Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-29T12:45:46.891Z Has data issue: false hasContentIssue false

Intrahemispheric reorganization of language in children with medically intractable epilepsy of the left hemisphere

Published online by Cambridge University Press:  20 March 2007

DARREN S. KADIS
Affiliation:
Department of Psychology, University of Toronto, Toronto, Ontario, Canada Department of Psychology, Hospital for Sick Children, Toronto, Ontario, Canada
KOJI IIDA
Affiliation:
Division of Neurosurgery, Hiroshima University, Hiroshima, Japan
ELIZABETH N. KERR
Affiliation:
Department of Psychology, Hospital for Sick Children, Toronto, Ontario, Canada
WILLIAM J. LOGAN
Affiliation:
Department of Pediatrics, Division of Neurology, University of Toronto, Toronto, Ontario, Canada Department of Neurology, Hospital for Sick Children; Toronto, Ontario, Canada
MARY PAT MCANDREWS
Affiliation:
Department of Psychology, University of Toronto, Toronto, Ontario, Canada Applied and Interventional Research, Toronto Western Research Institute, Toronto, Ontario, Canada
AYAKO OCHI
Affiliation:
Department of Neurology, Hospital for Sick Children; Toronto, Ontario, Canada
HIROSHI OTSUBO
Affiliation:
Department of Pediatrics, Division of Neurology, University of Toronto, Toronto, Ontario, Canada Department of Neurology, Hospital for Sick Children; Toronto, Ontario, Canada
JAMES T. RUTKA
Affiliation:
Department of Surgery, Division of Neurosurgery, University of Toronto, and Department of Neurosurgery, Hospital for Sick Children, Toronto, Ontario, Canada
O. CARTER SNEAD III
Affiliation:
Department of Pediatrics, Division of Neurology, University of Toronto, Toronto, Ontario, Canada Department of Neurology, Hospital for Sick Children; Toronto, Ontario, Canada
SHELLY K. WEISS
Affiliation:
Department of Pediatrics, Division of Neurology, University of Toronto, Toronto, Ontario, Canada Department of Neurology, Hospital for Sick Children; Toronto, Ontario, Canada
MARY LOU SMITH
Affiliation:
Department of Psychology, University of Toronto, Toronto, Ontario, Canada Department of Psychology, Hospital for Sick Children, Toronto, Ontario, Canada

Abstract

We investigated language representation in nine children (six male, three female; 5.6–17.7 years of age) who underwent surgical treatment of medically intractable epilepsy of the left hemisphere. Although interhemispheric reorganization has been previously documented in similar groups, this is the first study to systematically evaluate possible intrahemispheric effects of early insult. All cases had left hemisphere seizure foci and underwent extraoperative stimulation mapping (ESM) for language localization prior to receiving cortical resections. To compare ESM findings across subjects and to assess intrahemispheric reorganization, we developed a novel coregistration technique whereby independent raters plotted two-dimensional (2D) ESM findings in 3D standard space. Expressive language sites identified with ESM were compared with a structural probability map of pars opercularis, or Broca's area. The average difference between independent raters' estimates of 28 language sites was 3.9 mm (SD = 2.0), indicating excellent agreement; the coregistration procedure permitted assessment of 2D ESM findings in 3D standard space. We observed language sites in regions substantially anterior and superior to canonical Broca's area, possibly reflecting intrahemispheric reorganization. Findings suggest that left hemisphere insult in young children may result in anterior displacement of language within the frontal cortex. (JINS, 2007, 13, 505–516.)This study was drawn from a thesis submitted by D.S.K. in partial fulfillment of requirements of the MA degree through the Graduate Program in Psychology and the Collaborative Program in Neuroscience at the University of Toronto (Ontario, Canada).

Type
NEUROBEHAVIORAL GRAND ROUNDS
Copyright
© 2007 The International Neuropsychological Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Akai, T., Otsubo, H., Pang, E.W., Rutka, J.T., Chitoku, S., Weiss, S.K., & Snead, O.C., III. (2002). Complex central cortex in pediatric patients with malformations of cortical development. Journal of Child Neurology, 17, 347352.Google Scholar
Bates, E., Reilly, J., Wulfeck, B., Dronkers, N., Opie, M., Fenson, J., Kriz, S., Jeffries, R., Miller, L., & Herbst, K. (2001). Differential effects of unilateral lesions on language production in children and adults. Brain and Language, 79, 223265.Google Scholar
Berl, M.M., Balsamo, L.M., Xu, B., Moore, E.N., Weinstein, S.L., Conry, J.A., Perl, P.L., Sachs, B.C., Grandin, C.B., Frattali, C., Ritter, F.J., Sato, S., Theodore, W.H., & Gaillard, W.D. (2005). Seizure focus affects regional language networks assessed by fMRI. Neurology, 65, 16041611.Google Scholar
Bhatnagar, S.C., Mandybur, G.T., Buckingham, H.W., & Andy, O.J. (2000). Language representation in the human brain: Evidence from cortical mapping. Brain and Language, 74, 238259.Google Scholar
Blank, S.C., Bird, H., Turkheimer, F., & Wise, R.J. (2003). Speech production after stroke: The role of the right pars opercularis. Annals of Neurology, 54, 310320.Google Scholar
Bogen, J.E. & Bogen, G.M. (1976). Wernicke's region—where is it? Annals of the New York Academy of Sciences, 280, 834843.Google Scholar
Brazdil, M., Zakopcan, J., Kuba, R., Fanfrdlova, Z., & Rektor, I. (2003). Atypical hemispheric language dominance in left temporal lobe epilepsy as a result of the reorganization of language functions. Epilepsy & Behavior, 4, 414419.Google Scholar
Broca, P. (1961). Remarques sur le sié de la faculté du langage articulé, suivies d'une observation d'aphémie (perte de la parole). Bulletin de la Société Anatomique, 6, 330357.Google Scholar
Brown, T.T., Lugar, H.M., Coalson, R.S., Miezin, F.M., Petersen, S.E., & Schlaggar, B.L. (2005). Developmental changes in human cerebral functional organization for word generation. Cerebral Cortex, 15, 275290.Google Scholar
Burgund, E.D., Kang, H.C., Kelly, J.E., Buckner, R.L., Snyder, A.Z., Petersen, S.E., & Schlaggar, B.L. (2002). The feasibility of a common stereotactic space for children and adults in fMRI studies of development. Neuroimage, 17, 184200.Google Scholar
Cao, Y., Vikingstad, E.M., George, K.P., Johnson, A.F., & Welch, K.M. (1999). Cortical language activation in stroke patients recovering from aphasia with functional MRI. Stroke, 30, 23312340.Google Scholar
Chitoku, S., Otsubo, H., Harada, Y., Jay, V., Rutka, J.T., Weiss, S.K., Abdoll, M., & Snead, O.C., III. (2001). Extraoperative cortical stimulation of motor function in children. Pediatric Neurology, 24, 344350.Google Scholar
Chitoku, S., Otsubo, H., Harada, Y., Jay, V., Rutka, J.T., Weiss, S.K., Elliott, I., Ochi, A., Masaomi, K., & Snead, O.C., III. (2003). Characteristics of prolonged afterdischarges in children with malformations of cortical development. Journal of Child Neurology, 18, 247253.Google Scholar
Devinsky, O., Perrine, K., Hirsch, J., McMullen, W., Pacia, S., & Doyle, W. (2000). Relation of cortical language distribution and cognitive function in surgical epilepsy patients. Epilepsia, 41, 400404.Google Scholar
DeVos, K.J., Wyllie, E., Geckler, C., Kotagal, P., & Comair, Y. (1995). Language dominance in patients with early childhood tumors near left hemisphere language areas. Neurology, 45, 349356.Google Scholar
Duchowny, M., Jayakar, P., Harvey, A.S., Resnick, T., Alvarez, L., Dean, P., & Levin, B. (1996). Language cortex representation: Effects of developmental versus acquired pathology. Annals of Neurology, 40, 3138.Google Scholar
Duncan, J.D., Moss, S.D., Bandy, D.J., Manwaring, K., Kaplan, A.M., Reiman, E.M., Chen, K., Lawson, M.A., & Wodrich, D.L. (1997). Use of positron emission tomography for presurgical localization of eloquent brain areas in children with seizures. Pediatric Neurosurgery, 26, 144156.Google Scholar
Fernandes, M.A. & Smith, M.L. (2000). Comparing the Fused Dichotic Words Test and the Intracarotid Amobarbital Procedure in children with epilepsy. Neuropsychologia, 38, 12161228.Google Scholar
Fernandez, B., Cardebat, D., Demonet, J.F., Joseph, P.A., Mazaux, J.M., Barat, M., & Allard, M. (2004). Functional MRI follow-up study of language processes in healthy subjects and during recovery in a case of aphasia. Stroke, 35, 21712176.Google Scholar
Friston, K.J., Ashburner, J., Poline, J.B., Frith, C.D., Heather, J.D., & Frackowiak, R.S.J. (1995). Spatial registration and normalization of images. Human Brain Mapping, 2, 165189.Google Scholar
Gaillard, W.D., Balsamo, L., Grandin, C.B., Braniecki, S.H., Papero, P.H., Weinstein, S., Conry, J., Pearl, P.L., Sachs, B., Sato, S., Jabbari, B., Vezina, L.G., Frattali, C., & Theodore, W.H. (2002). Language dominance in partial epilepsy patients identified with an fMRI reading task. Neurology, 59, 160161.Google Scholar
Helmstaedter, C., Kurthen, M., Linke, D.B., & Elger, C.E. (1997). Patterns of language dominance in focal left and right hemisphere epilepsies: Relation to MRI findings, EEG, sex, and age at onset of epilepsy. Brain and Cognition, 33, 135150.Google Scholar
Lesser, R.P., Luders, H., Klem, G., Dinner, D.S., Morris, H.H., & Hahn, J. (1984). Cortical afterdischarge and functional response thresholds: Results of extraoperative testing. Epilepsia, 25, 615621.Google Scholar
Liegeois, F., Connelly, A., Cross, J.H., Boyd, S.G., Gadian, D.G., Vargha-Khadem, F., & Baldeweg, T. (2004). Language reorganization in children with early-onset lesions of the left hemisphere: An fMRI study. Brain, 127(Pt 6), 12291236.Google Scholar
Minassian, B.A., Otsubo, H., Weiss, S., Elliott, I., Rutka, J.T., & Snead, O.C., III. (1999). Magnetoencephalographic localization in pediatric epilepsy surgery: Comparison with invasive intracranial electroencephalography. Annals of Neurology, 46, 627633.Google Scholar
Mohr, J.P., Pessin, M.S., Finkelstein, S., Funkenstein, H.H., Duncan, G.W., & Davis, K.R. (1978). Broca aphasia: Pathologic and clinical. Neurology, 28, 311324.Google Scholar
Muller, R.A., Rothermel, R.D., Behen, M.E., Muzik, O., Chakraborty, P.K., & Chugani, H.T. (1999). Language organization in patients with early and late left-hemisphere lesion: A PET study. Neuropsychologia, 37, 545557.Google Scholar
Muller, R.A., Rothermel, R.D., Behen, M.E., Muzik, O., Mangner, T.J., Chakraborty, P.K., & Chugani, H.T. (1998). Brain organization of language after early unilateral lesion: A PET study. Brain and Language, 62, 422451.Google Scholar
Ojemann, G.A. (1979). Individual variability in cortical localization of language. Journal of Neurosurgery, 50, 164169.Google Scholar
Ojemann, G.A. (1983). Brain organization for language from the perspective of electrical stimulation mapping. Behavioural Brain Research, 2, 189326.Google Scholar
Ojemann, S.G., Berger, M.S., Lettich, E., & Ojemann, G.A. (2003). Localization of language function in children: Results of electrical stimulation mapping. Journal of Neurosurgery, 98, 465470.Google Scholar
Ojemann, G., Ojemann, J., Lettich, E., & Berger, M. (1989). Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. Journal of Neurosurgery, 71, 316326.Google Scholar
Onal, C., Otsubo, H., Araki, T., Chitoku, S., Ochi, A., Weiss, S., Elliott, I., Snead, O.C., III, Rutka, J.T., & Logan, W. (2003). Complications of invasive subdural grid monitoring in children with epilepsy. Journal of Neurosurgery, 98, 10171026.Google Scholar
Pataraia, E., Simos, P.G., Castillo, E.M., Billingsley-Marshall, R.L., McGregor, A.L., Breier, J.I., Sarkari, S., & Papanicolaou, A.C. (2004). Reorganization of language-specific cortex in patients with lesions or mesial temporal epilepsy. Neurology, 63, 18251832.Google Scholar
Penfield, W. & Roberts, L. (1959). Speech and brain-mechanisms. Princeton, NJ: Princeton University Press.
Petrides, M. & Pandya, D.N. (Eds.). (1994). Comparative architectonic analysis of the human and the macaque frontal cortex. (Vol. 9). Amsterdam: Elsevier.
Poeppel, D. & Hickok, G. (2004). Towards a new functional anatomy of language. Cognition, 92, 112.Google Scholar
Quinones-Hinojosa, A., Ojemann, S.G., Sanai, N., Dillon, W.P., & Berger, M.S. (2003). Preoperative correlation of intraoperative cortical mapping with magnetic resonance imaging landmarks to predict localization of the Broca area. Journal of Neurosurgery, 99, 311318.Google Scholar
Rasmussen, T. & Milner, B. (1977). The role of early left-brain injury in determining lateralization of cerebral speech functions. Annals of the New York Academy of Sciences, 299, 355369.Google Scholar
Reilly, J.S., Bates, E.A., & Marchman, V.A. (1998). Narrative discourse in children with early focal brain injury. Brain and Language, 61, 335375.Google Scholar
Rorden, C. & Brett, M. (2000). Stereotaxic display of brain lesions. Behavioural Neurology, 12, 191200.Google Scholar
Rosen, H.J., Petersen, S.E., Linenweber, M.R., Snyder, A.Z., White, D.A., Chapman, L., Dromerick, A.W., Fiez, J.A., & Corbetta, M.D. (2000). Neural correlates of recovery from aphasia after damage to left inferior frontal cortex. Neurology, 55, 18831894.Google Scholar
Rutka, J.T., Otsubo, H., Kitano, S., Sakamoto, H., Shirasawa, A., Ochi, A., & Snead, O.C., III. (1999). Utility of digital camera-derived intraoperative images in the planning of epilepsy surgery for children. Neurosurgery, 45, 11861191.Google Scholar
Saltzman-Benaiah, J., Scott, K., & Smith, M.L. (2003). Factors associated with atypical speech representation in children with intractable epilepsy. Neuropsychologia, 41, 19671974.Google Scholar
Satz, P., Strauss, E., Wada, J., & Orsini, D.L. (1988). Some correlates of intra- and interhemispheric speech organization after left focal brain injury. Neuropsychologia, 26, 345350.Google Scholar
Schwartz, T.H., Devinsky, O., Doyle, W., & Perrine, K. (1998). Preoperative predictors of anterior temporal language areas. Journal of Neurosurgery, 89, 962970.Google Scholar
Smith, S.M. (2002). Fast robust automated brain extraction. Human Brain Mapping, 17(3), 143155.Google Scholar
Snead, O.C., III. (2001). Surgical treatment of medically refractory epilepsy in childhood. Brain & Development, 23, 199207.Google Scholar
Springer, J.A., Binder, J.R., Hammeke, T.A., Swanson, S.J., Frost, J.A., Bellgowan, P.S., Brewer, C.C., Perry, H.M., Morris, G.L., & Mueller, W.M. (1999). Language dominance in neurologically normal and epilepsy subjects: A functional MRI study. Brain, 122(Pt 11), 20332046.Google Scholar
Talairach, J. & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain. New York: Thieme.
Thiel, A., Herholz, K., Koyuncu, A., Ghaemi, M., Kracht, L.W., Habedank, B., & Heiss, W.D. (2001). Plasticity of language networks in patients with brain tumors: A positron emission tomography activation study. Annals of Neurology, 50, 620629.Google Scholar
Tomaiuolo, F., MacDonald, J.D., Caramanos, Z., Posner, G., Chiavaras, M., Evans, A.C., & Petrides, M. (1999). Morphology, morphometry and probability mapping of the pars opercularis of the inferior frontal gyrus: An in vivo MRI analysis. European Journal of Neuroscience, 11, 30333046.Google Scholar
Vargha-Khadem, F., O'Gorman, A.M., & Watters, G.V. (1985). Aphasia and handedness in relation to hemispheric side, age at injury and severity of cerebral lesion during childhood. Brain, 108(Pt 3), 677696.Google Scholar
Vingerhoets, G., Deblaere, K., Backes, W.H., Achten, E., Boon, P., Boon, P.J., Hofman, P., Vermeulen, J., Vonck, K., Wilmink, J., & Aldenkamp, A.P. (2004). Lessons for neuropsychology from function MRI in patients with epilepsy. Epilepsy & Behavior, 5, S81S89.Google Scholar
Weber, B., Wellmer, J., Reuber, M., Mormann, F., Weis, S., Urbach, H., Ruhlmann, J., Elger, C.E., & Fernandez, G. (2006). Left hippocampal pathology is associated with atypical language lateralization in patients with focal epilepsy. Brain, 129, 346351.Google Scholar
Wellmer, J., von Oertzen, J., Schaller, C., Urbach, H., Konig, R., Widman, G., Van Roost, D., & Elger, C.E. (2002). Digital photography and 3D MRI-based multimodal imaging for individualized planning of respective neocortical epilepsy surgery. Epilepsia, 43, 15431550.Google Scholar
Wernicke, C. (1874). Der aphasische Symptomencomplex. Breslaux, Germany: Max Cohn and Weigert.