Subthalamic Beta-targeted Neurofeedback Speeds Up Movement Initiation but Increases Tremor in Parkinsonian Patients

Overview

Journal Elife

Specialty Biology

Date 2020 Nov 18

PMID 33205752

Citations 10

Authors

Shenghong He

Abteen Mostofi

Emilie Syed

Flavie Torrecillos

Gerd Tinkhauser

Petra Fischer

Alek Pogosyan

Harutomo Hasegawa

Yuanqing Li

Keyoumars Ashkan

Erlick Pereira

Peter Brown

Huiling Tan

Affiliations

Soon will be listed here.

Abstract

Previous studies have explored neurofeedback training for Parkinsonian patients to suppress beta oscillations in the subthalamic nucleus (STN). However, its impacts on movements and Parkinsonian tremor are unclear. We developed a neurofeedback paradigm targeting STN beta bursts and investigated whether neurofeedback training could improve motor initiation in Parkinson's disease compared to passive observation. Our task additionally allowed us to test which endogenous changes in oscillatory STN activities are associated with trial-to-trial motor performance. Neurofeedback training reduced beta synchrony and increased gamma activity within the STN, and reduced beta band coupling between the STN and motor cortex. These changes were accompanied by reduced reaction times in subsequently cued movements. However, in Parkinsonian patients with pre-existing symptoms of tremor, successful volitional beta suppression was associated with an amplification of tremor which correlated with theta band activity in STN local field potentials, suggesting an additional cross-frequency interaction between STN beta and theta activities.

Citing Articles

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References

Legenstein R, Pecevski D, Maass W . A learning theory for reward-modulated spike-timing-dependent plasticity with application to biofeedback. PLoS Comput Biol. 2008; 4(10):e1000180. PMC: 2543108. DOI: 10.1371/journal.pcbi.1000180. View

Ros T, Baars B, Lanius R, Vuilleumier P . Tuning pathological brain oscillations with neurofeedback: a systems neuroscience framework. Front Hum Neurosci. 2015; 8:1008. PMC: 4270171. DOI: 10.3389/fnhum.2014.01008. View

Thibault R, Lifshitz M, Raz A . The self-regulating brain and neurofeedback: Experimental science and clinical promise. Cortex. 2015; 74:247-61. DOI: 10.1016/j.cortex.2015.10.024. View

Little S, Brown P . Debugging Adaptive Deep Brain Stimulation for Parkinson's Disease. Mov Disord. 2020; 35(4):555-561. PMC: 7166127. DOI: 10.1002/mds.27996. View

He S, Everest-Phillips C, Clouter A, Brown P, Tan H . Neurofeedback-Linked Suppression of Cortical β Bursts Speeds Up Movement Initiation in Healthy Motor Control: A Double-Blind Sham-Controlled Study. J Neurosci. 2020; 40(20):4021-4032. PMC: 7219286. DOI: 10.1523/JNEUROSCI.0208-20.2020. View

Little S, Beudel M, Zrinzo L, Foltynie T, Limousin P, Hariz M . Bilateral adaptive deep brain stimulation is effective in Parkinson's disease. J Neurol Neurosurg Psychiatry. 2015; 87(7):717-21. PMC: 4941128. DOI: 10.1136/jnnp-2015-310972. View

Lofredi R, Neumann W, Bock A, Horn A, Huebl J, Siegert S . Dopamine-dependent scaling of subthalamic gamma bursts with movement velocity in patients with Parkinson's disease. Elife. 2018; 7. PMC: 5819947. DOI: 10.7554/eLife.31895. View

Houston B, Thompson M, Ko A, Chizeck H . A machine-learning approach to volitional control of a closed-loop deep brain stimulation system. J Neural Eng. 2018; 16(1):016004. DOI: 10.1088/1741-2552/aae67f. View

Fischer P, Pogosyan A, Cheeran B, Green A, Aziz T, Hyam J . Subthalamic nucleus beta and gamma activity is modulated depending on the level of imagined grip force. Exp Neurol. 2017; 293:53-61. PMC: 5429975. DOI: 10.1016/j.expneurol.2017.03.015. View

10.

Tan H, Wade C, Brown P . Post-Movement Beta Activity in Sensorimotor Cortex Indexes Confidence in the Estimations from Internal Models. J Neurosci. 2016; 36(5):1516-28. PMC: 4737767. DOI: 10.1523/JNEUROSCI.3204-15.2016. View

11.

Peles O, Werner-Reiss U, Bergman H, Israel Z, Vaadia E . Phase-Specific Microstimulation Differentially Modulates Beta Oscillations and Affects Behavior. Cell Rep. 2020; 30(8):2555-2566.e3. DOI: 10.1016/j.celrep.2020.02.005. View

12.

Hirschmann J, Hartmann C, Butz M, Hoogenboom N, Ozkurt T, Elben S . A direct relationship between oscillatory subthalamic nucleus-cortex coupling and rest tremor in Parkinson's disease. Brain. 2013; 136(Pt 12):3659-70. DOI: 10.1093/brain/awt271. View

13.

McFarland D, Sarnacki W, Wolpaw J . Effects of training pre-movement sensorimotor rhythms on behavioral performance. J Neural Eng. 2015; 12(6):066021. PMC: 4843806. DOI: 10.1088/1741-2560/12/6/066021. View

14.

Sitaram R, Ros T, Stoeckel L, Haller S, Scharnowski F, Lewis-Peacock J . Closed-loop brain training: the science of neurofeedback. Nat Rev Neurosci. 2016; 18(2):86-100. DOI: 10.1038/nrn.2016.164. View

15.

Torrecillos F, Tinkhauser G, Fischer P, Green A, Aziz T, Foltynie T . Modulation of Beta Bursts in the Subthalamic Nucleus Predicts Motor Performance. J Neurosci. 2018; 38(41):8905-8917. PMC: 6181312. DOI: 10.1523/JNEUROSCI.1314-18.2018. View

16.

Qasim S, de Hemptinne C, Swann N, Miocinovic S, Ostrem J, Starr P . Electrocorticography reveals beta desynchronization in the basal ganglia-cortical loop during rest tremor in Parkinson's disease. Neurobiol Dis. 2015; 86:177-86. PMC: 4842026. DOI: 10.1016/j.nbd.2015.11.023. View

17.

Neumann W, Degen K, Schneider G, Brucke C, Huebl J, Brown P . Subthalamic synchronized oscillatory activity correlates with motor impairment in patients with Parkinson's disease. Mov Disord. 2016; 31(11):1748-1751. PMC: 5120686. DOI: 10.1002/mds.26759. View

18.

Carney R . Neurofeedback Training Enables Voluntary Alteration of β-Band Power in the Subthalamic Nucleus of Individuals with Parkinson's Disease. eNeuro. 2019; 6(2). PMC: 6498418. DOI: 10.1523/ENEURO.0144-19.2019. View

19.

Tinkhauser G, Torrecillos F, Pogosyan A, Mostofi A, Bange M, Fischer P . The Cumulative Effect of Transient Synchrony States on Motor Performance in Parkinson's Disease. J Neurosci. 2020; 40(7):1571-1580. PMC: 7044725. DOI: 10.1523/JNEUROSCI.1975-19.2019. View

20.

Tinkhauser G, Pogosyan A, Tan H, Herz D, Kuhn A, Brown P . Beta burst dynamics in Parkinson's disease OFF and ON dopaminergic medication. Brain. 2017; 140(11):2968-2981. PMC: 5667742. DOI: 10.1093/brain/awx252. View