Skip to main content
Erschienen in: Journal of Clinical Monitoring and Computing 5/2017

26.08.2016 | Original Research

Efficacy and safety of novel high-frequency multi-train stimulation for recording transcranial motor evoked potentials in a rat model

verfasst von: Tsuyoshi Deguchi, Shunji Tsutsui, Hiroki Iwahashi, Yukihiro Nakagawa, Munehito Yoshida

Erschienen in: Journal of Clinical Monitoring and Computing | Ausgabe 5/2017

Einloggen, um Zugang zu erhalten

Abstract

Recently, low-frequency multi-train stimulation (MTS) was shown to effectively enhance transcranial motor-evoked potentials (TcMEPs). In contrast, high- frequency double-train stimulation was reported to elicit a marked facilitation. The aim of this study was to evaluate the efficacy of high-frequency MTS in the augmentation of potentials. In addition, we investigated the safety of high-frequency MTS, behaviorally and histologically. TcMEPs were recorded from the triceps surae muscle in 38 rats. A multipulse stimulus was delivered repeatedly at different rates (2, 5, 10, 20, and 50 Hz), and was defined as MTS. A conditioned taste aversion method was used to investigate the effect of high-frequency MTS on learning and memory function. Subsequently, animals were sacrificed, and the brains were removed and examined using the standard hematoxylin-eosin method. Compared with conventional single train stimulation, TcMEP amplitudes increased 1.3, 2.1, 1.9, and 2.0 times on average with 5, 10, 20, and 50 Hz stimulation, respectively. The aversion index was >0.8 in all animals after they received 100 high-frequency MTSs. Histologically, no pathological changes were evident in the rat brains. High-frequency MTS shows potential to effectively enhance TcMEP responses, and to be used safely in transcranial brain stimulation.
Literatur
1.
Zurück zum Zitat Kothbauer K, Deletis V, Epstein FJ. Intraoperative spinal cord monitoring for intramedullary surgery: an essential adjunct. Pediatr Neurosurg. 1997;26:247–54.CrossRefPubMed Kothbauer K, Deletis V, Epstein FJ. Intraoperative spinal cord monitoring for intramedullary surgery: an essential adjunct. Pediatr Neurosurg. 1997;26:247–54.CrossRefPubMed
2.
Zurück zum Zitat Cioni B, Meglio M, Rossi GF. Intraoperative motor evoked potentials monitoring in spinal neurosurgery. Arch Ital Biol. 1999;137:115–26.PubMed Cioni B, Meglio M, Rossi GF. Intraoperative motor evoked potentials monitoring in spinal neurosurgery. Arch Ital Biol. 1999;137:115–26.PubMed
3.
Zurück zum Zitat Meylaerts SA, Jacobs MJ, van Iterson V, De Haan P, Kalkman CJ. Comparison of transcranial motor evoked potentials and somatosensory evoked potentials during thoracoabdominal aortic aneurysm repair. Ann Surg. 1999;230:742–9.CrossRefPubMedPubMedCentral Meylaerts SA, Jacobs MJ, van Iterson V, De Haan P, Kalkman CJ. Comparison of transcranial motor evoked potentials and somatosensory evoked potentials during thoracoabdominal aortic aneurysm repair. Ann Surg. 1999;230:742–9.CrossRefPubMedPubMedCentral
4.
Zurück zum Zitat Kombos T, Suess O, Ciklatekerlio O, Brock M. Monitoring of intraoperative motor evoked potentials to increase the safety of surgery in and around the motor cortex. J Neurosurg. 2001;95:608–14.CrossRefPubMed Kombos T, Suess O, Ciklatekerlio O, Brock M. Monitoring of intraoperative motor evoked potentials to increase the safety of surgery in and around the motor cortex. J Neurosurg. 2001;95:608–14.CrossRefPubMed
5.
Zurück zum Zitat Langeloo DD, Lelivelt A, Louis JH, Slappendel R, de Kleuver M. Transcranial electrical motor-evoked potential monitoring during surgery for spinal deformity: a study of 145 patients. Spine. 2003;28:1043–50 (Phila Pa 1976).PubMed Langeloo DD, Lelivelt A, Louis JH, Slappendel R, de Kleuver M. Transcranial electrical motor-evoked potential monitoring during surgery for spinal deformity: a study of 145 patients. Spine. 2003;28:1043–50 (Phila Pa 1976).PubMed
6.
Zurück zum Zitat Hilibrand AS, Schwartz DM, Sethuraman V, Vaccaro AR, Albert TJ. Comparison of transcranial electric motor and somatosensory evoked potential monitoring during cervical spine surgery. J Bone Joint Surg Am. 2004;86:1248–53.CrossRefPubMed Hilibrand AS, Schwartz DM, Sethuraman V, Vaccaro AR, Albert TJ. Comparison of transcranial electric motor and somatosensory evoked potential monitoring during cervical spine surgery. J Bone Joint Surg Am. 2004;86:1248–53.CrossRefPubMed
7.
Zurück zum Zitat Calancie B, Molano MR. Alarm criteria for motor-evoked potentials. What’s wrong with the ‘‘presence-or-absence’’ approach? Spine. 2008;33:406–14 (Phila Pa 1976).CrossRefPubMed Calancie B, Molano MR. Alarm criteria for motor-evoked potentials. What’s wrong with the ‘‘presence-or-absence’’ approach? Spine. 2008;33:406–14 (Phila Pa 1976).CrossRefPubMed
8.
Zurück zum Zitat Sakaki K, Kawabata S, Ukegawa D, Hirai T, Ishii S, Tomori M, et al. Warning thresholds on the basis of origin of amplitude changes in transcranial electrical motor-evoked potential monitoring for cervical compression myelopathy. Spine. 2012;37:E913–21 (Phila Pa 1976).CrossRefPubMed Sakaki K, Kawabata S, Ukegawa D, Hirai T, Ishii S, Tomori M, et al. Warning thresholds on the basis of origin of amplitude changes in transcranial electrical motor-evoked potential monitoring for cervical compression myelopathy. Spine. 2012;37:E913–21 (Phila Pa 1976).CrossRefPubMed
9.
Zurück zum Zitat Muramoto A, Imagama S, Ito Z, Wakao N, Ando K, Tauchi R, et al. The cutoff amplitude of transcranial motor-evoked potentials for predicting postoperative motor deficits in thoracic spine surgery. Spine. 2013;38:E21–7 (Phila Pa 1976).CrossRefPubMed Muramoto A, Imagama S, Ito Z, Wakao N, Ando K, Tauchi R, et al. The cutoff amplitude of transcranial motor-evoked potentials for predicting postoperative motor deficits in thoracic spine surgery. Spine. 2013;38:E21–7 (Phila Pa 1976).CrossRefPubMed
10.
Zurück zum Zitat Woodforth IJ, Hicks RG, Crawford MR, Stephen JP, Burke DJ. Variability of motor-evoked potentials recording during nitrous oxide anesthesia from the tibialis anterior muscle after transcranial electrical stimulation. Anesth Analg. 1996;82:744–9.PubMed Woodforth IJ, Hicks RG, Crawford MR, Stephen JP, Burke DJ. Variability of motor-evoked potentials recording during nitrous oxide anesthesia from the tibialis anterior muscle after transcranial electrical stimulation. Anesth Analg. 1996;82:744–9.PubMed
11.
Zurück zum Zitat Tsutsui S, Yamada H, Hashizume H, Minamide A, Nakagawa Y, Iwasaki H, et al. Quantification of the proportion of motor neurons recruited by transcranial electrical stimulation during intraoperative motor evoked potential monitoring. J Clin Monit Comput. 2013;27:633–7.CrossRefPubMed Tsutsui S, Yamada H, Hashizume H, Minamide A, Nakagawa Y, Iwasaki H, et al. Quantification of the proportion of motor neurons recruited by transcranial electrical stimulation during intraoperative motor evoked potential monitoring. J Clin Monit Comput. 2013;27:633–7.CrossRefPubMed
12.
Zurück zum Zitat Andersson G, Ohlin A. Spatial facilitation of motor evoked responses in monitoring during spinal surgery. Clin Neurophysiol. 1999;110:720–4.CrossRefPubMed Andersson G, Ohlin A. Spatial facilitation of motor evoked responses in monitoring during spinal surgery. Clin Neurophysiol. 1999;110:720–4.CrossRefPubMed
13.
Zurück zum Zitat Journée HL, Polak HE, de Kleuver M, Langeloo DD, Postma AA. Improved neuromonitoring during spinal surgery using doubletrain transcranial electrical stimulation. Med Biol Eng Comput. 2004;42:110–3.CrossRefPubMed Journée HL, Polak HE, de Kleuver M, Langeloo DD, Postma AA. Improved neuromonitoring during spinal surgery using doubletrain transcranial electrical stimulation. Med Biol Eng Comput. 2004;42:110–3.CrossRefPubMed
14.
Zurück zum Zitat Kakimoto M, Kawaguchi M, Yamamoto Y, Inoue S, Horiuchi T, Nakase H, et al. Tetanic stimulation of the peripheral nerve before transcranial electrical stimulation can enlarge amplitudes of myogenic motor evoked potentials during general anesthesia with neuromuscular blockade. Anesthesiology. 2005;102:733–8.CrossRefPubMed Kakimoto M, Kawaguchi M, Yamamoto Y, Inoue S, Horiuchi T, Nakase H, et al. Tetanic stimulation of the peripheral nerve before transcranial electrical stimulation can enlarge amplitudes of myogenic motor evoked potentials during general anesthesia with neuromuscular blockade. Anesthesiology. 2005;102:733–8.CrossRefPubMed
15.
Zurück zum Zitat Frei FJ, Ryhult SE, Duitmann E, Hasler CC, Luetschg J, Erb TO. Intraoperative monitoring of motor evoked potentials in children undergoing spinal surgery. Spine. 2007;32:911–7 (Phila Pa 1976).CrossRefPubMed Frei FJ, Ryhult SE, Duitmann E, Hasler CC, Luetschg J, Erb TO. Intraoperative monitoring of motor evoked potentials in children undergoing spinal surgery. Spine. 2007;32:911–7 (Phila Pa 1976).CrossRefPubMed
16.
Zurück zum Zitat Hayashi H, Kawaguchi M, Yamamoto Y, Inoue S, Koizumi M, Ueda Y, et al. Evaluation of reliability of posttetanic motor evoked potential monitoring during spinal surgery under general anesthesia. Spine. 2008;33:E994–1000 (Phila Pa 1976).CrossRefPubMed Hayashi H, Kawaguchi M, Yamamoto Y, Inoue S, Koizumi M, Ueda Y, et al. Evaluation of reliability of posttetanic motor evoked potential monitoring during spinal surgery under general anesthesia. Spine. 2008;33:E994–1000 (Phila Pa 1976).CrossRefPubMed
17.
Zurück zum Zitat Deletis V. Intraoperative neurophysiology and methodologies used to monitor the functional integrity of the motor system. In: Deletis V, Shils JL, editors. Neurophysiology in neurosurgery. New York: Academic Press; 2002. p. 25–51.CrossRef Deletis V. Intraoperative neurophysiology and methodologies used to monitor the functional integrity of the motor system. In: Deletis V, Shils JL, editors. Neurophysiology in neurosurgery. New York: Academic Press; 2002. p. 25–51.CrossRef
18.
Zurück zum Zitat MacDonald DB, Al Zayed Z, Khoudeir I, Stigsby B. Monitoring scoliosis surgery with combined multiple pulse transcranial electric motor and cortical somatosensory-evoked potentials from the lower and upper extremities. Spine. 2003;28:194–203 (Phila Pa 1976).CrossRefPubMed MacDonald DB, Al Zayed Z, Khoudeir I, Stigsby B. Monitoring scoliosis surgery with combined multiple pulse transcranial electric motor and cortical somatosensory-evoked potentials from the lower and upper extremities. Spine. 2003;28:194–203 (Phila Pa 1976).CrossRefPubMed
19.
Zurück zum Zitat MacDonald DB, Al Zayed Z, Al Saddigi A. Four-limb muscle motor evoked potential and optimized somatosensory evoked potential monitoring with decussation assessment: results in 206 thoracolumbar spine surgeries. Eur Spine J. 2007;16(Suppl 2):171–87.CrossRefPubMedCentral MacDonald DB, Al Zayed Z, Al Saddigi A. Four-limb muscle motor evoked potential and optimized somatosensory evoked potential monitoring with decussation assessment: results in 206 thoracolumbar spine surgeries. Eur Spine J. 2007;16(Suppl 2):171–87.CrossRefPubMedCentral
20.
Zurück zum Zitat Deletis V, Sala F. Corticospinal tract monitoring with D- and I-waves from the spinal cord and muscle MEPs from limb muscles. In: Nuwer MR, editor. Intraoperative monitoring of neural function. Handbook of clinical neurophysiology, vol. 8. Amsterdam: Elsevier; 2008. p. 235–51.CrossRef Deletis V, Sala F. Corticospinal tract monitoring with D- and I-waves from the spinal cord and muscle MEPs from limb muscles. In: Nuwer MR, editor. Intraoperative monitoring of neural function. Handbook of clinical neurophysiology, vol. 8. Amsterdam: Elsevier; 2008. p. 235–51.CrossRef
21.
Zurück zum Zitat MacDonald DB, Skinner S, Shils J, Yingling C. Intraoperative motor evoked potential monitoring—a position statement by the American society of neurophysiological monitoring. Clin Neurophysiol. 2013;124:2291–316.CrossRefPubMed MacDonald DB, Skinner S, Shils J, Yingling C. Intraoperative motor evoked potential monitoring—a position statement by the American society of neurophysiological monitoring. Clin Neurophysiol. 2013;124:2291–316.CrossRefPubMed
22.
Zurück zum Zitat Tsutsui S, Iwasaki H, Yamada H, Hashizume H, Minamide A, Nakagawa Y, et al. Augmentation of motor evoked potentials using multi-train transcranial stimulation in intraoperative neurophysiologic monitoring during spinal surgery. J Clin Monit Comput. 2015;29:35–9.CrossRefPubMed Tsutsui S, Iwasaki H, Yamada H, Hashizume H, Minamide A, Nakagawa Y, et al. Augmentation of motor evoked potentials using multi-train transcranial stimulation in intraoperative neurophysiologic monitoring during spinal surgery. J Clin Monit Comput. 2015;29:35–9.CrossRefPubMed
23.
Zurück zum Zitat MacDonald DB. Safety of intraoperative transcranial electrical stimulation motor evoked potential monitoring. J Clin Neurophysiol. 2002;19:416–29.CrossRefPubMed MacDonald DB. Safety of intraoperative transcranial electrical stimulation motor evoked potential monitoring. J Clin Neurophysiol. 2002;19:416–29.CrossRefPubMed
24.
Zurück zum Zitat Chambers KC. A neural model for conditioned taste aversions. Annu Rev Neurosci. 1990;13:373–85.CrossRefPubMed Chambers KC. A neural model for conditioned taste aversions. Annu Rev Neurosci. 1990;13:373–85.CrossRefPubMed
25.
Zurück zum Zitat Bures J, Bermudez-Rattoni F, Yamamoto T, editors. Conditioned taste aversion: memory of special kind. New York: Oxford University Press; 1998. Bures J, Bermudez-Rattoni F, Yamamoto T, editors. Conditioned taste aversion: memory of special kind. New York: Oxford University Press; 1998.
26.
Zurück zum Zitat Barker LM, Best MR, Domjam M. Learning Mechanisms in Food Selection. Waco: Baylor University Press; 1999. Barker LM, Best MR, Domjam M. Learning Mechanisms in Food Selection. Waco: Baylor University Press; 1999.
27.
Zurück zum Zitat Shaw N. Disruption of conditioned taste aversion: evidence that ECS weakens the gustatory engram. Behav Neural Biol. 1988;49:302–9.CrossRefPubMed Shaw N. Disruption of conditioned taste aversion: evidence that ECS weakens the gustatory engram. Behav Neural Biol. 1988;49:302–9.CrossRefPubMed
28.
Zurück zum Zitat King JW, Yarita M, Yamamoto T, Matsumiya Y. Memory for conditioned taste aversion is diminished by transcranial magnetic stimulation. Physiol Behav. 1990;48:713–7.CrossRef King JW, Yarita M, Yamamoto T, Matsumiya Y. Memory for conditioned taste aversion is diminished by transcranial magnetic stimulation. Physiol Behav. 1990;48:713–7.CrossRef
29.
Zurück zum Zitat Alstermark B, Isa T, Okki Y, Saito Y. Disynaptic pyramidal excitation in forelimb motoneurons mediated via C3–C4 propriospinal neurons in the Macaca fuscata. J Neurophysiol. 1999;82:3580–5.PubMed Alstermark B, Isa T, Okki Y, Saito Y. Disynaptic pyramidal excitation in forelimb motoneurons mediated via C3–C4 propriospinal neurons in the Macaca fuscata. J Neurophysiol. 1999;82:3580–5.PubMed
30.
Zurück zum Zitat Alstermark B, Ogawa J, Isa T. Lack of monosynaptic corticomotoneuronal EPSPs in rats: disynaptic EPSPs mediated via reticulospinal neurons and polysynaptic EPSPs via segmental interneurons. J Neurophysiol. 2004;91:1832–9.CrossRefPubMed Alstermark B, Ogawa J, Isa T. Lack of monosynaptic corticomotoneuronal EPSPs in rats: disynaptic EPSPs mediated via reticulospinal neurons and polysynaptic EPSPs via segmental interneurons. J Neurophysiol. 2004;91:1832–9.CrossRefPubMed
31.
Zurück zum Zitat Penfield W, Boldrey E. Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain. 1937;60:339–443.CrossRef Penfield W, Boldrey E. Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain. 1937;60:339–443.CrossRef
32.
Zurück zum Zitat Marangell LB, Silver JM, Yudofsky SC. Psychopharmacology and electroconvulsive therapy. In: Hales RE, Yudofsky SC, Talbot JA, editors. The American psychiatric press textbook of psychiatry. 3rd ed. American psychiatric press; 1999. p. 1025–9. Marangell LB, Silver JM, Yudofsky SC. Psychopharmacology and electroconvulsive therapy. In: Hales RE, Yudofsky SC, Talbot JA, editors. The American psychiatric press textbook of psychiatry. 3rd ed. American psychiatric press; 1999. p. 1025–9.
33.
Zurück zum Zitat Wasserman EM. Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the safety of repetitive transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol. 1998;108:1–16.CrossRef Wasserman EM. Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the safety of repetitive transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol. 1998;108:1–16.CrossRef
34.
Zurück zum Zitat Stenberg J, Levy D, Zangen A. Impairment of aversive memory reconsolidation by localized intracranial electrical stimulation. Eur J Neurosci. 2009;29:964–9.CrossRef Stenberg J, Levy D, Zangen A. Impairment of aversive memory reconsolidation by localized intracranial electrical stimulation. Eur J Neurosci. 2009;29:964–9.CrossRef
35.
Zurück zum Zitat Hemmer LB, Zeeni C, Bebawy JF, Bendok BR, Cotton MA, Shah NB, et al. The incidence of unacceptable movement with motor evoked potentials during craniotomy for anuerysm clipping. World Neurosurg. 2014;81:99–104.CrossRefPubMed Hemmer LB, Zeeni C, Bebawy JF, Bendok BR, Cotton MA, Shah NB, et al. The incidence of unacceptable movement with motor evoked potentials during craniotomy for anuerysm clipping. World Neurosurg. 2014;81:99–104.CrossRefPubMed
Metadaten
Titel
Efficacy and safety of novel high-frequency multi-train stimulation for recording transcranial motor evoked potentials in a rat model
verfasst von
Tsuyoshi Deguchi
Shunji Tsutsui
Hiroki Iwahashi
Yukihiro Nakagawa
Munehito Yoshida
Publikationsdatum
26.08.2016
Verlag
Springer Netherlands
Erschienen in
Journal of Clinical Monitoring and Computing / Ausgabe 5/2017
Print ISSN: 1387-1307
Elektronische ISSN: 1573-2614
DOI
https://doi.org/10.1007/s10877-016-9930-9

Weitere Artikel der Ausgabe 5/2017

Journal of Clinical Monitoring and Computing 5/2017 Zur Ausgabe

Update AINS

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.