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Reviews in the Neurosciences

Editor-in-Chief: Huston, Joseph P.

Editorial Board: Topic, Bianca / Adeli, Hojjat / Buzsaki, Gyorgy / Crawley, Jacqueline / Crow, Tim / Gold, Paul / Holsboer, Florian / Korth, Carsten / Li, Jay-Shake / Lubec, Gert / McEwen, Bruce / Pan, Weihong / Pletnikov, Mikhail / Robbins, Trevor / Schnitzler, Alfons / Stevens, Charles / Steward, Oswald / Trojanowski, John


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Volume 27, Issue 3

Issues

The difference between electrical microstimulation and direct electrical stimulation – towards new opportunities for innovative functional brain mapping?

Marion Vincent / Olivier Rossel / Mitsuhiro Hayashibe / Guillaume Herbet
  • Département de Neurochirurgie, Hôpital Gui de Chauliac, F-34295 Montpellier, France
  • Institut des Neurosciences de Montpellier, INSERM U1051, Hôpital Saint Eloi, F-34091 Montpellier, France
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Hugues Duffau
  • Département de Neurochirurgie, Hôpital Gui de Chauliac, F-34295 Montpellier, France
  • Institut des Neurosciences de Montpellier, INSERM U1051, Hôpital Saint Eloi, F-34091 Montpellier, France
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ David Guiraud / François Bonnetblanc
  • Corresponding author
  • INRIA, Université de Montpellier, LIRMM, équipe DEMAR, F-34095 Montpellier, France
  • Cognition, Action et Plasticité Sensorimotrice, INSERM U1093, Université de Bourgogne, UFR STAPS, F-27877 Dijon, France
  • Institut Universitaire de France, F-75005 Paris, France
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2015-12-08 | DOI: https://doi.org/10.1515/revneuro-2015-0029

Abstract

Both electrical microstimulation (EMS) and direct electrical stimulation (DES) of the brain are used to perform functional brain mapping. EMS is applied to animal fundamental neuroscience experiments, whereas DES is performed in the operating theatre on neurosurgery patients. The objective of the present review was to shed new light on electrical stimulation techniques in brain mapping by comparing EMS and DES. There is much controversy as to whether the use of DES during wide-awake surgery is the ‘gold standard’ for studying the brain function. As part of this debate, it is sometimes wrongly assumed that EMS and DES induce similar effects in the nervous tissues and have comparable behavioural consequences. In fact, the respective stimulation parameters in EMS and DES are clearly different. More surprisingly, there is no solid biophysical rationale for setting the stimulation parameters in EMS and DES; this may be due to historical, methodological and technical constraints that have limited the experimental protocols and prompted the use of empirical methods. In contrast, the gap between EMS and DES highlights the potential for new experimental paradigms in electrical stimulation for functional brain mapping. In view of this gap and recent technical developments in stimulator design, it may now be time to move towards alternative, innovative protocols based on the functional stimulation of peripheral nerves (for which a more solid theoretical grounding exists).

Keywords: behaviour; direct electrical stimulation; electrical microstimulation; electrophysiology; functional brain mapping

References

  • Agnew, W.F. and McCreery, D.B. (1987). Considerations for safety in the use of extracranial stimulation for motor evoked potentials. Neurosurgery 20, 143–147.Google Scholar

  • Asanuma, H. and Rosén, I. (1972). Topographical organization of cortical efferent zones projecting to distal forelimb muscles in the monkey. Exp. Brain Res. 14, 243–256.Google Scholar

  • Asanuma, H. and Sakata, H. (1967). Functional organization of a cortical efferent system examined with focal depth stimulation in cats. J. Neurophysiol. 30, 35–54.Google Scholar

  • Bello, L., Riva, M., Fava, E., Ferpozzi, V., Castellano, A., Raneri, F., Pessina, F., Bizzi, A., Falini, A., and Cerri, G. (2014). Tailoring neurophysiological strategies with clinical context enhances resection and safety and expands indications in gliomas involving motor pathways. Neuro. Oncol. 16, 1110–1128.Google Scholar

  • Berger, M.S. and Rostomily, R.C. (1997). Low grade gliomas: functional mapping resection strategies, extent of resection, and outcome. J. Neurooncol. 34, 85–101.Google Scholar

  • Berger, M.S., Ghatan, S., Haglund, M.M., Dobbins, J., and Ojemann, G.A. (1993). Low-grade gliomas associated with intractable epilepsy: seizure outcome utilizing electrocorticography during tumour resection. J. Neurosurg. 79, 62–69.Google Scholar

  • Bhadra, N. and Kilgore, K.L. (2005). High-frequency electrical conduction block of mammalian peripheral motor nerve. Muscle Nerve 32, 782–790.Google Scholar

  • Bishop, P.O., Burke, W., and Davis, R. (1962). Single-unit recording from antidromically activated optic radiation neurones. J. Physiol. 162, 432–450.Google Scholar

  • Bizzi, E. (1967). Discharge of frontal eye field neurons during eye movements in unanesthetized monkeys. Science 157, 1588–1590.Google Scholar

  • Bonnetblanc, F., Desmurget, M., and Duffau, H. (2006). Low grade gliomas and cerebral plasticity: fundamental and clinical implications. Med. Sci. 22, 389–394.Google Scholar

  • Borchers, S., Himmelbach, M., Logothetis, N., and Karnath, H.O. (2012). Direct electrical stimulation of human cortex – the gold standard for mapping brain functions? Nat. Rev. Neurosci. 13, 63–70.Google Scholar

  • Braitenberg, V. and Schüz, A. (1998). Cortex: Statistics and Geometry of Neuronal Connectivity (Berlin: Springer).Google Scholar

  • Bruce, C.J., Goldberg, M.E., Bushnell, M.C., and Stanton, G.B. (1985). Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements. J. Neurophysiol. 54, 714–734.Google Scholar

  • Butovas, S. and Schwarz, C. (2007). Detection psychophysics of intracortical micro-stimulation in rat primary somatosensory cortex. Eur. J. Neurosci. 25, 2161–2169.Google Scholar

  • Cheney, P.D., Griffin, D.M., and Van Acker, G.M. (2013). Neural hijacking: action of high-frequency electrical stimulation on cortical circuits. Neuroscientist 19, 434–441.Google Scholar

  • Classen, J., Liepert, J., Wise, S.P., Hallett, M., and Cohen, L.G. (1998). Rapid plasticity of human cortical movement representation induced by practice. J. Neurophysiol. 79, 1117–1123.Google Scholar

  • Cole, K.S. (1968). Membranes, Ions, and Impulses: A Chapter of Classical Biophysics (Berkeley: University of California Press).Google Scholar

  • Crone, N.E., Miglioretti, D.L., Gordon, B., Sieracki, J.M., Wilson, M.T., Uematsu, S., and Lesser, R.P. (1998). Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis: I. Alpha and beta event-related desynchronization. Brain 121, 2271–2299.Google Scholar

  • Cushing, H. (1909). A note upon the faradic stimulation upon the postcentral gyrus in conscious patients. Brain 32, 44–53.Google Scholar

  • De Witt Hamer, P.C., Robles, S.G., Zwinderman, A.H., Duffau, H., and Berger, M.S. (2012). Impact of intraoperative stimulation brain mapping on glioma surgery outcome: a meta-analysis. J. Clin. Oncol. 30, 2559–2565.Google Scholar

  • Desmurget, M., Bonnetblanc, F., and Duffau, H. (2007). Contrasting acute and slow-growing lesions: a new door to brain plasticity. Brain 130, 898–914.Google Scholar

  • Desmurget, M., Reilly, K.T., Richard, N., Szathmari, A., Mottolese, C., and Sirigu, A. (2009). Movement intention after parietal cortex stimulation in humans. Science 324, 811–813.Google Scholar

  • Desmurget, M., Song, Z., Mottolese, C., and Sirigu, A. (2013). Re-establishing the merits of electrical brain stimulation. Trends Cogn. Sci. 17, 442–449.Google Scholar

  • du Boisgueheneuc, F., Levy, R., Volle, E., Seassau, M., Duffau, H., Kinkingnehun, S., Samson, Y., Zhang, S., and Dubois, B. (2006). Functions of the left superior frontal gyrus in humans: a lesion study. Brain 129, 3315–3328.Google Scholar

  • Duffau, H. (2001). Acute functional reorganisation of the human motor cortex during resection of central lesions: a study using intraoperative brain mapping. J. Neurol. Neurosurg. Psychiatry 70, 506–513.Google Scholar

  • Duffau, H. (2004). Cartographie fonctionnelle per-opératoire par stimulations électriques directes. Neurochirurgie 50, 474–483.Google Scholar

  • Duffau, H. (2005). Lessons from brain mapping in surgery for low-grade glioma: insights into associations between tumour and brain plasticity. Lancet Neurol. 4, 476–486.Google Scholar

  • Duffau, H. (2006). New concepts in surgery of WHO grade II gliomas: functional brain mapping, connectionism and plasticity – a review. J. Neurooncol. 79, 77–115.Google Scholar

  • Duffau, H. (2014). The huge plastic potential of adult brain and the role of connectomics: new insights provided by serial mappings in glioma surgery. Cortex 58, 325–337.Google Scholar

  • Duffau, H. (2015) Stimulation mapping of white matter tracts to study brain functional connectivity. Nat Rev Neurol. 11, 255–265.Google Scholar

  • Duffau, H., Sichez, J.P., and Lehéricy, S. (2000). Intraoperative unmasking of brain redundant motor sites during resection of a precentral angioma: evidence using direct cortical stimulation. Ann. Neurol. 47, 132–135.Google Scholar

  • Duffau, H., Capelle, L., Sichez, N., Denvil, D., Lopes, M., Sichez, J., Bitar, A., and Fohanno, D. (2002). Intraoperative mapping of the subcortical language pathways using direct stimulations. An anatomo-functional study. Brain 125, 199–214.Google Scholar

  • Duffau, H., Lopes, M., Arthuis, F., Bitar, A., Sichez, J.-P., Van Effenterre, R., and Capelle, L. (2005). Contribution of intraoperative electrical stimulations in surgery of low grade gliomas: a comparative study between two series without (1985–1996) and with (1996–2003) functional mapping in the same institution. J. Neurol. Neurosurg. Psychiatry 76, 845–851.Google Scholar

  • Duffau, H., Peggy Gatignol, S.T., Mandonnet, E., Capelle, L., and Taillandier, L. (2008). Intraoperative subcortical stimulation mapping of language pathways in a consecutive series of 115 patients with Grade II glioma in the left dominant hemisphere. J. Neurosurg. 109, 461–471.Google Scholar

  • Duffau, H., Moritz-Gasser, S., and Mandonnet, E. (2014). A re-examination of neural basis of language processing: proposal of a dynamic hodotopical model from data provided by brain stimulation mapping during picture naming. Brain Lang. 131, 1–10.Google Scholar

  • Durand, D. (1999). Electric stimulation of excitable tissue. In: The Biomedical Engineering Handbook, 2nd ed. J. D. Bronzino, ed. (Boca Raton, FL: CRC Press).Google Scholar

  • Ekstrom, L.B., Roelfsema, P.R., Arsenault, J.T., Bonmassar, G., and Vanduffel, W. (2008). Bottom-up dependent gating of frontal signals in early visual cortex. Science 321, 414–417.Google Scholar

  • Enatsu, R., Matsumoto, R., Piao, Z., O’Connor, T., Horning, K., Burgess, R.C., Bulacio, J., Bingaman, W., and Nair, D.R. (2013). Cortical negative motor network in comparison with sensorimotor network: a corticocortical evoked potential study. Cortex 49, 2080–2096.Google Scholar

  • Ferraina, S., Paré, M., and Wurtz, R.H. (2002) Comparison of corticocortical and cortical-collicular signals for the generation of saccadic eye movements. J. Neurophysiol. 87, 845–858.Google Scholar

  • Ferrier, D. (1874). Experiments on the brain of monkeys. Proc. R. Soc. Lond. 23, 409–430.Google Scholar

  • Foerster, O. and Altenburger, H. (1935) Elektrobiologische Vorgänge an der menschlichen Hirnrinde. Dtsch. Z. Nervenheilkd. 135, 277–288.Google Scholar

  • Fritsch, G. and Hitzig, E. (2009). Electric excitability of the cerebrum [Uber die elektrische Erregbarkeit des Grosshirns, 1870]. Epilepsy Behav. 15, 123–130.Google Scholar

  • Geddes, L.A. (1994). The first stimulators-reviewing the history of electrical stimulation and the devices crucial to its development. IEEE Eng. Med. Biol. 13, 532–542.Google Scholar

  • Geddes, L.A. (2004). Accuracy limitations of chronaxie values. IEEE Trans. Biomed. Eng. 51, 176–181.Google Scholar

  • Geddes, L.A. and Baker, L.E. (1967). The specific resistance of biological material – a compendium of data for the biomedical engineer and physiologist. Med. Biol. Eng. 5, 271–293.Google Scholar

  • Girvin, J.P. (1986). Cerebral (cortical) biostimulation. Pace 9, 764–771.Google Scholar

  • Gordon, B., Lesser, R.P., Rance, N.E., Hart, J., Webber, R., Uematsu, S., and Fisher, R.S. (1990). Parameters for direct cortical electrical stimulation in the human: histopathologic confirmation. Electroencephalogr. Clin. Neurophysiol. 75, 371–377.Google Scholar

  • Gorman, P.H. and Mortimer, J.T. (1983). The effect of stimulus parameters on the recruitment characteristics of direct nerve stimulation. IEEE Trans. Biomed. Eng. 30, 407–414.Google Scholar

  • Graziano, M.S.A., Taylor, C.S.R., and Moore, T. (2002a). Complex movements evoked by microstimulation of precentral cortex. Neuron 34, 841–851.Google Scholar

  • Graziano, M.S.A., Taylor, C.S.R., Moore, T., and Cooke, D.F. (2002b). The cortical control of movement revisited. Neuron 36, 349–362.Google Scholar

  • Griffin, D.M., Hudson, H.M., Belhaj-Saïf, A., and Cheney, P.D. (2011). Hijacking cortical motor output with repetitive microstimulation. J. Neurosci. 31, 13088–13096.Google Scholar

  • Griffin, D.M., Hudson, H.M., Belhaj-Saïf, A., and Cheney, P.D. (2014). EMG activation patterns associated with high frequency, long-duration intracortical microstimulation of primary motor cortex. J. Neurosci. 34, 1647–1656.Google Scholar

  • Grill, W.M. and Mortimer, J.T. (1995). Stimulus waveforms for selective neural stimulation. IEEE Eng. Med. Biol. 14, 375–385.Google Scholar

  • Guiraud, D. (2012). Interfacing the neural system to restore deficient functions: from theoretical studies to neuroprothesis design. C. R. Biol. 335, 1–8.Google Scholar

  • Haglund, M.M., Berger, M.S., Shamseldin, M., Lettich, E., and Ojemann, G.A. (1994). Cortical localization of temporal lobe language sites in patients with gliomas. Neurosurgery 34, 567–576.Google Scholar

  • Hamer, H.M., Lüders, H.O., Rosenow, F., and Najm, I. (2002). Focal clonus elicited by electrical stimulation of the motor cortex in humans. Epilepsy Res. 51, 155–166.Google Scholar

  • Histed, M.H., Bonin, V., and Reid, R.C. (2009). Direct activation of sparse, distributed populations of cortical neurons by electrical microstimulation. Neuron 63, 508–522.Google Scholar

  • Histed, M.H., Ni, A.M., and Maunsell, J.H.R. (2013). Insights into cortical mechanisms of behavior from microstimulation experiments. Prog. Neurobiol. 103, 115–130.Google Scholar

  • Hodgkin, A.L. and Katz, B. (1949). The effect of sodium ions on the electrical activity of giant axon of the squid. J. Physiol. 108, 37–77.Google Scholar

  • Ius, T., Angelini, E., Thiebaut de Schotten, M., Mandonnet, E., and Duffau, H. (2011). Evidence for potentials and limitations of brain plasticity using an atlas of functional resectability of WHO grade II gliomas: towards a “minimal common brain”. Neuroimage 56, 992–1000.Google Scholar

  • Keles, G.E., Lundin, D.A., Lamborn, K.R., Chang, E.F., Ojemann, G., and Berger, M.S. (2004). Intraoperative subcortical stimulation mapping for hemispherical perirolandic gliomas located within or adjacent to the descending motor pathways: evaluation of morbidity and assessment of functional outcome in 294 patients. J. Neurosurg. 100, 369–375.Google Scholar

  • Keller, C.J., Bickel, S., Entz, L., Ulbert, I., Milham, M.P., Kelly, C., and Mehta, A.D. (2011). Intrinsic functional architecture predicts electrically evoked responses in the human brain. Proc. Natl. Acad. Sci. USA 108, 10308–10313.Google Scholar

  • Keller, C.J., Honey, C.J., Mégevand, P., Entz, L., Ulbert, I., and Mehta, A.D. (2014). Mapping human brain networks with corticocortical evoked potentials. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 369: pii: 20130528.Google Scholar

  • Kimmel, D.L. and Moore, T. (2007). Temporal patterning of saccadic eye movement signals. J. Neurosci. 27, 7619–7630.Google Scholar

  • Klaes, C., Shi, Y., Kellis, S., Minxha, J., Revechkis, B. and Andersen, R.A. (2014). A cognitive neuroprosthetic that uses cortical stimulation for somatosensory feedback. J Neural Eng. 11, 056024.Google Scholar

  • Kombos, T. and Süss, O. (2009). Neurophysiological basis of direct cortical stimulation and applied neuroanatomy of the motor cortex: a review. Neurosurg. Focus 27, E3.Google Scholar

  • Kombos, T., Suess, O., Kern, B.C., Funk, T., Hoell, T., Kopetsch, O., and Brock, M. (1999). Comparison between monopolar and bipolar electrical stimulation of the motor cortex. Acta Neurochir. 141, 1295–1301.Google Scholar

  • Kombos, T., Suess, O., Funk, T., Kern, B.C., and Brock, M. (2000). Intra-operative mapping of the motor cortex during surgery in and around the motor cortex. Acta Neurochir. 142, 263–268.Google Scholar

  • Kraskov, A., Prabhu, G., Quallo, M.M., Lemon, R.N., and Brochier, T. (2011). Ventral premotor-motor cortex interactions in the macaque monkey during grasp: response of single neurons to intracortical microstimulation. J. Neurosci. 31, 8812–8821.Google Scholar

  • Krause, F. (1909). Die operative behandlung der épilepsie. Med. Klin. 5, 1418–1422.Google Scholar

  • Lapicque, L. (1907). Recherches quantitatives sur l’excitation électrique des nerfs traitée comme une polarisation. J. Physiol. Pathol. Gen. 9, 620–635.Google Scholar

  • Lemon, R.N. (1984). Methods for neuronal recording in conscious animals. In: IBRO Handbook Series: Methods in Neurosciences, vol. 4. A.D. Smith, ed. (Chichester, New York: Wiley), pp. 1–162.Google Scholar

  • Lemon, R.N. (2008). Descending pathways in motor control. Annu. Rev. Neurosci. 31, 195–218.Google Scholar

  • Leyton, A.S.F. and Sherrington, C.S. (1917). Observations on the excitable cortex of the chimpanzee, orang-outan, and gorilla. Exp. Phys. 11, 135–222.Google Scholar

  • Logothetis, N.K., Augath, M., Murayama, Y., Rauch, A., Sultan, F., Goense, J., Oeltermann, A., and Merkle, H. (2010). The effects of electrical microstimulation on cortical signal propagation. Nat. Neurosci. 13, 1283–1291.Google Scholar

  • Maciejasz, P., Badia, J. Boretius, T., Andreu, D., Stieglitz, T., Jensen, W., Navarro, X., and Guiraud, D. (2015). Delaying discharge after the stimulus significantly decreases muscle activation thresholds with small impact on the selectivity: an in vivo study using TIME. Med. Biol. Eng. Comput. 53, 371–379.Google Scholar

  • Maier, M.A., Kirkwood, P.A., Brochier, T., and Lemon, R.N. (2013). Responses of single corticospinal neurons to intracortical stimulation of primary motor and premotor cortex in the anesthetized macaque monkey. J. Neurophysiol. 109, 2982–2998.Google Scholar

  • Mandonnet, E., Winkler, P.A., and Duffau, H. (2010). Direct electrical stimulation as an input gate into brain functional networks: principles, advantages and limitations. Acta Neurochir. 152, 185–193.Google Scholar

  • Matsumoto, R., Nair, D.R., LaPresto, E., Najm, I., Bingaman, W., Shibasaki, H., and Lüders, H.O. (2004). Functional connectivity in the human language system: a corticocortical evoked potential study. Brain 127, 2316–2330.Google Scholar

  • Matsumoto, R., Nair, D.R., LaPresto, E., Bingaman, W., Shibasaki, H., and Lüders, H.O. (2007). Functional connectivity in human cortical motor system: a corticocortical evoked potential study. Brain 130, 181–197.Google Scholar

  • McNeal, D.R. (1976). Analysis of a model for excitation of myelinated nerve. IEEE Trans. Biomed. Eng. 23, 329–337.Google Scholar

  • Merrill, D.R., Bikson, M., and Jefferys, J.G.R. (2005). Electrical stimulation of excitable tissue: design of efficacious and safe protocols. J. Neurosci. Methods 141, 171–198.Google Scholar

  • Moore, T. and Fallah, M. (2001). Control of eye movements and spatial attention. Proc. Natl. Acad. Sci. USA 98, 1273–1276.Google Scholar

  • Moore, T. and Fallah, M. (2004). Microstimulation of the frontal eye field and its effects on covert spatial attention. J. Neurophysiol. 91, 152–162.Google Scholar

  • Movshon, J.A. and Newsome, W.T. (1996). Visual response properties of striate cortical neurons projecting to area MT in macaque monkeys. J. Neurosci. 16, 7733–7741.Google Scholar

  • Murasugi, C.M., Salzman, C.D., and Newsome, W.T. (1993). Microstimulation in visual area MT: effects of varying pulse amplitude and frequency. J. Neurosci. 13, 1719–1729.Google Scholar

  • Murphey, D.K. and Maunsell, J.H.R. (2007). Behavioral detection of electrical microstimulation in different cortical visual areas. Curr. Biol. 17, 862–867.Google Scholar

  • Nathan, S.S., Sinha, S.R., Gordon, B., Lesser, R.P., and Thakor, N.V. (1993). Determination of current density distributions generated by electrical stimulation of the human cerebral cortex. Electroencephalogr Clin. Neurophysiol. 86, 183–192.Google Scholar

  • Neuloh, G., Pechstein, U., and Schramm, J. (2007). Motor tract monitoring during insular glioma surgery. J. Neurosurg. 106, 582–592.Google Scholar

  • Nowak, L.G. and Bullier, J. (1998). Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter: I. Evidence from chronaxie measurements. Exp. Brain Res. 118, 477–488.Google Scholar

  • O’Doherty, J.E., Lebedev, M.A., Ifft, P.J., Zhuang, K.Z., Shokur, S., Bleuler, H. and Nicolelis, M.A. (2011). Active tactile exploration enabled by a brain-machine-brain interface. Nature 479, 228–231.Google Scholar

  • Ojemann, G., Ojemann, J., Lettich, E., and Berger, M. (1989). Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J. Neurosurg. 71, 316–326.Google Scholar

  • Penfield, W. (1947). Some observations on the cerebral cortex of man. Proc. R. Soc. Lond. B. Biol. Sci. 134, 329–347.Google Scholar

  • Penfield, W. and Boldrey, E. (1937) Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 60, 389–443.Google Scholar

  • Purpura, D.P., Pool, J.L., Ransohoff, J., Frumin, M.J., and Housepian, E.M. (1957) Observation on evoked dendritic potentials of human cortex. Electroencephalogr. Clin. Neurophysiol. 9, 453–459.Google Scholar

  • Purves, D., Augustine, G.J., Fitzpatrick, D., Katz, C.L., LaMantia, A.S., O McNamara, J., and Williams, S.M. (2001). Neuroscience, 2nd ed. (Sunderland: Sinauer Associates).Google Scholar

  • Ranck, J.B. (1975). Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res. 98, 417–440.Google Scholar

  • Rathelot, J.A. and Strick, P.L. (2006). Muscle representation in the macaque motor cortex: an anatomical perspective. Proc. Natl. Acad. Sci. USA 103, 8257–8262.Google Scholar

  • Rattay, F. (1999). The basic mechanism for the electrical stimulation of the nervous system. Neuroscience 89, 335–346.Google Scholar

  • Rattay, F., Paredes, L.P., and Leao, R.N. (2012). Strength-duration relationship for intra- versus extracellular stimulation with microelectrodes. Neuroscience 214, 1–13.Google Scholar

  • Rech, F., Herbet, G., Moritz-Gasser, S., and Duffau, H. (2013). Disruption of bimanual movement by unilateral subcortical electrostimulation. Hum. Brain Mapp. 35, 3439–3445.Google Scholar

  • Robinson, D.A. and Fuchs, A.F. (1969). Eye movements evoked by stimulation of frontal eye fields. J. Neurophysiol. 32, 637–648.Google Scholar

  • Romo, R., Hernández, A., Zainos, A., and Salinas, E. (1998). Somatosensory discrimination based on cortical microstimulation. Nature 392, 387–390.Google Scholar

  • Rosén, I. and Asanuma, H. (1972). Peripheral afferent inputs to the forelimb area of the monkey motor cortex: input-output relations. Exp. Brain Res. 14, 257–273.Google Scholar

  • Salzman, C.D., Murasugi, C.M., Britten, K.H., and Newsome, W.T. (1992). Microstimulation in visual area MT: effects on direction discrimination performance. J. Neurosci. 12, 2331–2355.Google Scholar

  • Sanai, N. and Berger, M.S. (2008). Glioma extent of resection and its impact on patient outcome. Neurosurgery 62, 753–764.Google Scholar

  • Sanai, N., Mirzadeh, Z., and Berger, M.S. (2008). Functional outcome after language mapping for glioma resection. N. Engl. J. Med. 358, 18–27.Google Scholar

  • Schucht, P., Moritz-Gasser, S., Herbet, G., Raabe, A., and Duffau, H. (2013). Subcortical electrostimulation to identify network subserving motor control. Hum. Brain Mapp. 34, 3023–3030.Google Scholar

  • Seidel, K., Beck, J., Stieglitz, L., Schucht, P., and Raabe, A. (2012). Low-threshold monopolar motor mapping for resection of primary motor cortex tumours. Neurosurgery 71, 104–114.Google Scholar

  • Sherrington, C.S., and Grünbaum, A.S.F. (1901). An Address on Localisation in the “motor” Cerebral Cortex. The British Medical Journal 2, 1857–1859.Google Scholar

  • Sinai, A., Bowers, C.W., Crainiceanu, C.M., Boatman, D., Gordon, B., Lesser, R.P., Lenz, F.A., and Crone, N.E. (2005). Electrocorticographic high gamma activity versus electrical cortical stimulation mapping of naming. Brain 128, 1556–1570.Google Scholar

  • Smith, J.S., Chang, E.F., Lamborn, K.R., Chang, S.M., Prados, M.D., Cha, S., Tihan, T., Vandenberg, S., McDermott, M.W., and Berger, M.S. (2008). Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J. Clin. Oncol. 26, 1338–1345.Google Scholar

  • Sommer, M.A. and Wurtz, R.H. (2002). A pathway in primate brain for internal monitoring of movements. Science 296, 1480–1482.Google Scholar

  • Stoney, S.D., Thompson, W.D., and Asanuma, H. (1968). Excitation of pyramidal tract cells by intracortical microstimulation: effective extent of stimulating current. J. Neurophysiol. 31, 659–669.Google Scholar

  • Strick, P.L. (2002). Stimulating research on motor cortex. Nat. Neurosci. 5, 714–715.Google Scholar

  • Stuart, G., Schiller, J., and Sakmann, B. (1997). Action potential initiation and propagation in rat neocortical pyramidal neurons. J. Physiol. 505, 617–632.Google Scholar

  • Szelényi, A., Bello, L., Duffau, H., Fava, E., Feigl, G.C., Galanda, M., Neuloh, G., Signorelli, F., and Sala, F. (2010). Intraoperative electrical stimulation in awake craniotomy: methodological aspects of current practice. Neurosurg. Focus 28, E7.CrossrefGoogle Scholar

  • Szelényi, A., Senft, C., Jardan, M., Forster, M.T., Franz, K., Seifert, V., and Vatter, H. (2011). Intra-operative subcortical electrical stimulation: a comparison of two methods. Clin. Neurophysiol. 122, 1470–1475.Google Scholar

  • Tan, D.W., Schiefer, M.A., Keith, M.W., Anderson, J.R., Tyler, J., and Tyler, D.J. (2014). A neural interface provides long-term stable natural touch perception. Sci. Transl. Med. 6, 257ra138.Google Scholar

  • Taniguchi, A.M., Cedzich, C., and Schramm, J. (1993). Modification of cortical stimulation for motor evoked potentials under general anesthesia: technical description. Neurosurgery 32, 219–226.Google Scholar

  • Tate, M.C., Herbet, G., Moritz-Gasser, S., Tate, J.E., and Duffau, H. (2014). Probabilistic map of critical functional regions of the human cerebral cortex: Broca’s area revisited. Brain 137, 2773–2782.Google Scholar

  • Tehovnik, E.J. (1996). Electrical stimulation of neural tissue to evoke behavioral responses. J. Neurosci. Methods 65, 1–17.Google Scholar

  • Tehovnik, E.J., Tolias, A S., Sultan, F., Slocum, W.M., and Logothetis, N.K. (2006). Direct and indirect activation of cortical neurons by electrical microstimulation. J. Neurophysiol. 96, 512–521.Google Scholar

  • Teixidor, P., Gatignol, P., Leroy, M., Masuet-Aumatell, C., Capelle, L., and Duffau, H. (2007). Assessment of verbal working memory before and after surgery for low-grade glioma. J. Neurooncol. 81, 305–313.Google Scholar

  • Thiebaut de Schotten, M., Urbanski, M., Duffau, H., Volle, E., Lévy, R., Dubois, B., and Bartolomeo, P. (2005). Direct evidence for a parietal-frontal pathway subserving spatial awareness in humans. Science 309, 2226–2228.Google Scholar

  • Tolias, A.S., Sultan, F., Augath, M., Oeltermann, A., Tehovnik, E.J., Schiller, P.H., and Logothetis, N.K. (2005). Mapping cortical activity elicited with electrical microstimulation using FMRI in the macaque. Neuron 48, 901–911.Google Scholar

  • Vansteensel, M.J., Bleichner, M.G., Dintzner, L.T., Aarnoutse, E.J., Leijten, F.S.S., Hermes, D., and Ramsey, N.F. (2013). Task-free electrocorticography frequency mapping of the motor cortex. Clin. Neurophysiol. 124, 1169–1174.Google Scholar

  • Vogt, C. and Vogt, O. (1919) Allgemeinere Ergebnisse unserer Hirnforschung. J. Psychol. Neurol. 25, 277–461.Google Scholar

  • Warman, E.N., Grill, W.M., and Durand, D. (1992). Modeling the effects of electric fields on nerve fibers: determination of excitation thresholds. IEEE Trans. Biomed. Eng. 39, 1244–1254.Google Scholar

  • Weiss, G. (1901). Sur la possibilité de rendre comparables entre eux les appareils servant à l’excitation. Arch. Ital. Biol. 35, 413–446.Google Scholar

  • Williams, Z.M. and Eskandar, E.N. (2006). Selective enhancement of associative learning by microstimulation of the anterior caudate. Nat. Neurosci. 9, 562–568.Google Scholar

  • Yamao, Y., Matsumoto, R., Kunieda, T., Arakawa, Y., Kobayashi, K., Usami, K., Shibata, S., Kikuchi, T., Sawamoto, N., Mikuni, N., et al. (2014a). Intraoperative dorsal language network mapping by using single-pulse electrical stimulation. Hum. Brain Mapp. 35, 4345–4361.Google Scholar

  • Yamao, Y., Matsumoto, R., Kunieda, T., Shibata, S., Shimotake, A., Kikuchi, T., Satow, T., Mikuni, N., Fukuyama, H., Ikeda, A., et al. (2014b). Neural correlates of mirth and laughter: a direct electrical cortical stimulation study. Cortex 66, 134–140.Google Scholar

  • Yamao, Y., Kunieda, T., and Matsumoto, R. (2015). Reply to Commentary on “Neural correlates of mirth and laughter: a direct electrical cortical stimulation study”. Cortex. pii: S0010-9452(15)00110-0.Google Scholar

  • Yordanova, Y.N., Moritz-Gasser, S., and Duffau, H. (2011). Awake surgery for WHO Grade II gliomas within “noneloquent” areas in the left dominant hemisphere: toward a “supratotal” resection. J. Neurosurg. 115, 232–239.Google Scholar

About the article

Corresponding author: François Bonnetblanc, INRIA, Université de Montpellier, LIRMM, équipe DEMAR, F-34095 Montpellier, France; Cognition, Action et Plasticité Sensorimotrice, INSERM U1093, Université de Bourgogne, UFR STAPS, F-27877 Dijon, France; and Institut Universitaire de France, F-75005 Paris, France, e-mail:


Received: 2015-06-23

Accepted: 2015-10-17

Published Online: 2015-12-08

Published in Print: 2016-04-01


Citation Information: Reviews in the Neurosciences, Volume 27, Issue 3, Pages 231–258, ISSN (Online) 2191-0200, ISSN (Print) 0334-1763, DOI: https://doi.org/10.1515/revneuro-2015-0029.

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