodent model of Parkinson's disease

et al. 2014

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Exaggerated beta range (15-30 Hz) oscillatory activity is observed in the basal ganglia of Parkinson's disease (PD) patients during implantation of deep brain stimulation electrodes. This activity has been hypothesized to contribute to motor dysfunction in PD patients. However, it remains unclear how these oscillations develop and how motor circuits become entrained into a state of increased synchronization in this frequency range after loss of dopamine. It is also unclear whether this increase in neuronal synchronization actually plays a significant role in inducing the motor symptoms of this disorder. The hemiparkinsonian rat has emerged as a useful model for investigating relationships between loss of dopamine, increases in oscillatory activity in motor circuits and behavioral state. Chronic recordings from these animals show exaggerated activity in the high beta/low gamma range (30-35 Hz) in the dopamine cell-lesioned hemisphere. This activity is not evident when the animals are in an inattentive rest state, but it can be stably induced and monitored in the motor cortex and basal ganglia when they are engaged in an on-going activity such as treadmill walking. This review discusses data obtained from this animal model and the implications and limitations of this data for obtaining further insight into the significance of beta range activity in PD.

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Persistent suppression of subthalamic beta-band activity during rhythmic finger tapping in Parkinson’s disease

Cited by 61 publications

References 55 publications

Motor cortical oscillations are abnormally suppressed during repetitive movement in patients with Parkinson’s disease

Motor cortical oscillations are abnormally suppressed during repetitive movement in patients with Parkinson’s disease

Functional correlates of exaggerated oscillatory activity in basal ganglia output in hemiparkinsonian rats

Oscillatory activity in basal ganglia and motor cortex in an awake behaving rodent model of Parkinson's disease

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