Abstract
Electrical stimulation during awake brain surgery is a classic method yielding direct information about brain-behavior relationships. This technique has provided key leaps in our understanding of the organization of the brain, including the discovery of the somatotopic organization of the primary sensory and motor cortices by Wilder Penfield and his colleagues in the 1950s or the previously unsuspected degree of inter-individual variability in the cortical representations of speech and language functions by George Ojemann and colleagues. The electrical stimulation technique, combined with an array of advanced neuroimaging methods, has expanded allowing us to test not only cortical functions but also the role of underlying white matter tracts in behavior. In this chapter, we will describe the method, its evolution, and the novel types of discoveries enabled by direct cortical and subcortical electrical stimulation of the human brain.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Coltheart M, Rastle K (1994) Serial processing in reading aloud: evidence for dual-route models of reading. J Exp Psychol Hum Percept Perform 20(6):1197–1211. https://doi.org/10.1037/0096-1523.20.6.1197
Plaut DC, McClelland JL, Seidenberg MS, Patterson K (1996) Understanding normal and impaired word reading: computational principles in quasi-regular domains. Psychol Rev 103(1):56–115. https://doi.org/10.1037/0033-295x.103.1.56
Snodgrass JG, Vanderwart M (1980) A standardized set of 260 pictures: norms for name agreement, image agreement, familiarity, and visual complexity. J Exp Psychol Hum Learn 6(2):174–215. https://doi.org/10.1037/0278-7393.6.2.174
Berman J, Chung S, Mukherjee P, Hess C, Han E, Henry R (2008) Probabilistic streamline q-ball tractography using the residual bootstrap. NeuroImage 39(1):215–222. https://doi.org/10.1016/j.neuroimage.2007.08.021
Caverzasi E et al (2016) Identifying preoperative language tracts and predicting postoperative functional recovery using HARDI q-ball fiber tractography in patients with gliomas. J Neurosurg 125(1):33–45. https://doi.org/10.3171/2015.6.JNS142203
Jordan KM, Amirbekian B, Keshavan A, Henry RG (2018) Cluster confidence index: a streamline-wise pathway reproducibility metric for diffusion-weighted MRI tractography. J Neuroimaging 28(1):64–69. https://doi.org/10.1111/jon.12467
Bucci M et al (2013) Quantifying diffusion MRI tractography of the corticospinal tract in brain tumors with deterministic and probabilistic methods. NeuroImage Clin 3:361–368. https://doi.org/10.1016/j.nicl.2013.08.008
Leclercq D et al (2010) Comparison of diffusion tensor imaging tractography of language tracts and intraoperative subcortical stimulations. J Neurosurg 112(3):503–511. https://doi.org/10.3171/2009.8.JNS09558
Jones DK, Knösche TR, Turner R (2013) White matter integrity, fiber count, and other fallacies: the do’s and don’ts of diffusion MRI. NeuroImage 73:239–254. https://doi.org/10.1016/j.neuroimage.2012.06.081
Thomas C et al (2014) Anatomical accuracy of brain connections derived from diffusion MRI tractography is inherently limited. Proc Natl Acad Sci U S A 111(46):16574–16579. https://doi.org/10.1073/pnas.1405672111
Englot DJ et al (2015) Epileptogenic zone localization using magnetoencephalography predicts seizure freedom in epilepsy surgery. Epilepsia 56(6):949–958. https://doi.org/10.1111/epi.13002
Traut T et al (2019) MEG imaging of recurrent gliomas reveals functional plasticity of hemispheric language specialization. Hum Brain Mapp 40(4):1082–1092. https://doi.org/10.1002/hbm.24430
Sartorius CJ, Berger MS (1998) Rapid termination of intraoperative stimulation-evoked seizures with application of cold Ringer’s lactate to the cortex. Technical note. J Neurosurg 88(2):349–351. https://doi.org/10.3171/jns.1998.88.2.0349
Penfield W, Roberts L (1959) Speech and brain-mechanisms. Princeton University Press, Princeton
Bulsara KR, Johnson J, Villavicencio AT (2005) Improvements in brain tumor surgery: the modern history of awake craniotomies. Neurosurg Focus 18(4):e5
Harris LJ, Almerigi JB (2009) Probing the human brain with stimulating electrodes: the story of Roberts Bartholow’s (1874) experiment on Mary Rafferty. Brain Cogn 70(1):92–115. https://doi.org/10.1016/j.bandc.2009.01.008
Morgan JP (1982) The first reported case of electrical stimulation of the human brain. J Hist Med Allied Sci 37(1):51–64. https://doi.org/10.1093/jhmas/xxxvii.1.51
Eccles J, Feindel W (1978) Wilder Graves Penfield, 26 January 1891–5 April 1976. Biogr Mem Fellows R Soc 24:473–513
Feindel W (1977) Wilder Penfield: his legacy to neurology. To praise an absent friend. Can Med Assoc J 116(12):1365–1367
Penfield W (1936) Epilepsy and surgical therapy. Arch Neurol Psychiatr 36(3):449–484. https://doi.org/10.1001/archneurpsyc.1936.02260090002001
Penfield W (1941) Epilepsy and cerebral localization: a study of the mechanism, treatment and prevention of epileptic seizures, 1st edn. Charles C. Thomas, Springfield
Penfield W, Boldrey E (1937) Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain J Neurol 60:389–443. https://doi.org/10.1093/brain/60.4.389
Penfield W, Rasmussen T (1950) The cerebral cortex of man. Macmillan, New York
Ojemann GA (1979) Individual variability in cortical localization of language. J Neurosurg 50(2):164–169. https://doi.org/10.3171/jns.1979.50.2.0164
Ojemann G, Ojemann J, Lettich E, Berger M (1989) Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J Neurosurg 71(3):316–326. https://doi.org/10.3171/jns.1989.71.3.0316
Sanai N, Mirzadeh Z, Berger MS (2008) Functional outcome after language mapping for glioma resection. N Engl J Med 358(1):18–27. https://doi.org/10.1056/NEJMoa067819
Duffau H (2014) Diffuse low-grade gliomas and neuroplasticity. Diagn Interv Imaging 95(10):945–955. https://doi.org/10.1016/j.diii.2014.08.001
Duffau H (2015) Stimulation mapping of white matter tracts to study brain functional connectivity. Nat Rev Neurol 11(5):255–265. https://doi.org/10.1038/nrneurol.2015.51
Duffau H (2017) Mapping the connectome in awake surgery for gliomas: an update. J Neurosurg Sci 61(6):612–630. https://doi.org/10.23736/S0390-5616.17.04017-6
Duffau H et al (2003) Usefulness of intraoperative electrical subcortical mapping during surgery for low-grade gliomas located within eloquent brain regions: functional results in a consecutive series of 103 patients. J Neurosurg 98(4):764–778. https://doi.org/10.3171/jns.2003.98.4.0764
Duffau H et al (2002) Intraoperative mapping of the subcortical language pathways using direct stimulations. An anatomo-functional study. Brain J Neurol 125(Pt 1):199–214
Duffau H, Peggy Gatignol ST, Mandonnet E, Capelle L, 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(3):461–471. https://doi.org/10.3171/JNS/2008/109/9/0461
Duffau H, Moritz-Gasser S, 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. https://doi.org/10.1016/j.bandl.2013.05.011
Catani M, Mesulam M (2008) The arcuate fasciculus and the disconnection theme in language and aphasia: history and current state. Cortex J Devoted Study Nerv Syst Behav 44(8):953–961. https://doi.org/10.1016/j.cortex.2008.04.002
Garcea FE et al (2017) Direct electrical stimulation in the human brain disrupts melody processing. Curr Biol 27(17):2684.e7–2691.e7. https://doi.org/10.1016/j.cub.2017.07.051
Piai V, Vos SH, Idelberger R, Gans P, Doorduin J, ter Laan M (2019) Awake surgery for a violin player: monitoring motor and music performance, a case report. Arch Clin Neuropsychol 34(1):132–137. https://doi.org/10.1093/arclin/acy009
Zatorre RJ, Chen JL, Penhune VB (2007) When the brain plays music: auditory-motor interactions in music perception and production. Nat Rev Neurosci 8(7):547–558. https://doi.org/10.1038/nrn2152
Maldaun MVC et al (2014) Awake craniotomy for gliomas in a high-field intraoperative magnetic resonance imaging suite: analysis of 42 cases: clinical article. J Neurosurg 121(4):810–817. https://doi.org/10.3171/2014.6.JNS132285
Chang EF, Kurteff G, Wilson SM (2017) Selective interference with syntactic encoding during sentence production by direct electrocortical stimulation of the inferior frontal gyrus. J Cogn Neurosci 30(3):411–420. https://doi.org/10.1162/jocn_a_01215
Corina DP, Gibson EK, Martin R, Poliakov A, Brinkley J, Ojemann GA (2005) Dissociation of action and object naming: evidence from cortical stimulation mapping. Hum Brain Mapp 24(1):1–10. https://doi.org/10.1002/hbm.20063
Gras-Combe G, Moritz-Gasser S, Herbet G, Duffau H (2012) Intraoperative subcortical electrical mapping of optic radiations in awake surgery for glioma involving visual pathways: clinical article. J Neurosurg 117(3):466–473. https://doi.org/10.3171/2012.6.JNS111981
Ries SK et al (2019) Roles of ventral versus dorsal pathways in language production: an awake language mapping study. Brain Lang 191:17–27. https://doi.org/10.1016/j.bandl.2019.01.001
Rofes A, Miceli G (2014) Language mapping with verbs and sentences in awake surgery: a review. Neuropsychol Rev 24(2):185–199. https://doi.org/10.1007/s11065-014-9258-5
Glaser WR, Düngelhoff FJ (1984) The time course of picture-word interference. J Exp Psychol Hum Percept Perform 10(5):640–654
Lupker SJ (1979) The semantic nature of response competition in the picture-word interference task. Mem Cogn 7(6):485–495. https://doi.org/10.3758/BF03198265
Bürki A (2017) Electrophysiological characterization of facilitation and interference in the picture-word interference paradigm. Psychophysiology 54(9):1370–1392. https://doi.org/10.1111/psyp.12885
Costa A, Alario FX, Caramazza A (2005) On the categorical nature of the semantic interference effect in the picture-word interference paradigm. Psychon Bull Rev 12(1):125–131
Piai V, Roelofs A, Acheson DJ, Takashima A (2013) Attention for speaking: domain-general control from the anterior cingulate cortex in spoken word production. Front Hum Neurosci 7:832. https://doi.org/10.3389/fnhum.2013.00832
Piai V, Roelofs A, Jensen O, Schoffelen J-M, Bonnefond M (2014) Distinct patterns of brain activity characterise lexical activation and competition in spoken word production. PLoS One 9(2):e88674. https://doi.org/10.1371/journal.pone.0088674
Hickok G, Poeppel D (2004) Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language. Cognition 92(1–2):67–99. https://doi.org/10.1016/j.cognition.2003.10.011
Rauschecker JP, Tian B (2000) Mechanisms and streams for processing of ‘what’ and ‘where’ in auditory cortex. Proc Natl Acad Sci U S A 97(22):11800–11806. https://doi.org/10.1073/pnas.97.22.11800
Saur D et al (2008) Ventral and dorsal pathways for language. Proc Natl Acad Sci U S A 105(46):18035–18040. https://doi.org/10.1073/pnas.0805234105
Tracy JI, Hampstead BM, Sathian K (2014) Cognitive plasticity in neurologic disorders. Oxford University Press, Oxford
Robles SG, Gatignol P, Lehéricy S, Duffau H (2008) Long-term brain plasticity allowing a multistage surgical approach to World Health Organization Grade II gliomas in eloquent areas. J Neurosurg 109(4):615–624. https://doi.org/10.3171/JNS/2008/109/10/0615
Ghinda CD, Duffau H (2017) Network plasticity and intraoperative mapping for personalized multimodal management of diffuse low-grade gliomas. Front Surg 4. https://doi.org/10.3389/fsurg.2017.00003
Keller CJ, Honey CJ, Mégevand P, Entz L, Ulbert I, Mehta AD (2014) Mapping human brain networks with cortico-cortical evoked potentials. Philos Trans R Soc B Biol Sci 369(1653). https://doi.org/10.1098/rstb.2013.0528
Kunieda T, Yamao Y, Kikuchi T, Matsumoto R (2015) New approach for exploring cerebral functional connectivity: review of cortico-cortical evoked potential. Neurol Med Chir (Tokyo) 55(5):374–382. https://doi.org/10.2176/nmc.ra.2014-0388
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2022 Springer Science+Business Media, LLC, part of Springer Nature
About this protocol
Cite this protocol
Ries, S.K., Jordan, K., Knight, R.T., Berger, M. (2022). Lesion-Behavior Awake Mapping with Direct Cortical and Subcortical Stimulation. In: Pustina, D., Mirman, D. (eds) Lesion-to-Symptom Mapping. Neuromethods, vol 180. Springer, New York, NY. https://doi.org/10.1007/978-1-0716-2225-4_14
Download citation
DOI: https://doi.org/10.1007/978-1-0716-2225-4_14
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-1-0716-2224-7
Online ISBN: 978-1-0716-2225-4
eBook Packages: Springer Protocols