Clinical functional MRI of the language domain in children with epilepsy
Corresponding Author
Marko Wilke
Department of Pediatric Neurology and Developmental Medicine, Children's Hospital, University of Tübingen, Germany
Experimental Pediatric Neuroimaging, Children's Hospital and Department of Neuroradiology, University of Tübingen, Germany
Department of Pediatric Neurology and Developmental Medicine, Children's Hospital, University of Tübingen, Hoppe-Seyler-Str. 1, 72076 Tübingen, GermanySearch for more papers by this authorTom Pieper
Neuropediatric Clinic and Clinic for Neurorehabilitation, Epilepsy Centre for Children and Adolescents, Behandlungszentrum Vogtareuth, Germany
Search for more papers by this authorKatja Lindner
Department of Pediatric Neurology and Developmental Medicine, Children's Hospital, University of Tübingen, Germany
Search for more papers by this authorThekla Dushe
Neuropediatric Clinic and Clinic for Neurorehabilitation, Epilepsy Centre for Children and Adolescents, Behandlungszentrum Vogtareuth, Germany
Search for more papers by this authorMartin Staudt
Department of Pediatric Neurology and Developmental Medicine, Children's Hospital, University of Tübingen, Germany
Neuropediatric Clinic and Clinic for Neurorehabilitation, Epilepsy Centre for Children and Adolescents, Behandlungszentrum Vogtareuth, Germany
Search for more papers by this authorWolfgang Grodd
Department of Neuroradiology, University of Tübingen, Germany
Search for more papers by this authorHans Holthausen
Neuropediatric Clinic and Clinic for Neurorehabilitation, Epilepsy Centre for Children and Adolescents, Behandlungszentrum Vogtareuth, Germany
Search for more papers by this authorIngeborg Krägeloh-Mann
Department of Pediatric Neurology and Developmental Medicine, Children's Hospital, University of Tübingen, Germany
Search for more papers by this authorCorresponding Author
Marko Wilke
Department of Pediatric Neurology and Developmental Medicine, Children's Hospital, University of Tübingen, Germany
Experimental Pediatric Neuroimaging, Children's Hospital and Department of Neuroradiology, University of Tübingen, Germany
Department of Pediatric Neurology and Developmental Medicine, Children's Hospital, University of Tübingen, Hoppe-Seyler-Str. 1, 72076 Tübingen, GermanySearch for more papers by this authorTom Pieper
Neuropediatric Clinic and Clinic for Neurorehabilitation, Epilepsy Centre for Children and Adolescents, Behandlungszentrum Vogtareuth, Germany
Search for more papers by this authorKatja Lindner
Department of Pediatric Neurology and Developmental Medicine, Children's Hospital, University of Tübingen, Germany
Search for more papers by this authorThekla Dushe
Neuropediatric Clinic and Clinic for Neurorehabilitation, Epilepsy Centre for Children and Adolescents, Behandlungszentrum Vogtareuth, Germany
Search for more papers by this authorMartin Staudt
Department of Pediatric Neurology and Developmental Medicine, Children's Hospital, University of Tübingen, Germany
Neuropediatric Clinic and Clinic for Neurorehabilitation, Epilepsy Centre for Children and Adolescents, Behandlungszentrum Vogtareuth, Germany
Search for more papers by this authorWolfgang Grodd
Department of Neuroradiology, University of Tübingen, Germany
Search for more papers by this authorHans Holthausen
Neuropediatric Clinic and Clinic for Neurorehabilitation, Epilepsy Centre for Children and Adolescents, Behandlungszentrum Vogtareuth, Germany
Search for more papers by this authorIngeborg Krägeloh-Mann
Department of Pediatric Neurology and Developmental Medicine, Children's Hospital, University of Tübingen, Germany
Search for more papers by this authorAbstract
Functional MRI (fMRI) for the assessment of language functions is increasingly used in the diagnostic workup of patients with epilepsy. Termed “clinical fMRI,” such an approach is also feasible in children who may display specific patterns of language reorganization. This study was aimed at assessing language reorganization in pediatric epilepsy patients, using fMRI. We studied 26 pediatric epilepsy patients (median age, 13.05 years; range, 5.6–18.7 years) and 23 healthy control children (median age, 9.37 years; range, 6.2–15.4 years), using two child-friendly fMRI tasks and adapted data-processing streams. Overall, 81 functional series could be analyzed. Reorganization seemed to occur primarily in homotopic regions in the contralateral hemisphere, but lateralization in the frontal as well as in the temporal lobes was significantly different between patients and controls. The likelihood to find atypical language organization was significantly higher in patients. Additionally, we found significantly stronger activation in the healthy controls in a primarily passive task, suggesting a systematic confounding influence of antiepileptic medication. The presence of a focal cortical dysplasia was significantly associated with atypical language lateralization. We conclude that important confounds need to be considered and that the pattern of language reorganization may be distinct from the patterns seen in later-onset epilepsy. Hum Brain Mapp, 2011. © 2010 Wiley-Liss, Inc.
REFERENCES
- Anderson DP, Harvey AS, Saling MM, Anderson V, Kean M, Abbott DF, Wellard RM, Jackson GD ( 2006): FMRI lateralization of expressive language in children with cerebral lesions. Epilepsia 47: 998–1008.
- Andersson JL, Hutton C, Ashburner J, Turner R, Friston K ( 2001): Modeling geometric deformations in EPI time series. Neuroimage 13: 903–919.
- Ashburner J, Friston KJ ( 2005): Unified segmentation. NeuroImage 26: 839–851.
- Barkovich AJ, Kuzniecky RI, Jackson GD, Guerrini R, Dobyns WB ( 2001): Classification system for malformations of cortical development: Update 2001. Neurology 57: 2168–2178.
- Bast T, Ramantani G, Seitz A, Rating D ( 2006): Focal cortical dysplasia: Prevalence, clinical presentation and epilepsy in children and adults. Acta Neurol Scand 113: 72–81.
- Bishop DV, Watt H, Papadatou-Pastou M ( 2009): An efficient and reliable method for measuring cerebral lateralization during speech with functional transcranial Doppler ultrasound. Neuropsychologia 47: 587–590.
- Briellmann RS, Labate A, Harvey AS, Saling MM, Sveller C, Lillywhite L, Abbott DF, Jackson GD ( 2006): Is language lateralization in temporal lobe epilepsy patients related to the nature of the epileptogenic lesion? Epilepsia 47: 916–920.
- Chugani HT, Shields WD, Shewmon DA, Olson DM, Phelps ME, Peacock WJ ( 2006): Infantile spasms. I. PET identifies focal cortical dysgenesis in cryptogenic cases for surgical treatment. Ann Neurol 27: 406–413.
- Everts R, Lidzba K, Wilke M, Kiefer C, Mordasini M, Schroth G, Perrig W, Steinlin M ( 2009): Strengthening of laterality of verbal and visuospatial functions during childhood and adolescence. Hum Brain Mapp 30: 473–483.
- Fauser S, Huppertz HJ, Bast T, Strobl K, Pantazis G, Altenmueller DM, Feil B, Rona S, Kurth C, Rating D, Korinthenberg R, Steinhoff BJ, Volk B, Schulze-Bonhage A ( 2006): Clinical characteristics in focal cortical dysplasia: A retrospective evaluation in a series of 120 patients. Brain 129: 1907–1916.
- Fernández G, Specht K, Weis S, Tendolkar I, Reuber M, Fell J, Klaver P, Ruhlmann J, Reul J, Elger CE ( 2003): Intrasubject reproducibility of presurgical language lateralization and mapping using fMRI. Neurology 60: 969–975.
- Friston KJ, Holmes AP, Worsley KJ, Poline JB, Frith C, Frackowiak RSJ ( 1995): Statistical parametric maps in functional imaging: A general linear approach. Hum Brain Mapp 2: 189–210.
- Gaillard WD, Balsamo L, Xu B, McKinney C, Papero PH, Weinstein S, Conry J, Pearl PL, Sachs B, Sato S, Vezina LG, Frattali C, Theodore WH ( 2004): fMRI language task panel improves determination of language dominance. Neurology 63: 1403–1408.
- Gallagher A, Bastien D, Pelletier I, Vannasing P, Legatt AD, Moshé SL, Jehle R, Carmant L, Lepore F, Béland R, Lassonde M ( 2008): A noninvasive, presurgical expressive and receptive language investigation in a 9-year-old epileptic boy using near-infrared spectroscopy. Epilepsy Behav 12: 340–346.
- Gizewski ER, de Greiff A, Maderwald S, Timmann D, Forsting M, Ladd ME ( 2007): fMRI at 7 T: Whole-brain coverage and signal advantages even infratentorially? NeuroImage 37: 761–768.
- Hayasaka S, Nichols TE ( 2004): Combining voxel intensity and cluster extent with permutation test framework. NeuroImage 23: 54–63.
- Heinke W, Fiebach CJ, Schwarzbauer C, Meyer M, Olthoff D, Alter K ( 2004): Sequential effects of propofol on functional brain activation induced by auditory language processing: An event-related functional magnetic resonance imaging study. Br J Anaesth 92: 641–650.
- Helmstaedter C, Fritz NE, González Pérez PA, Elger CE, Weber B ( 2006): Shift-back of right into left hemisphere language dominance after control of epileptic seizures: Evidence for epilepsy driven functional cerebral organization. Epilepsy Res 70: 257–262.
- Holland SK, Plante E, Weber Byars A, Strawsburg RH, Schmithorst VJ, Ball WS ( 2001): Normal fMRI brain activation patterns in children performing a verb generation task. NeuroImage 14: 837–843.
- Jayakar P, Bernal B, Santiago Medina L, Altman N ( 2002): False lateralization of language cortex on functional MRI after a cluster of focal seizures. Neurology 58: 490–492.
- Jonas R, Nguyen S, Hu B, Asarnow RF, LoPresti C, Curtiss S, de Bode S, Yudovin S, Shields WD, Vinters HV, Mathern GW ( 2004): Cerebral hemispherectomy: Hospital course, seizure, developmental, language, and motor outcomes. Neurology 62: 1712–1721.
- Kida I, Smith AJ, Blumenfeld H, Behar KL, Hyder F ( 2006): Lamotrigine suppresses neurophysiological responses to somatosensory stimulation in the rodent. NeuroImage 29: 216–224.
- Krsek P, Maton B, Korman B, Pacheco-Jacome E, Jayakar P, Dunoyer C, Rey G, Morrison G, Ragheb J, Vinters HV, Resnick T, Duchowny M ( 2008): Different features of histopathological subtypes of pediatric focal cortical dysplasia. Ann Neurol 63: 758–769.
- Lidzba K, Staudt M, Wilke M, Krägeloh-Mann I ( 2006): Visuospatial deficits in patients with early left-hemispheric lesions and functional reorganization of language: Consequence of lesion or reorganization? Neuropsychologia 44: 1088–1094.
- Liégeois F, Connelly A, Cross JH, Boyd SG, Gadian DG, Vargha-Khadem F, Baldeweg T ( 2004): Language reorganization in children with early-onset lesions of the left hemisphere: An fMRI study. Brain 127: 1229–1236.
- Logothetis NK, Pfeuffer J ( 2004): On the nature of the BOLD fMRI contrast mechanism. Magn Reson Imaging 22: 1517–1531.
- Lowen SB, Nickerson LD, Levin JM ( 2009): Differential effects of acute cocaine and placebo administration on visual cortical activation in healthy subjects measured using BOLD fMRI. Pharmacol Biochem Behav 92: 277–282.
- Macey PM, Macey KE, Kumar R, Harper RM ( 2004): A method for removal of global effects from fMRI time series. NeuroImage 22: 360–366.
- Maquet P, Hirsch E, Metz-Lutz MN, Motte J, Dive D, Marescaux C, Franck G ( 1995): Regional cerebral glucose metabolism in children with deterioration of one or more cognitive functions and continuous spike-and-wave discharges during sleep. Brain 118: 1497–1520.
- Mbwana J, Berl MM, Ritzl EK, Rosenberger L, Mayo J, Weinstein S, Conry JA, Pearl PL, Shamim S, Moore EN, Sato S, Vezina LG, Theodore WH, Gaillard WD ( 2009): Limitations to plasticity of language network reorganization in localization related epilepsy. Brain 132: 347–356.
- Möddel G, Lineweaver T, Schuele SU, Reinholz J, Loddenkemper T ( 2009): Atypical language lateralization in epilepsy patients. Epilepsia 50: 1505–1516.
- Moeller F, Siebner HR, Ahlgrimm N, Wolff S, Muhle H, Granert O, Boor R, Jansen O, Gotman J, Stephani U, Siniatchkin M ( 2009): fMRI activation during spike and wave discharges evoked by photic stimulation. NeuroImage 48: 682–695.
- Mühlau M, Wohlschläger AM, Gaser C, Valet M, Weindl A, Nunnemann S, Peinemann A, Etgen T, Ilg R ( 2009): Voxel-based morphometry in individual patients: A pilot study in early Huntington disease. AJNR Am J Neuroradiol 30: 539–543.
- Nakao Y, Itoh Y, Kuang TY, Cook M, Jehle J, Sokoloff L ( 2001): Effects of anesthesia on functional activation of cerebral blood flow and metabolism. Proc Natl Acad Sci USA 98: 7593–7598.
- Ogawa S, Lee TM ( 1990): Magnetic resonance imaging of blood vessels at high fields: In vivo and in vitro measurements and image simulation. Magn Reson Med 16: 9–18.
- Oldfield RC ( 1971): The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia 9: 97–113.
- O'Shaughnessy ES, Berl MM, Moore EN, Gaillard WD ( 2008): Pediatric functional magnetic resonance imaging (fMRI): Issues and applications. J Child Neurol 23: 791–801.
- Papanicolaou AC, Simos PG, Castillo EM, Breier JI, Sarkari S, Pataraia E, Billingsley RL, Buchanan S, Wheless J, Maggio V, Maggio WW ( 2004): Magnetoencephalography: A noninvasive alternative to the Wada procedure. J Neurosurg 100: 867–876.
- Rasmussen T, Milner B ( 1977): The role of early left-brain injury in determining lateralization of cerebral speech functions. Ann NY Acad Sci 299: 355–369.
- Ricci GB, De Carli D, Colonnese C, Di Gennaro G, Quarato PP, Cantore G, Esposito V, Garreffa G, Maraviglia B ( 2004): Hemodynamic response (BOLD/fMRI) in focal epilepsy with reference to benzodiazepine effect. Magn Reson Imaging 22: 1487–1492.
- Rosenberger LR, Zeck J, Berl MM, Moore EN, Ritzl EK, Shamim S, Weinstein SL, Conry JA, Pearl PL, Sato S, Vezina LG, Theodore WH, Gaillard WD ( 2009): Interhemispheric and intrahemispheric language reorganization in complex partial epilepsy. Neurology 72: 1830–1836.
- Ruff IM, Petrovich Brennan NM, Peck KK, Hou BL, Tabar V, Brennan CW, Holodny AI ( 2008): Assessment of the language laterality index in patients with brain tumor using functional MR imaging: Effects of thresholding, task selection, and prior surgery. AJNR Am J Neuroradiol 29: 528–535.
- Schapiro MB, Schmithorst VJ, Wilke M, Byars AW, Strawsburg RH, Holland SK ( 2004): BOLD fMRI signal increases with age in selected brain regions in children. Neuroreport 15: 2575–2578.
- Staudt M, Grodd W, Niemann G, Wildgruber D, Erb M, Krägeloh-Mann I ( 2001): Early left periventricular brain lesions induce right hemispheric organization of speech. Neurology 57: 122–125.
- Stippich C, Rapps N, Dreyhaupt J, Durst A, Kress B, Nennig E, Tronnier VM, Sartor K ( 2007): Localizing and lateralizing language in patients with brain tumors: Feasibility of routine preoperative functional MR imaging in 81 consecutive patients. Radiology 243: 828–836.
- Szaflarski JP, Binder JR, Possing ET, McKiernan KA, Ward BD, Hammeke TA ( 2002): Language lateralization in left-handed and ambidextrous people: fMRI data. Neurology 59: 238–244.
- Thulborn KR, Davis D, Erb P, Strojwas M, Sweeney JA ( 1996): Clinical fMRI: Implementation and experience. NeuroImage 4: S101–S107.
- Van Halen L ( 2001): The Statistics of Variation. In: BK Hall, editor. Variation. Amsterdam: Elsevier. pp 29–49.
- Voets NL, Adcock JE, Flitney DE, Behrens TE, Hart Y, Stacey R, Carpenter K, Matthews PM ( 2006): Distinct right frontal lobe activation in language processing following left hemisphere injury. Brain 129: 754–766.
- Widdess-Walsh P, Diehl B, Najm I ( 2006): Neuroimaging of focal cortical dysplasia. J Neuroimag 16: 185–196.
- Wilke M, Schmithorst VJ ( 2006): A combined bootstrap/histogram analysis approach for computing a lateralization index from neuroimaging data. NeuroImage 33: 522–530.
- Wilke M, Lidzba K ( 2007): LI-tool: A new toolbox to assess lateralization in functional MR-data. J Neurosci Methods 163: 128–136.
- Wilke M, Schmithorst VJ, Holland SK ( 2002): Assessment of spatial normalization of whole-brain magnetic resonance images in children. Hum Brain Mapp 17: 48–60.
- Wilke M, Lidzba K, Staudt M, Buchenau K, Grodd W, Krägeloh-Mann I ( 2005): Comprehensive language mapping in children, using fMRI: What's missing, counts. NeuroReport 16: 915–919.
- Wilke M, Lidzba K, Staudt M, Buchenau K, Grodd W, Krägeloh-Mann I ( 2006): An fMRI task battery for assessing hemispheric language dominance in children. NeuroImage 32: 400–410.
- Wilke M, Holland SK, Altaye M, Gaser C ( 2008): Template-O-Matic: A toolbox for creating customized pediatric templates. NeuroImage 41: 903–913.
- Wilke M, Staudt M, Juenger H, Grodd W, Braun C, Krägeloh-Mann I ( 2009): Somatosensory system in two types of motor reorganization in congenital hemiparesis: Topography and function. Hum Brain Mapp 30: 776–788.
- Wink AM, Roerdink JB ( 2004): Denoising functional MR images: A comparison of wavelet denoising and Gaussian smoothing. IEEE Trans Med Imaging 23: 374–387.
- Yerys BE, Jankowski KF, Shook D, Rosenberger LR, Barnes KA, Berl MM, Ritzl EK, Vanmeter J, Vaidya CJ, Gaillard WD ( 2009): The fMRI success rate of children and adolescents: Typical development, epilepsy, attention deficit/hyperactivity disorder, and autism spectrum disorders. Hum Brain Mapp 30: 3426–3435.
