Annals of Clinical Neurophysiology

The Korean Society of Clinical Neurophysiology (대한임상신경생리학회)
권호 표지
DOI QR코드

DOI QR Code

New approach of using cortico-cortical evoked potential for functional brain evaluation

  • Jo, Hyunjin (Department of Neurology, Samsung Medical Center, Sungkyunkwan University School of Medicine) ;
  • Kim, Dongyeop (Department of Neurology, Samsung Medical Center, Sungkyunkwan University School of Medicine) ;
  • Song, Jooyeon (Department of Neurology, Samsung Medical Center, Sungkyunkwan University School of Medicine) ;
  • Seo, Dae-Won (Department of Neurology, Samsung Medical Center, Sungkyunkwan University School of Medicine)
  • Received : 2021.05.03
  • Accepted : 2021.07.07
  • Published : 2021.10.31
Download PDF
⟨ Previous Next ⟩

Abstract

Cortico-cortical evoked potential (CCEP) mapping is a rapidly developing method for visualizing the brain network and estimating cortical excitability. The CCEP comprises the early N1 component the occurs at 10-30 ms poststimulation, indicating anatomic connectivity, and the late N2 component that appears at < 200 ms poststimulation, suggesting long-lasting effective connectivity. A later component at 200-1,000 ms poststimulation can also appear as a delayed response in some studied areas. Such delayed responses occur in areas with changed excitability, such as an epileptogenic zone. CCEP mapping has been used to examine the brain connections causally in functional systems such as the language, auditory, and visual systems as well as in anatomic regions including the frontoparietal neocortices and hippocampal limbic areas. Task-based CCEPs can be used to measure behavior. In addition to evaluations of the brain connectome, single-pulse electrical stimulation (SPES) can reflect cortical excitability, and so it could be used to predict a seizure onset zone. CCEP brain mapping and SPES investigations could be applied both extraoperatively and intraoperatively. These underused electrophysiologic tools in basic and clinical neuroscience might be powerful methods for providing insight into measures of brain connectivity and dynamics. Analyses of CCEPs might enable us to identify causal relationships between brain areas during cortical processing, and to develop a new paradigm of effective therapeutic neuromodulation in the future.

Keywords

Acknowledgement

This work was supported by Myung-In Pharm, Co., LTD. (No. PHO0210321).

References

  1. van den Heuvel MP, Sporns O. Network hubs in the human brain. Trends Cogn Sci 2013;17:683-696. https://doi.org/10.1016/j.tics.2013.09.012
  2. van Diessen E, Diederen SJ, Braun KP, Jansen FE, Stam CJ. Functional and structural brain networks in epilepsy: what have we learned? Epilepsia 2013;54:1855-1865. https://doi.org/10.1111/epi.12350
  3. Raichle ME. A paradigm shift in functional brain imaging. J Neurosci 2009;29:12729-12734. https://doi.org/10.1523/JNEUROSCI.4366-09.2009
  4. Sporns O. Structure and function of complex brain networks. Dialogues Clin Neurosci 2013;15:247-262. https://doi.org/10.31887/DCNS.2013.15.3/osporns
  5. Lacruz ME, Garcia Seoane JJ, Valentin A, Selway R, Alarcon G. Frontal and temporal functional connections of the living human brain. Eur J Neurosci 2007;26:1357-1370. https://doi.org/10.1111/j.1460-9568.2007.05730.x
  6. Conner CR, Ellmore TM, DiSano MA, Pieters TA, Potter AW, Tandon N. Anatomic and electro-physiologic connectivity of the language system: a combined DTI-CCEP study. Comput Biol Med 2011;41:1100-1109. https://doi.org/10.1016/j.compbiomed.2011.07.008
  7. Koubeissi MZ, Lesser RP, Sinai A, Gaillard WD, Franaszczuk PJ, Crone NE. Connectivity between perisylvian and bilateral basal temporal cortices. Cereb Cortex 2012;22:918-925. https://doi.org/10.1093/cercor/bhr163
  8. Swann NC, Cai W, Conner CR, Pieters TA, Claffey MP, George JS, et al. Roles for the pre-supplementary motor area and the right inferior frontal gyrus in stopping action: electrophysiological responses and functional and structural connectivity. Neuroimage 2012;59:2860-2870. https://doi.org/10.1016/j.neuroimage.2011.09.049
  9. Kubota Y, Enatsu R, Gonzalez-Martinez J, Bulacio J, Mosher J, Burgess RC, et al. In vivo human hippocampal cingulate connectivity: a corticocortical evoked potentials (CCEPs) study. Clin Neurophysiol 2013;124:1547-1556. https://doi.org/10.1016/j.clinph.2013.01.024
  10. Matsuzaki N, Juhasz C, Asano E. Cortico-cortical evoked potentials and stimulation-elicited gamma activity preferentially propagate from lower- to higher-order visual areas. Clin Neurophysiol 2013;124:1290-1296. https://doi.org/10.1016/j.clinph.2013.02.007
  11. Enatsu R, Gonzalez-Martinez J, Bulacio J, Kubota Y, Mosher J, Burgess RC, et al. Connections of the limbic network: a corticocortical evoked potentials study. Cortex 2015;62:20-33. https://doi.org/10.1016/j.cortex.2014.06.018
  12. Usami K, Milsap GW, Korzeniewska A, Collard MJ, Wang Y, Lesser RP, et al. Cortical responses to input from distant areas are modulated by local spontaneous alpha/beta oscillations. Cereb Cortex 2019;29:777-787. https://doi.org/10.1093/cercor/bhx361
  13. Kobayashi K, Matsumoto R, Usami K, Matsuhashi M, Shimotake A, Kikuchi T, et al. Cortico-cortical evoked potential by single-pulse electrical stimulation is a generally safe procedure. Clin Neurophysiol 2021;132:1033-1040. https://doi.org/10.1016/j.clinph.2020.12.022
  14. Takeyama H, Matsumoto R, Usami K, Nakae T, Kobayashi K, Shimotake A, et al. Human entorhinal cortex electrical stimulation evoked short-latency potentials in the broad neocortical regions: evidence from cortico-cortical evoked potential recordings. Brain Behav 2019;9:e01366.
  15. Keller CJ, Honey CJ, Megevand P, Entz L, Ulbert I, Mehta AD. Mapping human brain networks with cortico-cortical evoked potentials. Philos Trans R Soc Lond B Biol Sci 2014;369: 20130528. https://doi.org/10.1098/rstb.2013.0528
  16. Keller CJ, Bickel S, Entz L, Ulbert I, Milham MP, Kelly C, et al. Intrinsic functional architecture predicts electrically evoked responses in the human brain. Proc Natl Acad Sci U S A 2011;108:10308-10313. https://doi.org/10.1073/pnas.1019750108
  17. Fox MD, Raichle ME. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 2007;8:700-711. https://doi.org/10.1038/nrn2201
  18. Kobayashi M, Pascual-Leone A. Transcranial magnetic stimulation in neurology. Lancet Neurol 2003;2:145-156. https://doi.org/10.1016/S1474-4422(03)00321-1
  19. Hallett M. Transcranial magnetic stimulation: a primer. Neuron 2007;55:187-199. https://doi.org/10.1016/j.neuron.2007.06.026
  20. Purpura DP, Pool JL, Ransohoff J, Frumin MJ, Housepian EM. Observations on evoked dendritic potentials of human cortex. Electroencephalogr Clin Neurophysiol 1957;9:453-459. https://doi.org/10.1016/0013-4694(57)90034-2
  21. Fritsch B, Reis J, Martinowich K, Schambra HM, Ji Y, Cohen LG, et al. Direct current stimulation promotes BDNF-dependent synaptic plasticity: potential implications for motor learning. Neuron 2010;66:198-204. https://doi.org/10.1016/j.neuron.2010.03.035
  22. Medeiros LF, de Souza IC, Vidor LP, de Souza A, Deitos A, Volz MS, et al. Neurobiological effects of transcranial direct current stimulation: a review. Front Psychiatry 2012;3:110. https://doi.org/10.3389/fpsyt.2012.00110
  23. Paulus W. Transcranial electrical stimulation (tES-tDCS; tRNS, tACS) methods. Neuropsychol Rehabil 2011;21:602-617. https://doi.org/10.1080/09602011.2011.557292
  24. Matsumoto R, Nair DR, LaPresto E, Najm I, Bingaman W, Shibasaki H, et al. Functional connectivity in the human language system: a cortico-cortical evoked potential study. Brain 2004;127(Pt 10):2316-2330. https://doi.org/10.1093/brain/awh246
  25. Prime D, Rowlands D, O'Keefe S, Dionisio S. Considerations in performing and analyzing the responses of cortico-cortical evoked potentials in stereo-EEG. Epilepsia 2018;59:16-26. https://doi.org/10.1111/epi.13939
  26. Merrill DR, Bikson M, Jefferys JG. Electrical stimulation of excitable tissue: design of efficacious and safe protocols. J Neurosci Methods 2005;141:171-198. https://doi.org/10.1016/j.jneumeth.2004.10.020
  27. Goldring S, Harding GW, Gregorie EM. Distinctive electrophysiological characteristics of functionally discrete brain areas: a tenable approach to functional localization. J Neurosurg 1994;80:701-709. https://doi.org/10.3171/jns.1994.80.4.0701
  28. Vincent M, Rossel O, Hayashibe M, Herbet G, Duffau H, Guiraud D, et al. The difference between electrical microstimulation and direct electrical stimulation-towards new opportunities for innovative functional brain mapping? Rev Neurosci 2016;27:231-258. https://doi.org/10.1515/revneuro-2015-0029
  29. Mandonnet E, Dadoun Y, Poisson I, Madadaki C, Froelich S, Lozeron P. Axono-cortical evoked potentials: a proof-of-concept study. Neurochirurgie 2016;62:67-71. https://doi.org/10.1016/j.neuchi.2015.09.003
  30. Yamao Y, Matsumoto R, Kunieda T, Arakawa Y, Kobayashi K, Usami K, et al. Intraoperative dorsal language network mapping by using single-pulse electrical stimulation. Hum Brain Mapp 2014;35:4345-4361. https://doi.org/10.1002/hbm.22479
  31. Ezure K, Oshima T. Lateral spread of neuronal activity within the motor cortex investigated with intracellular responses to distant epicortical stimulation. Jpn J Physiol 1985;35:223-249. https://doi.org/10.2170/jjphysiol.35.223
  32. Steriade M, Amzica F. Intracortical and corticothalamic coherency of fast spontaneous oscillations. Proc Natl Acad Sci U S A 1996;93:2533-2538. https://doi.org/10.1073/pnas.93.6.2533
  33. Creutzfeldt OD, Watanabe S, Lux HD. Relations between EEG phenomena and potentials of single cortical cells. I. Evoked responses after thalamic and erpicortical stimulation. Electroencephalogr Clin Neurophysiol 1966;20:1-18. https://doi.org/10.1016/0013-4694(66)90136-2
  34. Mehta AD, Ulbert I, Schroeder CE. Intermodal selective attention in monkeys. II: physiological mechanisms of modulation. Cereb Cortex 2000;10:359-370. https://doi.org/10.1093/cercor/10.4.359
  35. Keller CJ, Honey CJ, Entz L, Bickel S, Groppe DM, Toth E, et al. Corticocortical evoked potentials reveal projectors and integrators in human brain networks. J Neurosci 2014;34:9152-9163. https://doi.org/10.1523/JNEUROSCI.4289-13.2014
  36. Tamura Y, Ogawa H, Kapeller C, Prueckl R, Takeuchi F, Anei R, et al. Passive language mapping combining real-time oscillation analysis with cortico-cortical evoked potentials for awake craniotomy. J Neurosurg 2016;125:1580-1588. https://doi.org/10.3171/2015.4.jns15193
  37. Araki K, Terada K, Usui K, Usui N, Araki Y, Baba K, et al. Bidirectional neural connectivity between basal temporal and posterior language areas in humans. Clin Neurophysiol 2015;126:682-688. https://doi.org/10.1016/j.clinph.2014.07.020
  38. Panesar SS, Yeh FC, Jacquesson T, Hula W, Fernandez-Miranda JC. A quantitative tractography study into the connectivity, segmentation and laterality of the human inferior longitudinal fasciculus. Front Neuroanat 2018;12:47. https://doi.org/10.3389/fnana.2018.00047
  39. Shimotake A, Matsumoto R, Ueno T, Kunieda T, Saito S, Hoffman P, et al. Direct exploration of the role of the ventral anterior temporal lobe in semantic memory: cortical stimulation and local field potential evidence from subdural grid electrodes. Cereb Cortex 2015;25:3802-3817. https://doi.org/10.1093/cercor/bhu262
  40. Mikuni N, Miyamoto S, Ikeda A, Satow T, Taki J, Takahashi J, et al. Subtemporal hippocampectomy preserving the basal temporal language area for intractable mesial temporal lobe epilepsy: preliminary results. Epilepsia 2006;47:1347-1353. https://doi.org/10.1111/j.1528-1167.2006.00610.x
  41. Nakae T, Matsumoto R, Kunieda T, Arakawa Y, Kobayashi K, Shimotake A, et al. Connectivity gradient in the human left inferior frontal gyrus: intraoperative cortico-cortical evoked potential study. Cereb Cortex 2020;30:4633-4650. https://doi.org/10.1093/cercor/bhaa065
  42. Enatsu R, Gonzalez-Martinez J, Bulacio J, Mosher JC, Burgess RC, Najm I, et al. Connectivity of the frontal and anterior insular network: a cortico-cortical evoked potential study. J Neurosurg 2016;125:90-101. https://doi.org/10.3171/2015.6.jns15622
  43. Dionisio S, Mayoglou L, Cho SM, Prime D, Flanigan PM, Lega B, et al. Connectivity of the human insula: a cortico-cortical evoked potential (CCEP) study. Cortex 2019;120:419-442. https://doi.org/10.1016/j.cortex.2019.05.019
  44. Bou Assi E, Rihana S, Nguyen DK, Sawan M. Effective connectivity analysis of iEEG and accurate localization of the epileptogenic focus at the onset of operculo-insular seizures. Epilepsy Res 2019;152:42-51. https://doi.org/10.1016/j.eplepsyres.2019.02.006
  45. Schmahmann JD, Pandya DN, Wang R, Dai G, D'Arceuil HE, de Crespigny AJ, et al. Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. Brain 2007;130(Pt 3):630-653. https://doi.org/10.1093/brain/awl359
  46. Yakovlev PI. Motility, behavior and the brain; stereodynamic organization and neural coordinates of behavior. J Nerv Ment Dis 1948;107:313-335. https://doi.org/10.1097/00005053-194810740-00001
  47. Papez JW. A proposed mechanism of emotion. 1937. J Neuropsychiatry Clin Neurosci 1995;7:103-112. https://doi.org/10.1176/jnp.7.1.103
  48. Yamao Y, Suzuki K, Kunieda T, Matsumoto R, Arakawa Y, Nakae T, et al. Clinical impact of intraoperative CCEP monitoring in evaluating the dorsal language white matter pathway. Hum Brain Mapp 2017;38:1977-1991. https://doi.org/10.1002/hbm.23498
  49. Valentin A, Alarcon G, Honavar M, Garcia Seoane JJ, Selway RP, Polkey CE, et al. Single pulse electrical stimulation for identification of structural abnormalities and prediction of seizure outcome after epilepsy surgery: a prospective study. Lancet Neurol 2005;4:718-726. https://doi.org/10.1016/S1474-4422(05)70200-3
  50. Valentin A, Anderson M, Alarcon G, Seoane JJ, Selway R, Binnie CD, et al. Responses to single pulse electrical stimulation identify epileptogenesis in the human brain in vivo. Brain 2002;125(Pt 8):1709-1718. https://doi.org/10.1093/brain/awf187
  51. Kamada K, Kapeller C, Takeuchi F, Gruenwald J, Guger C. Tailor-Made surgery based on functional networks for intractable epilepsy. Front Neurol 2020;11:73. https://doi.org/10.3389/fneur.2020.00073
  52. Flanagan D, Valentin A, Garcia Seoane JJ, Alarcon G, Boyd SG. Single-pulse electrical stimulation helps to identify epileptogenic cortex in children. Epilepsia 2009;50:1793-1803. https://doi.org/10.1111/j.1528-1167.2009.02056.x
  53. Lega B, Dionisio S, Flanigan P, Bingaman W, Najm I, Nair D, et al. Cortico-cortical evoked potentials for sites of early versus late seizure spread in stereoelectroencephalography. Epilepsy Res 2015;115:17-29. https://doi.org/10.1016/j.eplepsyres.2015.04.009
  54. Enatsu R, Piao Z, O'Connor T, Horning K, Mosher J, Burgess R, et al. Cortical excitability varies upon ictal onset patterns in neocortical epilepsy: a cortico-cortical evoked potential study. Clin Neurophysiol 2012;123:252-260. https://doi.org/10.1016/j.clinph.2011.06.030
  55. Usami K, Matsumoto R, Kobayashi K, Hitomi T, Shimotake A, Kikuchi T, et al. Sleep modulates cortical connectivity and excitability in humans: direct evidence from neural activity induced by single-pulse electrical stimulation. Hum Brain Mapp 2015;36:4714-4729. https://doi.org/10.1002/hbm.22948
  56. Spencer SS. Neural networks in human epilepsy: evidence of and implications for treatment. Epilepsia 2002;43:219-227. https://doi.org/10.1046/j.1528-1157.2002.26901.x
  57. Kundu B, Davis TS, Philip B, Smith EH, Arain A, Peters A, et al. A systematic exploration of parameters affecting evoked intracranial potentials in patients with epilepsy. Brain Stimul 2020;13:1232-1244. https://doi.org/10.1016/j.brs.2020.06.002
  58. Parker CS, Clayden JD, Cardoso MJ, Rodionov R, Duncan JS, Scott C, et al. Structural and effective connectivity in focal epilepsy. Neuroimage Clin 2017;17:943-952.
  59. Klamer S, Rona S, Elshahabi A, Lerche H, Braun C, Honegger J, et al. Multimodal effective connectivity analysis reveals seizure focus and propagation in musicogenic epilepsy. Neuroimage 2015;113:70-77. https://doi.org/10.1016/j.neuroimage.2015.03.027
  60. Martinez-Vargas JD, Strobbe G, Vonck K, van Mierlo P, Castellanos-Dominguez G. Improved localization of seizure onset zones using spatiotemporal constraints and time-varying source connectivity. Front Neurosci 2017;11:156.
  61. van Mierlo P, Carrette E, Hallez H, Raedt R, Meurs A, Vandenberghe S, et al. Ictal-onset localization through connectivity analysis of intracranial EEG signals in patients with refractory epilepsy. Epilepsia 2013;54:1409-1418. https://doi.org/10.1111/epi.12206
  62. Chaitanya G, Toth E, Pizarro D, Iasemidis L, Murray TA, Riley K, et al. Acute modulation of the limbic network with low and high-frequency stimulation of the human fornix. Epilepsy Behav Rep 2020;14:100363. https://doi.org/10.1016/j.ebr.2020.100363
  63. Suthana N, Fried I. Percepts to recollections: insights from single neuron recordings in the human brain. Trends Cogn Sci 2012;16:427-436. https://doi.org/10.1016/j.tics.2012.06.006
  64. Beauchamp MS, Sun P, Baum SH, Tolias AS, Yoshor D. Electro-corticography links human temporoparietal junction to visual perception. Nat Neurosci 2012;15:957-959. https://doi.org/10.1038/nn.3131