Asymmetry of planum temporale constrains interhemispheric language plasticity in children with focal epilepsy

Brain

Volumn 136, Issue 10, 2013, Pages 3163-3175

  Pahs, Gerald ^a,b,c   Rankin, Peter ^a,b   Helen Cross, J ^a,b   Croft, Louise ^a,b   Northam, Gemma B ^a,b   Liegeois, Frederique ^a,b   Greenway, Sarah ^a   Harrison, Sue ^a,b   Vargha Khadem, Faraneh ^a,b   Baldeweg, Torsten ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^c UNIV KLIN KINDER JUGENDHEILKUNDE   (Austria)

Author keywords

children; epilepsy; language lateralization; planum temporale

Indexed keywords

ARTICLE; BRAIN ASYMMETRY; BRAIN CORTEX; BRAIN SIZE; CHILD; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; ELECTROENCEPHALOGRAPHY; FEMALE; FOCAL EPILEPSY; FRONTAL LOBE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAY MATTER; HEMISPHERIC DOMINANCE; HUMAN; INFERIOR FRONTAL GYRUS; LANGUAGE; LEFT HEMISPHERE; MAJOR CLINICAL STUDY; MALE; NUCLEAR MAGNETIC RESONANCE SCANNER; PLANUM TEMPORALE; PRIORITY JOURNAL; RIGHT HEMISPHERE; SUPERIOR TEMPORAL GYRUS; SUPRASYLVIAN GYRUS; VOXEL BASED MORPHOMETRY;

EID: 84884877193     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awt225     Document Type: Article

References (99)

1. Adcock JE, Wise RG, Oxbury JM, Oxbury SM, Matthews PM. Quantitative fMRI assessment of the differences in lateralization of language-related brain activation in patients with temporal lobe epilepsy. Neuroimage 2003; 18: 423-38.
2. Anneken K, Konrad C, Drager B, Breitenstein C, Kennerknecht I, Ringelstein EB, et al. Familial aggregation of strong hemispheric language lateralization. Neurology 2004; 63: 2433-5.
3. Bates E, Wilson SM, Saygin AP, Dick F, Sereno MI, Knight RT, et al. Voxel-based lesion-symptom mapping. Nat Neurosci 2003; 6: 448-50.
4. Bernal B, Altman NR. Speech delay in children: a functional MR imaging study. Radiology 2003; 229: 651-8.
5. Bianco IH, Carl M, Russell C, Clarke JD, Wilson SW. Brain asymmetry is encoded at the level of axon terminal morphology. Neural Dev 2008; 3: 9.
6. Binder JR, Swanson SJ, Hammeke TA, Morris GL, Mueller WM, Fischer M, et al. Determination of language dominance using functional MRI: a comparison with the Wada test. Neurology 1996; 46: 978-84.
7. Brauer J, Anwander A, Perani D, Friederici AD. Dorsal and ventral pathways inlanguage development. Brain Lang 2013. pii: S0093- 934X(13)00070-9. Advance Access published on May 1, 2013, doi:10.1016/j.bandl.2013.03.001.
8. Briellmann RS, Labate A, Harvey AS, Harvey AS, Saling MM, Sveller C, et al. Is language lateralization in temporal lobe epilepsy patients related to the nature of the epileptogenic lesion? Epilepsia 2006; 47: 916-20.
9. Buchsbaum BR, Baldo J, Okada K, Berman KF, Dronkers N, D'Esposito M, et al. Conduction aphasia, sensory-motor integration, and phonological short-term memory-an aggregate analysis of lesion and fMRI data. Brain Lang 2011; 119: 119-28.
10. Chi JG, Dooling EC, Gilles FH. Left-right asymmetries of the temporal speech areas of the human fetus. Arch Neurol 1977; 34: 346-8.
11. Corballis MC. The evolution and genetics of cerebral asymmetry. Philos Trans R Soc Lond B Biol Sci 2009; 364: 867-79.
12. Dick AS, Raja Beharelle A, Solodkin A, Small SL. Interhemispheric functional connectivity following prenatal or perinatal brain injury predicts receptive language outcome. J Neurosci 2013; 33: 5612-25.
13. Dorsaint-Pierre R, Penhune VB, Watkins KE, Neelin P, Lerch JP, Bouffard M, et al. Asymmetries of the planum temporale and Heschl's gyrus: relationship to language lateralization. Brain 2006; 129: 1164-76.
14. Dos Santos SS, Woerner W, Walter C, Kreuder F, Lueken U, Westerhausen R, et al. Handedness, dichotic-listening ear advantage, and gender effects on planum temporale asymmetry-a volumetric investigation using structural magnetic resonance imaging. Neuropsychologia 2006; 44: 622-36.
15. Draganski B, May A. Training-induced structural changes in the adult human brain. Behav Brain Res 2008; 192: 137-42.
16. Duke ES, Tesfaye M, Berl MM, Walker JE, Ritzl EK, Fasano RE, et al. The effect of seizure focus on regional language processing areas. Epilepsia 2012; 53: 1044-50.
17. Eberstaller O. Zur Oberflächen-Anatomie der Grosshirn- Hemisphären. Wien. Med. Blätter, 1884; 7: 644-6.
18. Eckert MA, Leonard CM, Possing ET, Binder JR. Uncoupled leftward asymmetries for planum morphology and functional language processing. Brain Lang 2006; 98: 102-111.
19. Eckert MA, Lombardino LJ, Walczak AR, Bonihla L, Leonard CM, Binder JR. Manual and automated measures of superior temporal gyrus asymmetry: concordant structural predictors of verbal ability in children. Neuroimage 2008; 41: 813-22.
20. Economo C, Horn L. Ueber Windungsrelief, Maße und Rindenarchitektonik der Supratemporalfläche, ihre individuellen und ihre Seitenunterschiede. Zeitschr Neurol Psychiatr 1930; 130: 678-757.
21. Field A. Discovering statistics using SPSS. London: Sage Publications Limited; 2009.
22. Flechsig P. Bemerkungen über die Hörsphäre des menschlichen Gehirns. Neurologisches Zentralblatt 1908; 27: 2-7.
23. Foundas AL, Leonard CM, Gilmore R, Fennell E, Heilman KM. Planum temporale asymmetry and language dominance. Neuropsychologia 1994; 32: 1225-31.
24. Gaillard WD, Balsamo L, Xu B, Grandin CB, Braniecki SH, Papero PH, et al. Language dominance in partial epilepsy patients identified with an fMRI reading task. Neurology 2002; 59: 256-65.
25. Gaillard WD, Balsamo L, Xu B, McKinney C, Papero PH, Weinstein S, et al. fMRI language task panel improves determination of language dominance. Neurology 2004; 63: 1403-8.
26. Gaillard WD, Berl MM, Moore EN, Ritzl EK, Rosenberger LR, Weinstein SL, et al. Atypical language in lesional and nonlesional complex partial epilepsy. Neurology 2007; 69: 1761-71.
27. Gaillard WD, Berl MM, Duke ES, Ritzl E, Miranda S, Liew C, et al. fMRI language dominance and FDG-PET hypometabolism. Neurology 2011; 76: 1322-9.
28. Galaburda AM, LeMay M, Kemper TL, Geschwind N. Right-left asymmetrics in the brain. Science 1978; 199: 852-6.
29. Galuske RA, Schlote W, Bratzke H, Singer W. Interhemispheric asymmetries of the modular structure in human temporal cortex. Science 2000; 289: 1946-9.
30. Geschwind N. The organization of language and the brain. Science 1970; 170: 940-4.
31. Geschwind N, Levitsky W. Human brain: left-right asymmetries in temporal speech region. Science 1968; 161: 186-7.
32. Griffiths TD, Warren JD. The planum temporale as a computational hub. Trends Neurosci 2002; 25: 348-53.
33. Habas PA, Scott JA, Roosta A, Rajagopalan V, Kim K, Rousseau F, et al. Early folding patterns and asymmetries of the normal human brain detected from in utero MRI. Cereb Cortex 2012; 22: 13-25.
34. Harvey AS, Cross JH, Shinnar S, Mathern BW. Defining the spectrum of international practice in pediatric epilepsy surgery patients. Epilepsia 2008; 49: 146-55.
35. Hickok G, Okada K, Serences JT. Area Spt in the human planum temporale supports sensory-motor integration for speech processing. J Neurophysiol 2009; 101: 2725-32.
36. Hickok G, Poeppel D. The cortical organization of speech processing. Nat Rev Neurosci 2007; 8: 393-402.
37. Hill J, Dierker D, Neil J, Inder T, Knutsen A, Harwell J, et al. A surface-based analysis of hemispheric asymmetries and folding of cerebral cortex in term-born human infants. J Neurosci 2010; 30: 2268-76.
38. Isaacs E, Christie D, Vargha-Khadem F, Mishkin M. Effects of hemispheric side of injury, age at injury, and presence of seizure disorder on functional ear and hand asymmetries in hemiplegic children. Neuropsychologia 1996; 34: 127-37.
39. Janszky J, Jokeit H, Heinemann D, Schulz R, Woermann FG, Ebner A. Epileptic activity influences the speech organization in medial temporal lobe epilepsy. Brain 2003; 126: 2043-51.
40. Janszky J, Mertens M, Janszky I, Ebner A, Woermann FG. Leftsided interictal epileptic activity induces shift of language lateralization in temporal lobe epilepsy: an fMRI study. Epilepsia 2006; 47: 921-7.
41. Jayakar P, Bernal B, Santiago Medina L, Altman N. False lateralization of language cortex on functional MRI after a cluster of focal seizures. Neurology 2002; 58: 490-2.
42. Josse G, Kherif F, Flandin G, Seghier ML, Price CJ. Predicting language lateralization from gray matter. J Neurosci 2009; 29: 13516-23.
43. Keller SS, Roberts N, Garcia-Finana M, Mohammadi S, Ringelstein EB, Knecht S, et al. Can the language-dominant hemisphere be predicted by brain anatomy? J Cogn Neurosci 2011; 23: 2013-29.
44. Knecht S. Does language lateralization depend on the hippocampus? Brain 2004; 127: 1217-8.
45. Korman B, Bernal B, Duchowny M, Jayakar P, Altman N, Garaycoa G, et al. Atypical propositional language organization in prenatal and early-acquired temporal lobe lesions. J Child Neurol 2010; 25: 985-93.
46. Labudda K, Mertens M, Janszky J, Bien CG, Woermann FG. Atypical language lateralisation associated with right fronto-temporal grey matter increases-a combined fMRI and VBM study in left-sided mesial temporal lobe epilepsy patients. Neuroimage 2012; 59: 728-37.
47. Lehericy S, Cohen L, Bazin B, Samson S, Giacomini E, Rougetet R, et al. Functional MR evaluation of temporal and frontal language dominance compared with the Wada test. Neurology 2000; 54: 1625-33.
48. Liegeois F, Connelly A, Baldeweg T, Vargha-Khadem F. Speaking with a single cerebral hemisphere: fMRI language organization after hemispherectomy in childhood. Brain Lang 2008; 106: 195-203.
49. Liegeois F, Connelly A, Cross JH, Boyd SG, Gadian DG, Vargha- Khadem F, et al. Language reorganization in children with earlyonset lesions of the left hemisphere: an fMRI study. Brain 2004; 127: 1229-36.
50. Liegeois F, Connelly A, Salmond CH, Gadian DG, Vargha-Khadem F, Baldeweg T. A direct test for lateralization of language activation using fMRI: comparison with invasive assessments in children with epilepsy. Neuroimage 2002; 17: 1861-7.
51. Liegeois F, Cross JH, Gadian DG, Connelly A. Role of fMRI in the decision- making process: epilepsy surgery for children. J Magn Reson Imaging 2006; 23: 933-40.
52. Lillywhite LM, Saling MM, Harvey AS, Abbott DF, Archer JS, Vears DF, et al. Neuropsychological and functional MRI studies provide converging evidence of anterior language dysfunction in BECTS. Epilepsia 2009; 50: 2276-84.
53. Lüders H, Acharya J, Baumgartner C, Benbadis S, Bleasel A, Burgess R, et al. Semiological seizure classification. Epilepsia 1998; 39: 1006-13.
54. Mbwana J, Berl MM, Ritzl EK, Rosenberger L, Mayo J, Weinstein S, et al. Limitations to plasticity of language network reorganization in localization related epilepsy. Brain 2009; 132 (Pt 2): 7-56.
55. Meyer A. The frontal lobe syndrome, the aphasias and related conditions. A contribution to the history of cortical localization. Brain 1974; 97: 565-600.
56. Molko N, Cachia A, Riviere D, Mangin JF, Bruandet M, Le Bihan D, et al. Functional and structural alterations of the intraparietal sulcus in a developmental dyscalculia of genetic origin. Neuron 2003; 40: 847-58.
57. Monjauze C, Broadbent H, Boyd SG, Neville BG, Baldeweg T. Language deficits and altered hemispheric lateralization in young people in remission from BECTS. Epilepsia 2011; 52: e79-83.
58. Myers EH, Hampson M, Vohr B, Lacadie C, Frost SJ, Pugh KR, et al. Functional connectivity to a right hemisphere language center in prematurely born adolescents. Neuroimage 2010; 51: 1445-52.
59. Northam GB, Liegeois F, Chong WK, Wyatt JS, Baldeweg T. Total brain white matter is a major determinant of IQ in adolescents born preterm. Ann Neurol 2011; 69: 702-11.
60. Northam GB, Liegeois F, Tournier JD, Croft LJ, Johns PN, Chong WK, et al. Interhemispheric temporal lobe connectivity predicts language impairment in adolescents born preterm. Brain 2012; 135: 3781-98.
61. Oh YM, Koh EJ. Language lateralization in patients with temporal lobe epilepsy: a comparison between volumetric analysis and the Wada test. J Korean Neurosurg Soc 2009; 45: 329-35.
62. Petrides M, Pandya DN. Association fiber pathways to the frontal cortex from the superior temporal region in the rhesus monkey. J Comp Neurol 1988; 273: 52-66.
63. Powell HW, Parker GJ, Alexander DC, Symms MR, Boulby PA, Wheeler- Kingshott CA, et al. Hemispheric asymmetries in language-related pathways: a combined functional MRI and tractography study. Neuroimage 2006; 32: 388-99.
64. Preis S, Jancke L, Schmitz-Hillebrecht J, Steinmetz H. Child age and planum temporale asymmetry. Brain Cogn 1999; 40: 441-52.
65. Price CJ. The anatomy of language: a review of 100 fMRI studies published in 2009. Ann N Y Acad Sci 2010; 1191: 62-88.
66. Price CJ. A review and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading. Neuroimage 2012; 62: 816-47.
67. Pujol J, Deus J, Losilla JM, Capdevila A. Cerebral lateralization of language in normal left-handed people studied by functional MRI. Neurology 1999; 52: 1038-43.
68. Rasmussen T, Milner B. The role of early left-brain injury in determining lateralization of cerebral speech functions. Ann N Y Acad Sci 1977; 299: 355-69.
69. Ratcliff G, Dila C, Taylor L, Milner B. The morphological asymmetry of the hemispheres and cerebral dominance for speech: a possible relationship. Brain Lang 1980; 11: 87-98.
70. Rorden C, Karnath HO, Bonilha L. Improving lesion-symptom mapping. J Cogn Neurosci 2007; 19: 1081-8.
71. Rosenberger LR, Zeck J, Berl MM, Moore EN, Ritzl EK, Shamim S, et al. Interhemispheric and intrahemispheric language reorganization in complex partial epilepsy. Neurology 2009; 72: 1830-6.
72. Rubens AB, Mahowald MW, Hutton JT. Asymmetry of the lateral (sylvian) fissures in man. Neurology 1976; 26: 620-4.
73. Schmahmann JD, Pandya DN, Wang R, Dai G, D'Arceuil HE, de Crespigny AJ, et al. Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. Brain 2007; 130: 630-53.
74. Satz P, Orsini DL, Saslow E, Henry R. The pathological left-handedness syndrome. Brain Cogn 1985; 4: 27-46.
75. Saur D, Kreher BW, Schnell S, Kummerer D, Kellmeyer P, Vry MS, et al. Ventral and dorsal pathways for language. Proc Natl Acad Sci USA 2008; 105: 18035-40.
76. Scott SK, Blank CC, Rosen S, Wise RJ. Identification of a pathway for intelligible speech in the left temporal lobe. Brain 2000; 123 (Pt 12): 2400-6.
77. Seghier ML. Laterality index in functional MRI: methodological issues. Magn Reson Imaging 2008; 26: 594-601.
78. Shapleske J, Rossell SL, Woodruff PW, David AS. The planum temporale: a systematic, quantitative review of its structural, functional and clinical significance. Brain Res Brain Res Rev 1999; 29: 26-49.
79. Steinmetz H, Rademacher J, Jaencke L, Huang Y, Thron A, Zilles K. Total surface of temporoparietal intrasylvian cortex: diverging left-right asymmetries. Brain Lang 1990; 39: 357-72.
80. Steinmetz H. Structure, functional and cerebral asymmetry: in vivo morphometry of the planum temporale. Neurosci Biobehav Rev 1996; 20: 587-591.
81. Sun T, Walsh CA. Molecular approaches to brain asymmetry and handedness. Nat Rev Neurosci 2006; 7: 655-62.
82. Sveller C, Briellmann RS, Saling MM, Lillywhite L, Abbott DF, Masterton RA, et al. Relationship between language lateralization and handedness in left-hemispheric partial epilepsy. Neurology 2006; 67: 1813-7.
83. Teki S, Barnes GR, Penny WD, Iverson P, Woodhead ZVJ, Griffiths TD, et al. The right hemisphere supports but does not replace left hemisphere auditory function in patients with persisting aphasia. Brain 2013; 136 (Pt 6): 1901-12. doi:10.1093/brain/awt087.
84. Thivard L, Hombrouck J, du Montcel ST, Delmaire C, Cohen L, Samson S, et al. Productive and perceptive language reorganization in temporal lobe epilepsy. Neuroimage 2005; 24: 841-51.
85. Toga AW, Thompson PM. Mapping brain asymmetry. Nat Rev Neurosci 2003; 4: 37-48.
86. Tzourio N, Nkanga-Ngila B, Mazoyer B. Left planum temporale surface correlates with functional dominance during story listening. Neuroreport 1998; 9: 829-33.
87. Van Essen DC. A population-average, landmark- and surface-based (PALS) atlas of human cerebral cortex. Neuroimage 2005; 28: 635-62.
88. Vargha-Khadem F, Isaacs E, Watkins K, Mishkin M. Ontogenetic specialisation of hemispheric function. In: Oxbury JM, Polkey CE, Duchowny MS, editors. Intactable focal epilepsy. London: W.B Suanders; 2000.
89. Vlooswijk MC, Jansen JF, de Krom MC, Majoie HM, Hofman PA, Backes WH, et al. Functional MRI in chronic epilepsy: associations with cognitive impairment. Lancet Neurol 2010; 9: 1018-27.
90. Weber B, Wellmer J, Reuber M, Mormann F, Weis S, Urbach H, et al. Left hippocampal pathology is associated with atypical language lateralization in patients with focal epilepsy. Brain 2006; 129: 346-51.
91. Whitehouse AJ, Bishop DV. Cerebral dominance for language function in adults with specific language impairment or autism. Brain 2008; 131: 3193-200.
92. Wilke M, Holland SK, Altaye M, Gaser C. Template-O-Matic: a toolbox for creating customized pediatric templates. Neuroimage 2008; 41: 903-13.
93. Wilke M, Lidzba K. LI-tool: a new toolbox to assess lateralization in functional MR-data. J Neurosci Methods 2007; 163: 128-36.
94. Wilke M, Schmithorst VJ. A combined bootstrap/histogram analysis approach for computing a lateralization index from neuroimaging data. Neuroimage 2006; 33: 522-30.
95. Wise RJ, Scott SK, Blank SC, Mummery CJ, Murphy K, Warburton EA. Separate neural subsystems within 'Wernicke's area'. Brain 2001; 124: 83-95.
96. Witelson SF, Pallie W. Left hemisphere specialization for language in the newborn. Neuroanatomical evidence of asymmetry. Brain 1973; 96: 641-6.
97. Woermann FG, Jokeit H, Luerding R, Freitag H, Schulz R, Guertler S, et al. Language lateralization by Wada test and fMRI in 100 patients with epilepsy. Neurology 2003; 61: 699-701.
98. Yetkin FZ, Swanson S, Fischer M, Akansel G, Morris G, Mueller W, et al. Functional MR of frontal lobe activation: comparison with Wada language results. AJNR Am J Neuroradiol 1998; 19: 1095-8.
99. Zheng ZZ. The functional specialization of the planum temporale. J Neurophysiol 2009; 102: 3079-81.