Evaluation of the Cortical Silent Period of the Laryngeal Motor Cortex in Healthy Individuals

Mo Chen, Rebekah L S Summers, George S Goding, Sharyl Samargia, Christy L Ludlow, Cecília N Prudente, Teresa J Kimberley, Mo Chen, Rebekah L S Summers, George S Goding, Sharyl Samargia, Christy L Ludlow, Cecília N Prudente, Teresa J Kimberley

Abstract

Objective: This work aimed to evaluate the cortical silent period (cSP) of the laryngeal motor cortex (LMC) using the bilateral thyroarytenoid (TA) muscles with transcranial magnetic stimulation (TMS). Methods: In 11 healthy participants, fine-wire electromyography (EMG) was used to record bilateral TA muscle responses to single pulse TMS delivered to the LMC in both hemispheres. Peripheral responses to stimulation over the mastoid, where the vagus nerve exits the skull, were collected to verify the central origin of the cortical stimulation responses by comparing the latencies. Results: The cSP duration ranged from 41.7 to 66.4 ms. The peripherally evoked motor-evoked potential (MEP) peak occurred 5-9 ms earlier than the cortical responses (for both sides of TAs: p < 0.0001) with no silent period. The right TA MEP latencies were earlier than the left TA responses for both peripheral and cortical measures (p ≤ 0.0001). Conclusion: These findings demonstrate the feasibility of measuring cSP of LMC based on intrinsic laryngeal muscles responses during vocalization in healthy volunteers. Significance: The technique could be used to study the pathophysiology of neurological disorders that affect TA muscles, such as spasmodic dysphonia. Further, the methodology has application to other muscles of the head and neck not accessible using surface electrodes.

Keywords: TMS; Transcranial magnetic stimulation; cSP; cortical silent period; fine wire electrode; larynx; motor cortex excitability.

Figures

Figure 1
Figure 1
Experimental Set up. (A) Fine-wire electrodes. There were two channels (pairs of fine-wires) inserted into bilateral thyroarytenoid muscles; (B) Ground electrode. The strap ground electrode was placed under the BrainSight subject tracker band.
Figure 2
Figure 2
TMS coil placement for laryngeal motor cortex (LMC) and peripheral stimulation. (A) Coil position and angle for LMC stimulation (cSP test); (B) coil position and angle for peripheral stimulation.
Figure 3
Figure 3
Bilateral thyroarytenoid (TA) muscle responses to right peripheral and cortical stimulation in one participant. (A) Left TA recording without a response to right peripheral stimulation during rest (sample trace); (B) Right TA response to right peripheral stimulation during rest (MEP latency is 5.6 ms.); (C) Left TA recording without a response to right peripheral stimulation during vocalization (sample trace); (D) Right TA response to right peripheral stimulation (MEP peak latency is 5.7 ms.); (E) Average of 50 left TA responses to right cortical stimulation (MEP peak latency is 13.0 ms); (F) Average of 50 right TA responses to right cortical stimulation (MEP peak latency is 11.1 ms). Note the unilateral (ipsilateral) responses to peripheral stimulation and bilateral responses to cortical stimulation, which demonstrates the validity of cortical responses. MEP: motor evoked potential.
Figure 4
Figure 4
Bilateral thyroarytenoid (TA) motor evoked potential (MEP) responses to right cortical stimulation during voice production in Subject 02. (A) 50 individual traces of left TA responses to right cortical stimulation; (B) 50 individual traces of right TA responses to right cortical stimulation; (C) cSP from the left TA during right cortical stimulation (offset X at 42.5 ms); (D) cSP from the right TA during right cortical stimulation (offset X at 49.2 ms). The cSP moving average was calculated based on the average of the 50 trials. The stimuli were delivered at 0 ms. cSP: cortical silent period.
Figure 5
Figure 5
MEP latency comparisons. Red color represents peripheral stimulation responses (left). Blue color represents cortical stimulation responses (right). Thatched represents left TA responses. Solid represents right TA responses. The MEP latencies of left TA were significantly longer than the right TA in both peripheral and cortical stimulation. The MEP latencies of the cortical stimulation were significantly longer than the peripheral one in both left and right TAs. L-H: cortical Left Hemisphere; R-H: cortical Right Hemisphere. *p < 0.05.

References

    1. Atkins J. P. (1973). An electromyographic study of recurrent laryngeal nerve conduction and its clinical applications. Laryngoscope 83, 796–807. 10.1288/00005537-197305000-00015
    1. Calancie B., Nordin M., Wallin U., Hagbarth K. E. (1987). Motor-unit responses in human wrist flexor and extensor muscles to transcranial cortical stimuli. J. Neurophysiol. 58, 1168–1185.
    1. Chen M., Deng H., Schmidt R. L., Kimberley T. J. (2015). Low-Frequency repetitive transcranial magnetic stimulation targeted to premotor cortex followed by primary motor cortex modulates excitability differently than premotor cortex or primary motor cortex stimulation alone. Neuromodulation 18, 678–685. 10.1111/ner.12337
    1. Classen J., Benecke R. (1995). Inhibitory phenomena in individual motor units induced by transcranial magnetic stimulation. Electroencephalogr. Clin. Neurophysiol. 97, 264–274. 10.1016/0924-980X(95)00099-2
    1. Currà A., Romaniello A., Berardelli A., Cruccu G., Manfredi M. (2000). Shortened cortical silent period in facial muscles of patients with cranial dystonia. Neurology 54, 130–135. 10.1212/WNL.54.1.130
    1. Davey N. J., Romaiguère P., Maskill D. W., Ellaway P. H. (1994). Suppression of voluntary motor activity revealed using transcranial magnetic stimulation of the motor cortex in man. J. Physiol. 477(Pt 2), 223–235.
    1. Eldaief M. C., Press D. Z., Pascual-Leone A. (2013). Transcranial magnetic stimulation in neurology: a review of established and prospective applications. Neurol. Clin. Pract. 3, 519–526. 10.1212/01.CPJ.0000436213.11132.8e
    1. Ertekin C., Turman B., Tarlaci S., Celik M., Aydogdu I., Secil Y., et al. . (2001). Cricopharyngeal sphincter muscle responses to transcranial magnetic stimulation in normal subjects and in patients with dysphagia. Clin. Neurophysiol. 112, 86–94. 10.1016/S1388-2457(00)00504-6
    1. Eisen A. A., Shtybel W. (1990). AAEM minimonograph #35: clinical experience with transcranial magnetic stimulation. Muscle Nerve 13, 995–1011. 10.1002/mus.880131102
    1. Espadaler J., Rogić M., Deletis V., Leon A., Quijada C., Conesa G. (2012). Representation of cricothyroid muscles at the primary motor cortex (M1) in healthy subjects, mapped by navigated transcranial magnetic stimulation (nTMS). Clin. Neurophysiol. 123, 2205–2211. 10.1016/j.clinph.2012.04.008
    1. Ferbert A., Caramia D., Priori A., Bertolasi L., Rothwell J. C. (1992). Cortical projection to erector spinae muscles in man as assessed by focal transcranial magnetic stimulation. Electroencephalogr. Clin. Neurophysiol. 85, 382–387. 10.1016/0168-5597(92)90051-C
    1. Hallett M. (2007). Transcranial magnetic stimulation: a primer. Neuron 55, 187–199. 10.1016/j.neuron.2007.06.026
    1. Haug B. A., Schönle P. W., Knobloch C., Köhne M. (1992). Silent period measurement revives as a valuable diagnostic tool with transcranial magnetic stimulation. Electroencephalogr. Clin. Neurophysiol. 85, 158–160. 10.1016/0168-5597(92)90081-L
    1. Henriquez V. M., Schulz G. M., Bielamowicz S., Ludlow C. L. (2007). Laryngeal reflex responses are not modulated during human voice and respiratory tasks. J. Physiol. 585(Pt 3), 779–789. 10.1113/jphysiol.2007.143438
    1. Hirano M., Ohala J. (1969). Use of hooked-wire electrodes for electromyography of the intrinsic laryngeal muscles. J. Speech Hear. Res. 12:362. 10.1044/jshr.1202.362
    1. Inghilleri M., Berardelli A., Cruccu G., Manfredi M. (1993). Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction. J. Physiol. 466, 521–534.
    1. Katayama T., Aizawa H., Kuroda K., Suzuki Y., Kikuchi K., Kimura T., et al. . (2001). Cortical silent period in the tongue induced by transcranial magnetic stimulation. J. Neurol. Sci. 193, 37–41. 10.1016/S0022-510X(01)00647-5
    1. Khedr E. M., Aref E.-E. M. (2002). Electrophysiological study of vocal-fold mobility disorders using a magnetic stimulator. Eur. J. Neurol. 9, 259–267. 10.1046/j.1468-1331.2002.00394.x
    1. Kimberley T. J., Borich M. R., Prochaska K. D., Mundfrom S. L., Perkins A. E., Poepping J. M. (2009). Establishing the definition and inter-rater reliability of cortical silent period calculation in subjects with focal hand dystonia and healthy controls. Neurosci. Lett. 464, 84–87. 10.1016/j.neulet.2009.08.029
    1. Kimiskidis V. K., Papagiannopoulos S., Sotirakoglou K., Kazis D. A., Kazis A., Mills K. R. (2005). Silent period to transcranial magnetic stimulation: construction and properties of stimulus–response curves in healthy volunteers. Exp. Brain Res. 163, 21–31. 10.1007/s00221-004-2134-4
    1. Konrad P. (2005). The ABC of EMG: A Practical Introduction to Kinesiological Electromyography. Scottsdale, AZ: Noraxon INC.
    1. Kukowski B., Haug B. (1991). Quantitative evaluation of the silent period, evoked by transcranial magnetic stimulation during sustained muscle contraction, in normal man and in patients with stroke. Electromyogr. Clin. Neurophysiol. 32, 373–378.
    1. Kuna S. T., Insalaco G., Woodson G. E. (1988). Thyroarytenoid muscle activity during wakefulness and sleep in normal adults. J. Appl. Physiol. 65, 1332–1339.
    1. Lefaucheur J.-P. (2005). Excitability of the motor cortical representation of the external anal sphincter. Exp. Brain Res. 160, 268–272. 10.1007/s00221-004-2170-0
    1. Lefaucheur J.-P., Lofaso F. (2002). Diaphragmatic silent period to transcranial magnetic cortical stimulation for assessing cortical motor control of the diaphragm. Exp. Brain Res. 146, 404–409. 10.1007/s00221-002-1197-3
    1. Ludlow C. L. (2005). Central nervous system control of the laryngeal muscles in humans. Respir. Physiol. Neurobiol. 147, 205–222. 10.1016/j.resp.2005.04.015
    1. Ludlow C. L. (2015). Central nervous system control of voice and swallowing. J. Clin. Neurophysiol. 32, 294–303. 10.1097/WNP.0000000000000186
    1. Ludlow C. L., Adler C. H., Berke G. S., Bielamowicz S. A., Blitzer A., Bressman S. B., et al. . (2008). Research priorities in spasmodic dysphonia. Otolaryngol. Head Neck Surg. 139, 495–505. 10.1016/j.otohns.2008.05.624
    1. Mazziotta J., Toga A., Evans A., Fox P., Lancaster J., Zilles K., et al. . (2001). A four-dimensional probabilistic atlas of the human brain. J. Am. Med. Inform. Assoc. 8, 401–430. 10.1136/jamia.2001.0080401
    1. Orth M., Rothwell J. (2004). The cortical silent period: intrinsic variability and relation to the waveform of the transcranial magnetic stimulation pulse. Clin. Neurophysiol. 115, 1076–1082. 10.1016/j.clinph.2003.12.025
    1. Paradiso G. O., Cunic D. I., Gunraj C. A., Chen R. (2005). Representation of facial muscles in human motor cortex. J. Physiol. 567, 323–336. 10.1113/jphysiol.2005.088542
    1. Paulus W., Classen J., Cohen L. G., Large C. H., Di Lazzaro V., Nitsche M., et al. . (2008). State of the art: pharmacologic effects on cortical excitability measures tested by transcranial magnetic stimulation. Brain Stimul. 1, 151–163. 10.1016/j.brs.2008.06.002
    1. Rödel R. M. W., Olthoff A., Tergau F., Simonyan K., Kraemer D., Markus H., et al. . (2004). Human cortical motor representation of the larynx as assessed by Transcranial Magnetic Stimulation (TMS). Laryngoscope 114, 918–922. 10.1097/00005537-200405000-00026
    1. Rogić Vidaković M., Schönwald M. Z., Rotim K., Jurić T., Vulević Z., Tafra R., et al. . (2015). Excitability of contralateral and ipsilateral projections of corticobulbar pathways recorded as corticobulbar motor evoked potentials of the cricothyroid muscles. Clin. Neurophysiol. 126, 1570–1577. 10.1016/j.clinph.2014.11.001
    1. Roick H., von Giesen H. J., Benecke R. (1993). On the origin of the postexcitatory inhibition seen after transcranial magnetic brain stimulation in awake human subjects. Exp. Brain Res. 94, 489–498. 10.1007/BF00230207
    1. Rossini P. M., Barker A. T., Berardelli A., Caramia M. D., Caruso G., Cracco R. Q., et al. . (1994). Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr. Clin. Neurophysiol. 91, 79–92. 10.1016/0013-4694(94)90029-9
    1. Rossini P. M., Burke D., Chen R., Cohen L. G., Daskalakis Z., Di Iorio R., et al. . (2015). Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee. Clin. Neurophysiol. 126, 1071–1107. 10.1016/j.clinph.2015.02.001
    1. Säisänen L., Pirinen E., Teitti S., Könönen M., Julkunen P., Määttä S., et al. . (2008). Factors influencing cortical silent period: optimized stimulus location, intensity and muscle contraction. J. Neurosci. Methods 169, 231–238. 10.1016/j.jneumeth.2007.12.005
    1. Samargia S., Schmidt R., Kimberley T. J. (2014). Shortened cortical silent period in adductor spasmodic dysphonia: evidence for widespread cortical excitability. Neurosci. Lett. 560, 12–15. 10.1016/j.neulet.2013.12.007
    1. Siebner H. R., Dressnandt J., Auer C., Conrad B. (1998). Continuous intrathecal baclofen infusions induced a marked increase of the transcranially evoked silent period in a patient with generalized dystonia. Muscle Nerve 21, 1209–1212. 10.1002/(SICI)1097-4598(199809)21:9<1209::AID-MUS15>;2-M
    1. Silbert L. C., Nelson C., Holman S., Eaton R., Oken B. S., Lou J. S., et al. . (2006). Cortical excitability and age-related volumetric MRI changes. Clin. Neurophysiol. 117, 1029–1036. 10.1016/j.clinph.2006.02.003
    1. Simonyan K., Horwitz B. (2011). Laryngeal motor cortex and control of speech in humans. Neuroscientist 17, 197–208. 10.1177/1073858410386727
    1. Simonyan K., Ostuni J., Ludlow C. L., Horwitz B. (2009). Functional but not structural networks of the human laryngeal motor cortex show left hemispheric lateralization during syllable but not breathing production. J. Neurosci. 29, 14912–14923. 10.1523/JNEUROSCI.4897-09.2009
    1. Sims H. S., Yamashita T., Rhew K., Ludlow C. L. (1996). Assessing the clinical utility of the magnetic stimulator for measuring response latencies in the laryngeal muscles. Otolaryngol. Head Neck Surg. 114, 761–767. 10.1016/S0194-5998(96)70099-2
    1. Taylor J. L., Allen G. M., Butler J. E., Gandevia S. C. (1997). Effect of contraction strength on responses in biceps brachii and adductor pollicis to transcranial magnetic stimulation. Exp. Brain Res. 117, 472–478. 10.1007/s002210050243
    1. Thumfart W. F., Zorowka P., Pototschnig C., Eckel H. E. (1992). Electrophysiologic investigation of lower cranial nerve diseases by means of magnetically stimulated neuromyography of the larynx. Ann. Otol. Rhinol. Laryngol. 101, 629–634. 10.1177/000348949210100801
    1. Tinazzi M., Farina S., Edwards M., Moretto G., Restivo D., Fiaschi A., et al. . (2005). Task-specific impairment of motor cortical excitation and inhibition in patients with writer's cramp. Neurosci. Lett. 378, 55–58. 10.1016/j.neulet.2004.12.015
    1. Werhahn K. J., Classen J., Benecke R. (1995). The silent period induced by transcranial magnetic stimulation in muscles supplied by cranial nerves: normal data and changes in patients. J. Neurol. Neurosurg. Psychiatr. 59, 586–596. 10.1136/JNNP.59.6.586
    1. Wolters A., Ziemann U., Benecke R. (2008). The cortical silent period, in Oxford Handbook of Transcranial Stimulation, eds Epstein C. M., Wassermann E. M., Ziemann U. (New York, NY: Oxford University Press; ), 1–23.
    1. World Medical Association (2013). World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA. 310, 2191–2194. 10.1001/jama.2013.281053
    1. Wu L., Goto Y., Taniwaki T., Kinukawa N., Tobimatsu S. (2002). Different patterns of excitation and inhibition of the small hand and forearm muscles from magnetic brain stimulation in humans. Clin. Neurophysiol. 113, 1286–1294. 10.1016/S1388-2457(02)00160-8

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