Freudenburg, Zachary V

Leijten, Frans S S

Ramsey, Nick F

Schippers, Anouck

Vansteensel, Mariska J

Utrecht University Repository

lable at ScienceDirectBrain Stimulation 14 (2021) 287e289Contents lists avaiBrain Stimulationjournal homepage: http: / /www.journals .e lsevier .com/brain-st imulat ionDetailed somatotopy of tongue movement in the human sensorimotorcortex: A case study1. IntroductionDespite substantial evidence for a representation of body parts inthe sensorimotor cortex (SMC) [1], mapping of more detailed motorfunction in this brain area remains elusive. While some report anorderly somatotopic representation of individual fingers and articu-lators in the SMC [2,3], others demonstrate that such within-body-parts have overlapping neural representations [4,5], which suggestsa lack of discrete organization of within-body-part representations.Imaging techniques that are typically used to investigate brainfunction (e.g., fMRI) do not distinguish between critical and non-critical functionality. Observed activity with such techniques canthus represent non-essential involvement such as motor planningor a feedforward/efferent copy. Contrarily, electrical stimulationof the cortex elucidates only areas critical for execution of brainfunctions and thus allows for studying movement representationin isolation. Here, we applied cortical stimulation on a high-density (HD) electrocorticography (ECoG) electrode grid in a neuro-surgical patient to investigate the detailed representation of motorfunction on the SMC, following ECoG mapping of the tongue.2. Materials and methodsThe patient (male, 28 years-old) suffered from focal seizureswith impaired awareness. Seizures were medically refractory andMRI was negative. For epilepsy monitoring purposes and mappingof brain function prior to epilepsy surgery, subdural ECoG gridswere implanted for one week, including an HD-grid (64 channels,3 mm center-to-center electrode distance, 1 mm diameter, Ad-Tech Medical Instrument Corp) over the right ventral SMC. Elec-trode localization on the cortex (Fig. 1A) was performed using pro-cedures described earlier [6]. Informed consent was signed prior tostudy participation and consent for sharing footage of the lowerpart of the face was obtained retrospectively. The study was con-ducted according to the Declaration of Helsinki (2013).The patient performed a tongue movement task while ECoGdata was recorded from the HD-grid (sampling rate 512 Hz, 22bits, band-pass filter 0.15e134.4 Hz, Micromed, Italy). The patientwas instructed (visually on a computer screen placed at approxi-mately 1 m distance) to move his tongue horizontally inside hismouth, imagine making this movement, or relax during sixteen-second trials. These three conditions were repeated ten timeseach in random order. Here, we only considered the trials withexecuted tongue movements and rest trials.Task-related ECoG data from the HD grid was preprocessed usingmultiple steps. First, identification of electrodes with noisy or flathttps://doi.org/10.1016/j.brs.2021.01.0101935-861X/© 2021 The Author(s). Published by Elsevier Inc. This is an open access articchannels was carried out by identifying electrodes with deviationsin the power-density distribution, line noise values, and raw voltagedistributions (identifying the four corner reference electrodes whichwere facing the dura and which were not used in subsequent anal-ysis steps). Second, a 50 Hz notch filter was applied and data wascommon average-referenced. Subsequently, high-frequency band(HFB, 65e95 Hz) power was computed per electrode and samplepoint as described earlier [7]. The HFB power traces were dividedinto trials, and HFB power per trial was averaged over time for allelectrodes. The average HFB responses were compared betweenexecuted movement and rest conditions by computing the coeffi-cient of determination (R2 value) per electrode.Subsequently, clinical bipolar stimulation was administered(IRES 600 CH electrical stimulator, Micromed, Italy; 1 s trains of50 Hz, 2 mA, 0.1 ms biphasic square pulses) to twelve electrodepairs (of adjacent electrodes) of the HD grid that showed signifi-cantly increased activation during tongue movements as comparedto rest. Administered charge density per phase was kept below thesafety limit and was similar for all electrode pairs. Stimulation wasnot administered to the seizure onset location (mesiotemporal,medial temporal gyrus, and posterior temporobasal). Video record-ingsweremade of the patients’ face to visuallymonitor the physicaleffects of the stimulation, and the patient was asked to verballyreport any sensation and/or movement he experienced.3. ResultsElectrodes with significantly increased activity during move-ment compared to rest (p < .05, Bonferroni corrected) were locatedboth anterior and posterior to the central sulcus, with the highestresponses occurring more anteriorly (Fig. 1B).Stimulation of the twelve HD electrode pairs resulted in atongue movement in one of three directions, or in no movement(Fig. 1C). Notably, electrode pairs that resulted in tonguemovementin one direction upon stimulation were only 3 mm removed fromelectrode pairs that, when stimulated, resulted in tongue move-ment in another direction (Fig. 1D, Supplementary Video 1).Supplementary video related to this article can be found athttps://doi.org/10.1016/j.brs.2021.01.0104. DiscussionWe show that the ventral sensorimotor cortex contains a repre-sentation of different tongue movements at a detailed, millimeterscale. The clearly separated tongue movements that were inducedle under the CC BY license (http://creativecommons.org/licenses/by/4.0/).Fig. 1. Visualization of electrodes and neural representations of spontaneous and evoked movements.Black outlines within subfigures A, B, and C highlight the group of electrodes shown in the consecutive subfigure. A) Visualization of the HD-ECoG grid on the cortex with individualelectrodes in blue and the central sulcus in black. B) Visualization of significant HFB power changes related to movement versus rest conditions for the tongue movement task.Electrodes are colored according to their respective R2 values. Electrodes depicted in grey indicate non-significant R2 values. C) Visualization of stimulation results. Stimulationlocations that did not lead to movement are depicted with yellow dots. Arrows indicate the movement direction (based on the perspective of the observer) of the tongue in the left(red), right (blue), or upwards (green) direction as a response to stimulation over the two electrodes between which the arrow is visualized between which the arrow is locationedD) Visualization of three different tongue movements upon stimulation of three different pairs within a 3-mm radius around the central electrode. Starting position of the tonguewas outside of the mouth.A. Schippers, M.J. Vansteensel, Z.V. Freudenburg et al. Brain Stimulation 14 (2021) 287e289by stimulation of different, but neighboring, electrode pairs suggestthat different motor programs of a single body part each have theirown representation on the cortex, suggesting such a detailed orga-nization could be found for other body parts as well.Our findings are in line with previous findings that showed adetailed representation of within-limbmovements [2,3] but exposean unexpectedly detailed level of spatially separable representa-tions. This finding contributes new evidence to the long-standingdebate about segregation of detailed motor programs in the SMC.Interestingly, electrodes showing a significant response duringvoluntary left-right tongue movements overlapped with, but weremore spatially widespread than, electrodes that evoked left-righttongue movements upon stimulation. This observation confirmsthe notion that measurements of neural representations of volun-tary movements unveil more areas than only those representingcritical motor processes, while cortical stimulation does succeedin unveiling those critical areas.During spontaneous movement, we found the highest HFBresponse anterior in the inferior postcentral gyrus, i.e., on the so-matosensory cortex. This is in line with neurosurgical experience,which indicates a less strict separation between motor and sensoryfunction than generally assumed, possibly associated with inter-individual variation [1,8].To our knowledge, our findings represent the first support forthe existence of a detailed, distinct mototopy in the tongue area288of the sensorimotor cortex. Also, this case study illustrates thatcortical mapping with high-density grids is feasible and representsan interesting technique for distinct and detailed localization ofmotor function, only elucidating areas critical for movement execu-tion at high spatial detail. We propose that further investigationinto detailed mapping of within-body-part representations willrequire spatial specificity in the order of millimeters.Declaration of competing interestNone.AcknowledgementsWe would like to thank Erik Aarnoutse for his help with dataacquisition, the clinical staff for their contribution to the experi-ment, and the subject for his willingness to participate.Study fundingDutch Technology Foundation UGT7685, Dutch Science Founda-tion SGW-406-18-GO-086, and ERC Advanced Grant 320708.A. Schippers, M.J. Vansteensel, Z.V. Freudenburg et al. Brain Stimulation 14 (2021) 287e289References[1] Penfield W, Boldrey E. Somatic motor and sensory representation in the cere-bral cortex of man as studied by electrical stimulation. Brain 1937;60(4):389e443.[2] Miller KJ, Zanos S, Fetz EE, den Nijs M, Ojemann JG. Decoupling the cortical po-wer spectrum reveals real-time representation of individual finger movementsin humans. J. Neurosci. 2009;11:3132e7.[3] Conant D, Bouchard KE, Chang EF. Speech map in the human ventral sensory-motor cortex. Curr. Opin. Neurobiol. 2014;24:63e7.[4] Schellekens W, Petridou N, Ramsey NF. Detailed somatotopy in primary motorand somatosensory cortex revealed by Gaussian population receptive fields.Neuroimage 2018;179:337e47.[5] Grabski K, Lamalle L, Vilain C, et al. Functional MRI assessment of orofacial ar-ticulators: neural correlates of lip, jaw, larynx, and tongue movements. Hum.Brain Mapp. 2012;33:2306e21.[6] Branco MP, Leibbrand M, Vansteensel MJ, Freudenburg ZV, Ramsey NF. GridLoc:an automatic and unsupervised localization method for high-density ECoGgrids. Neuroimage 2018;179:225e34.[7] Salari E, Freudenburg ZV, Branco MP, Aarnoutse EJ, Vansteensel MJ, Ramsey NF.Classification of articulator movements and movement direction from sensori-motor cortex activity. Sci. Rep. 2019;9(1):1e12.289[8] Ladino LD, Rizvi S, Tellez-Zenteno. The Montreal procedure: the legacy of thegreat Wilder Penfield. Epilepsy Behav. 2018;83:151. 151.Anouck Schippers, Mariska J. Vansteensel, Zachary V. Freudenburg,Frans S.S. Leijten, Nick F. Ramsey*UMC Utrecht Brain Center, Department of Neurology andNeurosurgery, University Medical Center Utrecht, Utrecht, theNetherlands* Corresponding author. HP G03 1.29 P.O. Box 85500, 3508 GA, CXUtrecht, the Netherlands.E-mail address: n.f.ramsey@umcutrecht.nl (N.F. Ramsey).29 December 2020Available online 20 January 2021

Detailed somatotopy of tongue movement in the human sensorimotor cortex: A case study

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Detailed somatotopy of tongue movement in the human sensorimotor cortex: A case study

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