EDITORIAL article

Front. Hum. Neurosci., 17 May 2023

Sec. Brain Imaging and Stimulation

Volume 17 - 2023 | https://doi.org/10.3389/fnhum.2023.1211465

Editorial: The role of the basal ganglia in somatosensory-motor interactions: evidence from neurophysiology and behavior, volume II

  • 1. Department of Neurology, Amsterdam UMC, Amsterdam Neuroscience, University of Amsterdam, Amsterdam, Netherlands

  • 2. The Department of Pharmacology and Therapeutics, Institute of Systems, Molecular and Integrative Biology, University of Liverpool, Liverpool, United Kingdom

  • 3. The Walton Centre NHS Foundation Trust, Liverpool, United Kingdom

  • 4. Department of Kinesiology, California State University Sacramento, Sacramento, CA, United States

  • 5. Division of Neurology, Department of Medicine, University of Toronto, Toronto, ON, Canada

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In the second edition of the Research Topic, named “The role of the basal ganglia in somatosensory-motor interactions: evidence from neurophysiology and behavior II,” seven articles have been published. All seven contributions consisted of original work. Interestingly, each article used a unique approach (see Table 1) to study basal-ganglia function varying from psychophysics (Sengupta et al.) to invasive micro-electrode recordings (MER, Filyushkina et al.). This heterogeneity of approaches is in line with the approaches described in its predecessor (Beudel et al., 2020).

Table 1

ReferencesType(Brief) title(Unique) techniqueDisease
Basha et al.OriginalBeta band oscillations in the motor thalamusLFPET/PD
Campbell et al.OriginalThe impact of pulse timing on cortical and subthalamic nucleus deep brain stimulation evoked potentialsEEGPD
Chen et al.OriginalDisrupted Brain Structural Network Connection in de novo Parkinson's disease with RBDDTI(RBD) PD
Filyushkina et al.OriginalAttenuation of neural responses in subthalamic nucleus during internally guided voluntary movements in Parkinson's diseaseMERPD
Lan et al.OriginalFunctional connectivity of the basal ganglia subregions in pain syndromesResting state fMRIPain syndrome
Pinky et al.OriginalMultimodal magnetic resonance imaging of youth sport-related concussionMultimodal MRITBI
Sengupta et al.OriginalExploration of sensory-motor tradeoff behavior in Parkinson's diseasePsychophysicsPD

Overview of the published articles.

LFP, local field potential; ET, essential tremor; PD, Parkinson's disease; EEG, electro-encephalography; RBD, rapid eye movement sleep behavior disorder; DTI, diffusion tensor imaging; MER, micro electrode recording; fMRI, functional magnetic resonance imaging; TBI, traumatic brain injury.

One important question is whether the approaches used in the current edition were available in the era of the first edition (2019–2020). Although 3 years seems a short period, as we know after the pandemic, a lot can happen. One important development in studying the basal ganglia over the last 3 years is the availability of commercially available DBS devices by at least three companies that can record local field potentials (LFP's) from fully implanted devices (Chen et al., 2020; Marceglia et al., 2022; Stam et al., 2023). However, despite these developments, initial explorations have mainly focused on the feasibility of using this new technique before research programs will adapt toward LFP recordings from fully implantable DBS devices. At this moment, certain limitations in this technology are still present. For example, sampling frequencies are still restricted to 256 Hz by some devices, which makes it impossible to perform the pulse-timing work at the millisecond scale by Campbell et al. and the MER work by Filyushkina et al.. In theory, the third study that made use of subcortical recordings and studied the beta band (13–30 Hz) in the thalamus (Basha et al.), could have made use of the currently available fully-implantable devices that have also been able to record LFP activity in the thalamus (Buijink et al., 2022). Since LFP recordings from fully-implantable devices offer many advantages such as the possibility to record for longer periods and to apply adaptive stimulation paradigms (Nakajima et al., 2021), it is expected that the field will adapt this technology in the coming years.

Next to the applied methods in the Research Topic, the diseases studied are also noteworthy. Although the role of the basal ganglia in movement disorders has been studied extensively, this is far less the case for (urologic) pain syndromes and traumatic brain injury (TBI) as respectively described by Lan et al. and Pinky et al.. The findings of the study by Lan et al. further illustrate the role of the basal ganglia in pathological somatosensory-motor interactions in abnormal sensations (i.e., pain) and Pinky et al. studied the role of the caudate as modulator in the recovery of TBI. These insights show how studying basal-ganglia functions beyond movement disorders can help in developing neuro-modulation strategies and the development of (image-based) biomarkers. The development of biomarkers is also relevant for the prodromal stages of Parkinson's disease (PD) such as in patients with rapid eye movement sleep behavior disorder (RBD), which are at a higher risk for developing PD. By identifying these patients using advanced imaging approaches, such as described by Chen et al., patients may benefit in the future from disease- modifying therapies before the onset of motor symptoms (Athauda et al., 2019).

Although these insights from imaging studies comparing patient populations with controls are valuable for the reasons mentioned above, they lack a behavioral component showing how altered (network) processing actually leads to disturbed basal-ganglia function. In their contribution Sengupta et al. show the nature of response disinhibition in PD during natural movement performance whilst (Filyushkina et al.) were able to distinguish neural patterns of self-initiated vs externally cued response in the STN. With the dawn of DBS stimulation paradigms that influence decision making processes (Ghahremani et al., 2018; Herz et al., 2018), it is of utmost relevance to understand the basal-ganglia contributions underlying autonomous action selecting and its interference by either diseases (e.g., PD) or therapies (e.g., DBS).

Statements

Author contributions

All authors contributed to the editorial and have seen all revisions, including the final revision.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher’s note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

References

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    AthaudaD.MaclaganK.BudnikN.ZampedriL.HibbertS.Aviles-OlmosI.et al. (2019). Post hoc analysis of the exenatide-PD trial—factors that predict response. Eur. J. Neurosci. 49, 410421. 10.1111/ejn.14096

  • 2

    BeudelM.MacerolloA.BrownM. J. N.ChenR. (2020). Editorial: The role of the basal ganglia in somatosensory-motor interactions: evidence from neurophysiology and behavior. Front. Hum. Neurosci. 13, 451. 10.3389/fnhum.2019.00451

  • 3

    BuijinkA. W. G.Piña-FuentesD. A.StamM. J.BotM.SchuurmanP. R.van den MunckhofP.et al. (2022). Thalamic local field potentials recorded using the deep brain stimulation pulse generator. Clin. Neurophysiolo. Pract. 7, 103106. 10.1016/j.cnp.2022.03.002

  • 4

    ChenY.GongC.TianY.OrlovN.ZhangJ.GuoY.et al. (2020). Neuromodulation effects of deep brain stimulation on beta rhythm: a longitudinal local field potential study. Brain Stimul. 13, 17841792. 10.1016/j.brs.2020.09.027

  • 5

    GhahremaniA.AronA. R.UdupaK.SahaU.ReddyD.HutchisonW. D.et al. (2018). Event-related deep brain stimulation of the subthalamic nucleus affects conflict processing. Ann. Neurol.84, 515526. 10.1002/ana.25312

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    HerzD. M.LittleS.PedrosaD. J.TinkhauserG.CheeranB.FoltynieT.et al. (2018). Mechanisms underlying decision-making as revealed by deep-brain stimulation in patients with Parkinson's disease. Curr. Biol.28, 11691178.e6. 10.1016/j.cub.2018.02.057

  • 7

    MarcegliaS.ContiC.SvanidzeO.FoffaniG.LozanoA. M.MoroE.et al. (2022). Double-blind cross-over pilot trial protocol to evaluate the safety and preliminary efficacy of long-term adaptive deep brain stimulation in patients with Parkinson's disease. BMJ Open12, e049955. 10.1136/bmjopen-2021-049955

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    NakajimaA.ShimoY.FuseA.TokugawaJ.HishiiM.IwamuroH.et al. (2021). Case report: chronic adaptive deep brain stimulation personalizing therapy based on Parkinsonian state. Front. Hum. Neurosci. 15, 702961. 10.3389/fnhum.2021.702961

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    StamM. J.van WijkB. C. M.SharmaP.BeudelM.Piña-FuentesD. A.de BieR. M. A.et al. (2023). A comparison of methods to suppress electrocardiographic artifacts in local field potential recordings. Clin. Neurophysiol. 146, 147161. 10.1016/j.clinph.2022.11.011

Summary

Keywords

basal ganglia (BG), deep brain stimulation (DBS), micro electrode recording, local field potential (LFP), sensorimotor, traumatic brain injury (TBI), pain

Citation

Beudel M, Macerollo A, Brown MJN and Chen R (2023) Editorial: The role of the basal ganglia in somatosensory-motor interactions: evidence from neurophysiology and behavior, volume II. Front. Hum. Neurosci. 17:1211465. doi: 10.3389/fnhum.2023.1211465

Received

24 April 2023

Accepted

26 April 2023

Published

17 May 2023

Volume

17 - 2023

Edited and reviewed by

Mingzhou Ding, University of Florida, United States

Updates

Copyright

*Correspondence: Martijn Beudel

Disclaimer

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

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