Increases in oscillatory β activity in the basal ganglia are regarded as one of the main electrophysiological biomarkers of impaired motor control in Parkinson’s disease. The functional role of dynamic changes in rhythmic activity during movement execution is still not fully understood. Microelectrode recording analysis addressed rhythmic neuronal activity in the subthalamic nucleus in nine patients with Parkinson’s disease during neurosurgical operations to implant deep brain stimulation systems. The results revealed a significant positive correlation between the amplitudes of α (7–12 Hz) and low β (12–20 Hz) activity in the subthalamic nucleus and evaluations of motor symptoms in patients with Parkinson’s disease. The amplitude of rhythmic α activity, in contrast to that of β rhythms, was also found to decrease significantly when patients performed motor tests. Moreover, the extent of decreases in α activity correlated directly with the severity of bradykinesia. The results obtained suggest that, along with β activity, the rhythmic α-activity of neurons in the subthalamic nucleus also plays a role in motor control in patients with Parkinson’s disease.
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References
Alegre, M., Alonso-Frech, F., Rodríguez-Oroz, M. C., et al., “Movement-related changes in oscillatory activity in the human subthalamic nucleus: ipsilateral vs. contralateral movements,” Eur. J. Neurosci., 22, No. 9, 2315–2324 (2005).
Bate, D., Mächler, M., Bolker, B., and Walker, S., “Fitting linear mixed-effects models using lme4,” J. Stat. Softw., 67, No. 1, 1–48 (2015).
Belova, E. M., Semenova, U., Gamaleya, A. A., et al., “Is there a single beta oscillation band interfering with movement in Parkinson’s disease?” Eur. J. Neurosci., 54, No. 1, 4381–4391 (2021).
Bichsel, O., Gassert, R., Stieglitz, L., et al., “Functionally separated networks for self-paced and externally-cued motor execution in Parkinson’s disease: Evidence from deep brain recordings in humans,” NeuroImage, 177, 20–29 (2018).
Drebitz, E., Schledde, B., Kreiter, A. K., and Wegener, D., “Optimizing the yield of multi-unit activity by including the entire spiking activity,” Front. Neurosci., 13, 83.745 (2019).
Eisinger, R. S., Cagle, J. N., Opri, E., et al., “Parkinsonian beta dynamics during rest and movement in the dorsal pallidum and subthalamic nucleus,” J. Neurosci., 40, No. 14, 2859–2867 (2020).
Feldmann, L. K., Lofredi, R., Neumann, W.-J., et al., “Toward therapeutic electrophysiology: beta-band suppression as a biomarker in chronic local field potential recordings,” NPJ Park. Dis., 8, No. 1, 44 (2022).
Galvan, A. and Wichmann, T., “Pathophysiology of Parkinsonism,” Clin. Neurophysiol., 119, No. 7, 1459–1474 (2008).
Geng, X., Xu, X., Horn, A., et al., “Intra-operative characterisation of subthalamic oscillations in Parkinson’s disease,” Clin. Neurophysiol., 129, No. 5, 1001–1010 (2018).
Godinho, F., Fim Neto, A., Bianqueti, B. L., et al., “Spectral characteristics of subthalamic nucleus local fi eld potentials in Parkinson’s disease: Phenotype and movement matter,” Eur. J. Neurosci., 53, No. 8, 2804–2818 (2021).
Hammond, C., Bergman, H., and Brown, P., “Pathological synchronization in Parkinson’s disease: networks, models and treatments,” Trends Neurosci., 30, No. 7, 357–364 (2007).
Horn, A., Neumann, W.-J., Degen, K., et al., “Toward an electrophysiological “sweet spot” for deep brain stimulation in the subthalamic nucleus,” Hum. Brain Mapp., 38, No. 7, 3377–3390 (2017).
Khawaldeh, S., Tinkhauser, G., Shah, S. A., et al., “Subthalamic nucleus activity dynamics and limb movement prediction in Parkinson’s disease,” Brain, 143, No. 2, 582–596 (2020).
Kuhn, A. A., Kempf, F., Brucke, C., et al., “High-frequency stimulation of the subthalamic nucleus suppresses oscillatory activity in patients with Parkinson’s disease in parallel with improvement in motor performance,” J. Neurosci., 28, No. 24, 6165–6173 (2008).
Kühn, A. A., Kupsch, A., Schneider, G.-H., and Brown, P., “Reduction in subthalamic 8–35 Hz oscillatory activity correlates with clinical improvement in Parkinson’s disease: STN activity and motor improvement,” Eur. J. Neurosci., 23, No. 7, 1956–1960 (2006).
Kühn, A. A., Trottenberg, T., Kivi, A., et al., “The relationship between local field potential and neuronal discharge in the subthalamic nucleus of patients with Parkinson’s disease,” Exp. Neurol., 194, No. 1, 212–220 (2005).
Kühn, A. A., Tsui, A., Aziz, T., et al., “Pathological synchronisation in the subthalamic nucleus of patients with Parkinson’s disease relates to both bradykinesia and rigidity,” Exp. Neurol., 215, No. 2, 380–387 (2009).
Kuznetsova, A., Brockhof, P. B., and Christensen, R. H. B., “lmerTest package: tests in linear mixed effects models,” J. Stat. Softw., 1, No. 13, 1–26 (2017).
Little, S., Pogosyan, A., Neal, S., et al., “Adaptive deep brain stimulation in advanced Parkinson disease,” Ann. Neurol., 74, No. 3, 449–457 (2013).
Lofredi, R., Tan, H., Neumann, W.-J., et al., “Beta bursts during continuous movements accompany the velocity decrement in Parkinson’s disease patients,” Neurobiol. Dis., 127, 462–471 (2019).
Marmor, O., Rappel, P., Valsky, D., et al., “Movement context modulates neuronal activity in motor and limbic-associative domains of the human parkinsonian subthalamic nucleus,” Neurobiol. Dis., 136, 104716 (2020).
Moran, A. and Bar-Gad, I., “Revealing neuronal functional organization through the relation between multi-scale oscillatory extracellular signals,” J. Neurosci. Meth., 186, No. 1, 116–129 (2010).
Neumann, W.-J., Degen, K., Schneider, G.-H., et al., “Subthalamic synchronized oscillatory activity correlates with motor impairment in patients with Parkinson’s disease: Correlation of subthalamic β oscillations and PD symptoms,” Mov. Disord., 31, No. 11, 1748–1751 (2016).
Neuville, R. S., Petrucci, M. N., Wilkins, K. B., et al., “Differential effects of pathological beta burst dynamics between Parkinson’s disease phenotypes across different movements,” Front. Neurosci., 15, 733203 (2021).
Oswal, A., Beudel, M., Zrinzo, L., et al., “Deep brain stimulation modulates synchrony within spatially and spectrally distinct resting state networks in Parkinson’s disease,” Brain, 139, No. 5, 1482–1496 (2016).
Oswal, A., Brown, P., and Litvak, V., “Movement related dynamics of subthalamo-cortical alpha connectivity in Parkinson’s disease,” NeuroImage, 70, 132–142 (2013).
Rappel, P., Grosberg, S., Arkadir, D., et al., “Theta-alpha oscillations characterize emotional subregion in the human ventral subthalamic nucleus,” Mov. Disord., 35, No. 2, 337–343 (2020).
Scherer, M., Steiner, L. A., Kalia, S. K., et al., “Single-neuron bursts encode pathological oscillations in subcortical nuclei of patients with
Parkinson’s disease and essential tremor,” Proc. Natl. Acad. Sci. USA, 119, No. 35 (2022).
Sharott, A., Gulberti, A., Zittel, S., et al., “Activity parameters of subthalamic nucleus neurons selectively predict motor symptom severity in Parkinson’s disease,” J. Neurosci., 34, No. 18, 6273–6285 (2014).
Steiner, L. A., Neumann, W.-J., Staub-Bartelt, F., et al., “Subthalamic beta dynamics mirror Parkinsonian bradykinesia months after neurostimulator implantation: STN Beta Dynamics Mirror Parkinsonian Bradykinesia,” Mov. Disord., 32, No. 8, 1183–1190 (2017).
Tinkhauser, G., Pogosyan, A., Tan, H., et al., “Beta burst dynamics in Parkinson’s disease OFF and ON dopaminergic medication,” Brain, 140, No. 11, 2968–2981 (2017a).
Tinkhauser, G., Pogosyan, A., Little, S., et al., “The modulatory effect of adaptive deep brain stimulation on beta bursts in Parkinson’s disease,” Brain, 140, No. 4, 1053–1067 (2017b).
van Wijk, B. C. M., Neumann, W.-J., Kroneberg, D., et al., “Functional connectivity maps of theta/alpha and beta coherence within the subthalamic nucleus region,” NeuroImage, 257, 119320 (2022).
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Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 73, No. 6, pp. 725–734, November–December, 2023.
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Nezvinskiy, A.A., Belova, E.M., Sayfulina, K.E. et al. The Relationship between the Rhythmic Alpha Activity of the Subthalamic Nucleus and Motor Symptoms in Patients with Parkinson’s Disease. Neurosci Behav Physi 54, 263–269 (2024). https://doi.org/10.1007/s11055-024-01594-x
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DOI: https://doi.org/10.1007/s11055-024-01594-x