Abstract
Direct electrical stimulation (DES) is used to perform functional brain mapping during awake surgery and in epileptic patients. DES may be coupled with the measurement of Evoked Potentials (EP) to study the conductive and integrative properties of activated neural ensembles and probe the spatiotemporal dynamics of short- and long-range networks. However, its electrophysiological effects remain by far unknown. We recorded ECoG signals on two patients undergoing awake brain surgery and measured EP on functional sites after cortical stimulations and were the firsts to record three different types of EP on the same patients. Using low-intensity (1–3 mA) to evoke electrogenesis we observed that: (i) “true” remote EPs are attenuated in amplitude and delayed in time due to the divergence of white matter pathways; (ii) “false” remote EPs are attenuated but not delayed: as they originate from the same electrical source; (iii) Singular but reproducible positive components in the EP can be generated when the DES is applied in the temporal lobe or the premotor cortex; and (iv) rare EP can be triggered when the DES is applied subcortically: these can be either negative, or surprisingly, positive. We proposed different activation and electrophysiological propagation mechanisms following DES, based on the nature of activated neural elements and discussed important methodological pitfalls when measuring EP in the brain. Altogether, these results pave the way to map the connectivity in real-time between the DES and the recording sites; to characterize the local electrophysiological states and to link electrophysiology and function. In the future, and in practice, this technique could be used to perform electrophysiological mapping in order to link (non)-functional to electrophysiological responses with DES and could be used to guide the surgical act itself.
Similar content being viewed by others
References
Adrian E (1936) The spread of activity in the cerebral cortex. J Physiol 88(2):127–161
Boyer A, Duffau H; Vincent M, Ramdani S, Mandonnet E, Guiraud D, Bonnetblanc F (2018) Electrophysiological activity evoked by direct electrical stimulation of the human brain: interest of the P0 component. Conf Proc IEEE Eng Med Biol Soc, pp. 2210–2213
Boyer A, Duffau H, Mandonnet E; Vincent MA, Ramdani S, Guiraud D, Bonnetblanc F (2019) Attenuation and delay of remote potentials evoked by direct electrical stimulation during brain surgery. Brain Topogr. https://doi.org/10.1007/s10548-019-00732-w
Buzsáki G, Anastassiou C, Koch C (2012) The origin of extracellular fields and currents: EEG, ECoG, LFP and spikes. Nat Rev Neurosci 13(6):407–420
Deras P, Moulinié G, Maldonado IL, Moritz-Gasser S, Duffau H, Bertram L (2012) Intermittent general anesthesia with controlled ventilation for asleep-awake-asleep brain surgery: a prospective series of 140 gliomas in eloquent areas. Neurosurgery 71:764–72
Duffau H (2015) Stimulation mapping of white matter tracts to study brain functional connectivity. Nat Rev Neurol 11(5):255–265
Goldring S, Harding G, Gregorie E (1994) Distinctive electrophysiological characteristics of functionally discrete brain areas: a tenable approach to functional localization. J Neurosurg 80(4):701–709
Goldring S et al (1961) Direct response of human cerebral cortex. Arch Neurol 4:590–8
Kandel E, Schwartz J, Jessell T (2000) Principles of neural science, 4th edn. McGraw-Hill, New York
Landau WM, Clare MH (1956) A note on the characteristic response pattern in primary sensory projection cortex of the cat following a synchronous afferent volley. Electroencephalogr Clin Neurophysiol 8:457–464
Li C, Chou S (1962) Cortical intracellular synaptic potentials and direct cortical stimulation. J Cell Comp Physiol 60:1–16
Mandonnet E, Winkler P, Duffau H (2010) Direct electrical stimulation as an input gate into brain functional networks: principles, advantages and limitations. Acta Neurochir (Wien) 152(2):185–193
Mandonnet E, Dadoun Y, Poisson I, Madadaki C, Froelich S, Lozeron P (2016) Axono-cortical evoked potentials: a proof-of-concept study. Neurochirurgie 62:67–71
Matsumoto R et al (2007) Functional connectivity in human cortical motor system: a cortico-cortical evoked potential study. Brain 130(1):181–197
Matsumoto R et al (2004) Functional connectivity in the human language system: a cortico-cortical evoked potential study. Brain 127(10):2316–2330
Shimada S, Kunii N, Kawai K et al (2017) Impact of volume-conducted potential in interpretation of cortico-cortical evoked potential: Detailed analysis of high-resolution electrocorticography using two mathematical approaches. Clin Neurophysiol 128(4):549–557
Stohr PE, Goldring S, O’Leary JL (1963) Patterns of unit discharge associated with direct cortical response in monkey and cat. Electrocephalogr Clio Neurophysiol 15:882–888
Sugaya E, Goldring S, O’Leary JL (1964) Intracellular potentials associated with direct cortical response and seizure discharge in cat. Electrocephalogr Clio Neurophysiol 17:661–669
Vincent M et al (2016) The difference between electrical microstimulation and direct electrical stimulation: towards new opportunities for innovative functional brain mapping? Rev Neurosci 27(3):231–258
Vincent M et al (2017) Electrophysiological brain mapping: basics of recording evoked potentials induced by electrical stimulation and its physiological spreading in the human brain. Clin Neurophysiol 128(10):1886–1890
Vincent M, Bonnetblanc F, Mandonnet E, Boyer A, Duffau H, Guiraud D (2020) Measuring the electrophysiological effects of direct electrical stimulation after awake brain surgery. J Neural Eng 17(1):016047. https://doi.org/10.1088/1741-2552/ab5cdd
Yamao Y et al (2014) Intraoperative dorsal language network mapping by using single-pulse electrical stimulation. Hum Brain Map 35(9):4345–4361
Funding
Research supported by the LabEx NUMEV project (n° ANR- 10-LABX-20) funded by the French government’s “Investissements d’Avenir” program managed by the French National Research Agency (ANR) and complementary grants from the Institut Universitaire de France and INSERM laboratory (U1093).
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Stefano Seri.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Boyer, A., Ramdani, S., Duffau, H. et al. Electrophysiological Mapping During Brain Tumor Surgery: Recording Cortical Potentials Evoked Locally, Subcortically and Remotely by Electrical Stimulation to Assess the Brain Connectivity On-line. Brain Topogr 34, 221–233 (2021). https://doi.org/10.1007/s10548-020-00814-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10548-020-00814-0