TMS brain mapping of the pharyngeal cortical representation in healthy subjects

BACKGROUND Brain mapping is fundamental to understanding brain organization and function. However, a major drawback to the traditional Brodmann parcellation technique is the reliance on the use of postmortem specimens. It has therefore historically been difficult to make any comparison regarding functional data from different regions or hemispheres within the same individual. Moreover, this method has been significant limited by subjective boundaries and classification criteria and therefore suffer from reproducibility issues. The development of transcranial magnetic stimulation (TMS) offers an alternative approach to brain mapping, specifically the motor cortical regions by eliciting quantifiable functional reactions. OBJECTIVE To precisely describe the motor cortical topographic representation of pharyngeal constrictor musculature using TMS and to further map the brain for use as a tool to study brain plasticity. METHODS 51 healthy subjects (20 male/31 female, 19-26 years old) were tested using single-pulse TMS combined with intraluminal catheter-guided high-resolution manometry and a standardized grid cap. We investigated various parameters of the motor-evoked potential (MEP) that include the motor map area, amplitude, latency, center of gravity (CoG) and asymmetry index. RESULTS Cortically evoked response latencies were similar for the left and right hemispheres at 6.79 ± 0.22 and 7.24 ± 0.27 ms, respectively. The average scalp positions (relative to the vertex) of the pharyngeal motor cortical representation were 10.40 ± 0.19 (SE) cm medio-lateral and 3.20 ± 0.20 (SE) cm antero-posterior in the left hemisphere and 9.65 ± 0.24 (SE) cm medio-lateral and 3.18 ± 0.23 (SE) cm antero-posterior in the right hemisphere. The mean motor map area of the pharynx in the left and right hemispheres were 9.22 ± 0.85(SE) cm2and 10.12 ± 1.24(SE) cm2, respectively. The amplitudes of the MEPs were 35.94 ± 1.81(SE)uV in the left hemisphere and 34.49 ± 1.95(SE)uV in the right hemisphere. By comparison, subtle but consistent differences in the degree of the bilateral hemispheric representation were also apparent both between and within individuals. CONCLUSION The swallowing musculature has a bilateral motor cortical representation across individuals, but is largely asymmetric within single subjects. These results suggest that TMS mapping using a guided intra-pharyngeal EMG catheter combined with a standardized gridded cap might be a useful tool to localize brain function/dysfunction by linking brain activation to the corresponding physical reaction.

[1]  S. Roman,et al.  Challenges in the swallowing mechanism: nonobstructive dysphagia in the era of high-resolution manometry and impedance. , 2011, Gastroenterology clinics of North America.

[2]  S. Hamdy,et al.  "Virtual" lesioning of the human oropharyngeal motor cortex: a videofluoroscopic study. , 2012, Archives of physical medicine and rehabilitation.

[3]  D. Nowak,et al.  Mapping cortical hand motor representation using TMS: A method to assess brain plasticity and a surrogate marker for recovery of function after stroke? , 2016, Neuroscience & Biobehavioral Reviews.

[4]  S. Cramer,et al.  Systematic assessment of training-induced changes in corticospinal output to hand using frameless stereotaxic transcranial magnetic stimulation , 2007, Nature Protocols.

[5]  Aad van der Lugt,et al.  Fiber density asymmetry of the arcuate fasciculus in relation to functional hemispheric language lateralization in both right- and left-handed healthy subjects: A combined fMRI and DTI study , 2007, NeuroImage.

[6]  Scott H. Frey,et al.  Handedness-dependent and -independent cerebral asymmetries in the anterior intraparietal sulcus and ventral premotor cortex during grasp planning , 2011, NeuroImage.

[7]  Srikantan S. Nagarajan,et al.  Language mapping with navigated repetitive TMS: Proof of technique and validation , 2013, NeuroImage.

[8]  John C. Rothwell,et al.  The cortical topography of human swallowing musculature in health and disease , 1996, Nature Medicine.

[9]  S. Hamdy,et al.  Cold thermal oral stimulation produces immediate excitability in human pharyngeal motor cortex , 2018, Neurogastroenterology and motility : the official journal of the European Gastrointestinal Motility Society.

[10]  John C. Rothwell,et al.  Long-term reorganization of human motor cortex driven by short-term sensory stimulation , 1998, Nature Neuroscience.

[11]  J. Rothwell,et al.  Priming Pharyngeal Motor Cortex by Repeated Paired Associative Stimulation , 2013, Neurorehabilitation and neural repair.

[12]  Won Hyuk Chang,et al.  Effects of Bilateral Repetitive Transcranial Magnetic Stimulation on Post-Stroke Dysphagia , 2017, Brain Stimulation.

[13]  J. Pandolfino,et al.  High-Resolution Manometry Correlates of Ineffective Esophageal Motility , 2012, The American Journal of Gastroenterology.

[14]  L. Aglio,et al.  Brain mapping using transcranial magnetic stimulation. , 2011, Neurosurgery clinics of North America.

[15]  J. Rothwell,et al.  Mapping causal interregional influences with concurrent TMS–fMRI , 2008, Experimental Brain Research.

[16]  A. Straube,et al.  TMS motor cortical brain mapping in patients with complex regional pain syndrome type I , 2006, Clinical Neurophysiology.

[17]  Christian Grefkes,et al.  Functional localization in the human brain: Gradient‐echo, spin‐echo, and arterial spin‐labeling fMRI compared with neuronavigated TMS , 2011, Human brain mapping.

[18]  Rainer W. Paine,et al.  Mapping Different Intra-Hemispheric Parietal-Motor Networks Using Twin Coil TMS , 2013, Brain Stimulation.

[19]  E. Yumoto,et al.  Swallowing pressure and pressure profiles in young healthy adults , 2014, The Laryngoscope.

[20]  C. Civardi,et al.  Hemispheric asymmetries of cortico-cortical connections in human hand motor areas , 2000, Clinical Neurophysiology.

[21]  Viviana Versace,et al.  Long-Term Effects on Cortical Excitability and Motor Recovery Induced by Repeated Muscle Vibration in Chronic Stroke Patients , 2011, Neurorehabilitation and neural repair.

[22]  E. Khedr,et al.  Therapeutic role of rTMS on recovery of dysphagia in patients with lateral medullary syndrome and brainstem infarction , 2009, Journal of Neurology, Neurosurgery & Psychiatry.

[23]  Age and gender effects on submental motor-evoked potentials , 2014, AGE.

[24]  Simon B Eickhoff,et al.  Imaging-based parcellations of the human brain , 2018, Nature Reviews Neuroscience.

[25]  J. Rothwell,et al.  Non‐invasive magnetic stimulation of the human cerebellum facilitates cortico‐bulbar projections in the swallowing motor system , 2011, Neurogastroenterology and motility : the official journal of the European Gastrointestinal Motility Society.

[26]  Keith M. McGregor,et al.  Motor map reliability and aging: a TMS/fMRI study , 2012, Experimental Brain Research.

[27]  A. Machado,et al.  Age-Related Weakness of Proximal Muscle Studied with Motor Cortical Mapping: A TMS Study , 2014, PloS one.

[28]  C. Zimmer,et al.  The variability of motor evoked potential latencies in neurosurgical motor mapping by preoperative navigated transcranial magnetic stimulation , 2017, BMC Neuroscience.

[29]  Bernhard Meyer,et al.  Preoperative motor mapping by navigated transcranial magnetic brain stimulation improves outcome for motor eloquent lesions. , 2014, Neuro-oncology.

[30]  J. Rothwell,et al.  Treatment of post‐stroke dysphagia with repetitive transcranial magnetic stimulation , 2009, Acta neurologica Scandinavica.

[31]  Shaheen Hamdy,et al.  Remote effects of intermittent theta burst stimulation of the human pharyngeal motor system , 2012, The European journal of neuroscience.

[32]  F. Liu,et al.  The effect of bolus consistency on swallowing function measured by high‐resolution manometry in healthy volunteers , 2017, The Laryngoscope.

[33]  M. Ridding,et al.  Test–retest reliability of motor evoked potentials (MEPs) at the submental muscle group during volitional swallowing , 2009, Journal of Neuroscience Methods.

[34]  V. Seifert,et al.  Test-retest Reliability of Navigated Transcranial Magnetic Stimulation of the Motor Cortex , 2014, Neurosurgery.

[35]  E. Khedr,et al.  Dysphagia and hemispheric stroke: A transcranial magnetic study , 2008, Neurophysiologie Clinique/Clinical Neurophysiology.

[36]  J. G. Grab,et al.  Robotic TMS mapping of motor cortex in the developing brain , 2018, Journal of Neuroscience Methods.

[37]  Richard D. Jones,et al.  Journal of Neuroscience Methods the Effect of Swallowing Treatments on Corticobulbar Excitability: a Review of Transcranial Magnetic Stimulation Induced Motor Evoked Potentials , 2022 .

[38]  Christian Gerloff,et al.  Ipsilesional motor area size correlates with functional recovery after stroke: a 6-month follow-up longitudinal TMS motor mapping study. , 2015, Restorative neurology and neuroscience.

[39]  I. Delvendahl,et al.  Navigated transcranial magnetic stimulation does not decrease the variability of motor-evoked potentials , 2010, Brain Stimulation.

[40]  Ruud W. Selles,et al.  TMS motor mapping: Comparing the absolute reliability of digital reconstruction methods to the golden standard , 2019, Brain Stimulation.

[41]  S. Hamdy,et al.  Exploring the effects of synchronous pharyngeal electrical stimulation with swallowing carbonated water on cortical excitability in the human pharyngeal motor system , 2016, Neurogastroenterology and motility : the official journal of the European Gastrointestinal Motility Society.

[42]  J. Pandolfino,et al.  High-resolution manometry and esophageal pressure topography: filling the gaps of convention manometry. , 2013, Gastroenterology clinics of North America.

[43]  Rocco Cavaleri,et al.  The reliability and validity of rapid transcranial magnetic stimulation mapping , 2018, Brain Stimulation.

[44]  M. Hallett,et al.  Noninvasive mapping of muscle representations in human motor cortex. , 1992, Electroencephalography and clinical neurophysiology.

[45]  Z. Dou,et al.  Effects of Theta Burst Stimulation on Suprahyoid Motor Cortex Excitability in Healthy Subjects , 2017, Brain Stimulation.

[46]  G Schlaug,et al.  Multimodal output mapping of human central motor representation on different spatial scales , 1998, The Journal of physiology.

[47]  M. Malcolm,et al.  Reliability of transcranial magnetic stimulation for mapping swallowing musculature in the human motor cortex , 2008, Clinical Neurophysiology.

[48]  J. Rothwell,et al.  Characterization of corticobulbar pharyngeal neurophysiology in dysphagic patients with Parkinson's disease. , 2014, Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association.

[49]  H. Goodkin,et al.  The influence of gender, hand dominance, and upper extremity length on motor evoked potentials , 2010, Journal of Clinical Monitoring and Computing.