Abnormal functional lateralization and activity of language brain areas in typical specific language impairment (developmental dysphasia)

Brain

Volumn 134, Issue 10, 2011, Pages 3044-3058

  De Guibert, Clément ^a,b,c,d   Maumet, Camille ^a,b   Jannin, Pierre ^a,b   Ferré, Jean Christophe ^a,b,d   Tréguier, Catherine ^d   Barillot, Christian ^a,b   Le Rumeur, Elisabeth ^d   Allaire, Catherine ^d   Biraben, Arnaud ^d  

^a INRIA   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

^c Language Sciences   (France)

^d RENNES UNIVERSITY HOSPITAL   (France)

Author keywords

cerebral function; cerebral lateralization; functional MRI; language development; specific language impairment

Indexed keywords

ADOLESCENT; ADULT; ARTICLE; CAUDATE NUCLEUS; CHILD; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; DYSPHASIA; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GUSTATORY CORTEX; HEMISPHERIC DOMINANCE; HUMAN; INFERIOR FRONTAL GYRUS; LEFT HEMISPHERE; MALE; PARS OPERCULARIS; PARS TRIANGULARIS; PHONETICS; PRIORITY JOURNAL; SCHOOL CHILD; SUPERIOR TEMPORAL GYRUS; SUPRAMARGINAL GYRUS; WERNICKE AREA;

EID: 80054063586     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awr141     Document Type: Article

References (114)

1. Ackermann H, Riecker A. The contribution(s) of the insula to speech production: a review of the clinical and functional imaging literature. Brain Struct Funct 2010; 214: 419-33.
2. Alm PA. Stuttering and the basal ganglia circuits: a critical review of possible relations. J Commun Disord 2004; 37: 325-69. (Pubitemid 38680901)
3. Annett M. Left, right, hand and brain: the Right Shift Theory. Hillsdale, NJ: Erlbaum; 1985.
4. Ashburner J, Friston KJ. Unified segmentation. Neuroimage 2005; 26: 839-51. (Pubitemid 40825026)
5. Balsamo LM, Xu B, Grandin CB, Petrella JR, Braniecki SH, Elliott TK, et al. A functional magnetic resonance imaging study of left hemisphere language dominance in children. Arch Neurol 2002; 59: 1168-74. (Pubitemid 34755831)
6. Bates E. Origins of language disorders: a comparative approach. Dev Neuropsychol 1997; 13: 447-76. (Pubitemid 127509813)
7. Belton E, Salmon CH, Watkins KE, Vargha-Khadem F, Gadian DG. Bilateral brain abnormalities associated with dominantly inherited verbal and orofacial dyspraxia. Hum Brain Mapp 2003; 18: 194-200. (Pubitemid 36331575)
8. Bernal B, Altman NR. Speech delay in children: a functional MR imaging study. Radiology 2003; 229: 651-8. (Pubitemid 37467565)
9. Bishop DV. Uncommon understanding: development and disorders of comprehension in children. East Sussex, UK: Hove; 1997.
10. Bishop DV. How does the brain learn language. Insights from the study of children with and without language Impairment. Dev Med Child Neurol 2000; 42: 133-42. (Pubitemid 30083907)
11. Bishop DV. Diagnostic dilemmas in specific language impairment. In: Verhoeven L, Van Balkom J, editors. Classification of developmental language disorders. Mahwah, NJ: Erlbaum; 2004. p. 309-26.
12. Bishop DV. What causes specific language impairment in children? Curr Dir Psychol Sci 2006; 15: 217-21. (Pubitemid 44800063)
13. Bishop DV, Hayiou-Thomas ME. Heritability of specific language impairment depends on diagnostic criteria. Genes Brain Behav 2008; 7: 365-72. (Pubitemid 351490241)
14. Bishop DV, Snowling MJ. Developmental dyslexia and specific language impairment: same or different? Psychol Bull 2004; 130: 858-86. (Pubitemid 39508392)
15. Blank SC, Scott SK, Murphy K, Warburton E, Wise RJ. Speech production: Wernicke, Broca and beyond. Brain 2002; 125: 1829-38.
16. Bohland JW, Guenther FH. An fMRI investigation of syllable sequence production. Neuroimage 2006; 32: 821-41. (Pubitemid 44149157)
17. Booth JR, Wood L, Lu D, Houk JC, Bitan T. The role of the basal ganglia and cerebellum in language processing. Brain Res 2007; 1133: 136-44. (Pubitemid 46123259)
18. Brown S, Ingham RJ, Ingham JC, Laird AR, Fox PT. Stuttered and fluent speech production: an ALE meta-analysis of functional neuroimaging studies. Hum Brain Mapp 2005; 25: 105-17. (Pubitemid 40656197)
19. Brown S, Laird AR, Pfordresher PQ, Thelen SM, Turkeltaub P, Liotti M. The somatotopy of speech: phonation and articulation in the human motor cortex. Brain Cogn 2009; 70: 31-41.
20. Catani M, Jones DK, ffytche DH. Perisylvian language networks of the human brain. Ann Neurol 2005; 57: 8-16. (Pubitemid 40053310)
21. Chevrie-Muller C, Plaza M. Nouvelles Epreuves pour l'Examen du Langage (N-EEL). Paris: Editions du Centre de Psychologie Appliquée; 2001.
22. Chevrie-Muller C, Simon AM, Fournier S. Batterie Langage oral et écrit. Mémoire. Attention (L2MA). Paris: Editions du Centre de Psychologie Appliquée; 1997.
23. Chiron C, Pinton F, Masure MC, Duvelleroy-Hommet C, Leon F, Billard C. Hemispheric specialization using SPECT and stimulation tasks in children with dysphasia and dystrophia. Dev Med Child Neurol 1999; 41 512-20. (Pubitemid 29389591)
24. Conti-Ramsden G. Processing and linguistic markers in young children with specific language impairment (SLI). J Speech Lang Hear Res 2003; 46: 1029-37. (Pubitemid 37204250)
25. Conti-Ramsden G, Crutchley A, Botting N. The extent to which psychometric tests differentiate subgroups of children with SLI. J Speech Lang Hear Res 1997; 40: 765-77. (Pubitemid 27338102)
26. Crinion JT, Lambon-Ralph MA, Warburton EA, Howard D, Wise RJ. Temporal lobe regions engaged during normal speech comprehension. Brain 2003; 126: 1193-201. (Pubitemid 36522961)
27. Crinion JT, Leff AP. Recovery and treatment of aphasia after stroke: functional imaging studies. Curr Opin Neurol 2007; 20: 667-73. (Pubitemid 350085008)
28. Deblaere K, Backes WH, Hofman P, Vandemaele P, Boon PA, Vonck K, et al. Developing a comprehensive presurgical functional MRI protocol for patients with intractable temporal lobe epilepsy: a pilot study. Neuroradiology 2002; 44: 667-73. (Pubitemid 36075929)
29. De Fossé L, Hodge SM, Makris N, Kennedy DN, Caviness VS, McGrath L, et al. Language-association cortex asymmetry in autism and specific language impairment. Ann Neurol 2004; 56: 757-66. (Pubitemid 39578438)
30. De Guibert C, Maumet C, Ferré JC, Jannin P, Biraben A, Allaire C, et al. fMRI language mapping in children: a panel of language tasks using visual and auditory stimulation without reading or metalinguistic requirements. Neuroimage 2010; 51: 897-909.
31. Dibbets P, Bakker K, Jolles J. Functional MRI of task switching in children with Specific Language Impairment (SLI). Neurocase 2006; 12: 71-9. (Pubitemid 43354859)
32. Dronkers NF. A new brain region for coordinating speech articulation. Nature 1996; 384: 159-61. (Pubitemid 26386469)
33. Duffau H, Bauchet L, Lehé ricy S, Capelle L. Functional compensation of the left dominant insula for language. Neuroreport 2001; 12: 2159-63. (Pubitemid 32646264)
34. Dunn M, Flax J, Sliwinksi M, Aram D. The use of spontaneous language measures as criteria for identifying children with specific language impairment: an attempt to reconcile clinical and research incongruence. J Speech Lang Hear Res 1996; 39: 643-54.
35. Ellis Weismer E, Plante E, Jones M, Tomblin JB. A functional magnetic resonance imaging investigation of verbal working memory in adolescents with specific language impairment. J Speech Lang Hear Res 2005; 48: 405-25. (Pubitemid 41043712)
36. Fisher SE, Lai CS, Monaco AP. Deciphering the genetic basis of speech and language disorders. Ann Rev Neurosci 2003; 26: 57-80. (Pubitemid 37064928)
37. Friederici AD. The neural basis of language development and its impairment. Neuron 2006a; 52: 941-52. (Pubitemid 44909410)
38. Friederici AD. What's in control of language? Nat Neurosci 2006b; 9: 991-2. (Pubitemid 44264906)
39. Friston KJ, Fletcher P, Josephs O, Holmes A, Rugg MD, Turner R. Event-related fMRI: characterizing differential responses. Neuroimage 1998; 7: 30-40. (Pubitemid 28355037)
40. Friston KJ, Holmes AP, Worsley KJ, Poline JB, Frith CD, Frackowiack RS. Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 1995; 2: 189-210. (Pubitemid 124008664)
41. 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. (Pubitemid 39426272)
42. Gaillard WD, Moore EN, Weber DA, Ritzl EK, Berl MM. Functional magnetic resonance imaging in normal and pathological language development. In: Riva D, Rapin I, Zardini G, editors. Language: normal and pathological development. Montrogue: John Libbey Eurotext; 2006. p. 105-20.
43. Gaillard WD, Sachs BC, Whitnah JR, Ahmad Z, Balsamo LM, Petrella JR, et al. Developmental aspects of language processing: fMRI of verbal fluency in children and adults. Hum Brain Mapp 2003; 18: 176-85. (Pubitemid 36331573)
44. Gauger LM, Lombardino LJ, Leonard CM. Brain morphology in children with specific language impairment. J Speech Lang Hear Res 1997; 40: 1272-84. (Pubitemid 28008823)
45. Geschwind N, Galaburda AM. Cerebral lateralization. Biological mechanisms, associations, and pathology. I. A hypothesis and a program for research. Arch Neurol 1985; 42: 428-59. (Pubitemid 15113010)
46. Giraud AL, Neumann K, Bachoud-Levi AC, von Gudenberg AW, Euler HA, Lanfermann H, et al. Severity of dysfluency correlates with basal ganglia activity in persistent developmental stuttering. Brain Lang 2008; 104: 190-9. (Pubitemid 351173293)
47. Grahn JA, Parkinson JA, Owen AM. The cognitive functions of the caudate nucleus. Prog Neurobiol 2008; 86: 141-55.
48. Hardyck C, Petrinovich LF. Left-handedness. Psychol Bull 1977; 84: 385-404.
49. Harris GJ, Chabris CF, Clark J, Urban T, Aharon I, Steele S, et al. Brain activation during semantic processing in autism spectrum disorders via functional magnetic resonance imaging. Brain Cogn 2006; 61: 54-68.
50. Heim S, Grande M, Meffert E, Eickhoff SB, Schreiber H, Kukolja J, et al. Cognitive levels of performance account for hemispheric lateralisation effects in dyslexic and normally reading children. Neuroimage 2010; 53: 1346-58.
51. Herbert MR, Kenet T. Brain abnormalities in language disorders and in autism. Pediatr Clin North Am 2007; 54: 563-83. (Pubitemid 46830796)
52. Herbert MR, Ziegler DA, Deutsch CK, O'Brien LM, Kennedy DN, Filipek PA, et al. Brain asymmetries in autism and developmental language disorder: a nested whole-brain analysis. Brain 2005; 128: 213-26. (Pubitemid 40070534)
53. Hickok G, Buchsbaum B, Humphries C, Muftuler T. Auditory-motor interaction revealed by fMRI: speech, music, and working memory in area Spt. J Cogn Neurosci 2003; 15: 673-82. (Pubitemid 36871881)
54. Hickok G, Poeppel D. The cortical organization of speech processing. Nat Rev Neurosci 2007; 8: 393-402. (Pubitemid 46652465)
55. Hillis AE. Aphasia: progress in the last quarter of a century. Neurology 2007; 69: 200-13. (Pubitemid 47051726)
56. Hillis AE, Work M, Barker PB, Jacobs MA, Breese EL, Maurer K. Re-examining the brain regions crucial for orchestrating speech articulation. Brain 2004; 127: 1479-87. (Pubitemid 38899401)
57. Holland SK, Vannest J, Mecoli M, Jacola LM, Tillema JM, Karunanayaka PR, et al. Functional MRI of language lateralization during development in children. Int J Audiol 2007; 46: 533-51. (Pubitemid 350194925)
58. Hugdahl K, Gundersen H, Brekke C, Thomsen T, Rimol LM, Ersland L, et al. fMRI brain activation in a Finnish family with specific language impairment compared with a normal control group. J Speech Lang Hear Res 2004; 47: 162-72. (Pubitemid 38338390)
59. Jäncke L, Siegenthaler T, Preis S, Steinmetz H. Decreased white-matter density in a left-sided fronto-temporal network in children with developmental language disorder: evidence for anatomical anomalies in a motor-language network. Brain Lang 2007; 102: 91-8. (Pubitemid 46809753)
60. Jernigan TL, Hessenlink JR, Sowell E, Tallal PA. Cerebral structure on magnetic resonance imaging in language-and-learning-impaired children. Arch Neurol 1991; 48: 539-45.
61. Just MA, Cherkassky VL, Keller TA, Minshew NJ. Cortical activation and synchronization during sentence comprehension in high-functioning autism: evidence of underconnectivity. Brain 2004; 127: 1811-21. (Pubitemid 39061557)
62. Kell CA, Neumann K, von Kriegstein K, Posenenske C, von Gudenberg AW, Euler A, et al. How the brain repairs stuttering. Brain 2009; 132: 2747-60.
63. Keller SS, Crow T, Foundas A, Amunts K, Roberts N. Broca's area: nomenclature, anatomy, typology and asymmetry. Brain Lang 2009; 109: 29-48.
64. Kleinhans NM, Mü ller RA, Cohen DN, Courchesne E. Atypical functional lateralization of language in autism spectrum disorders. Brain Res 2008; 1221: 115-25.
65. Knaus TA, Silver AM, Lindgren KA, Hadjikhani N, Tager-Flusberg H. fMRI activation during a language task in adolescents with ASD. J Int Neuropsychol Soc 2008; 14: 967-79.
66. Leach JL, Holland SK. Functional MRI in children: clinical and research applications. Pediatr Radiol 2010; 40: 31-49.
67. Leonard CM, Lombardino LJ, Walsh K, Eckert MA, Mockler JL, Rowe LA, et al. Anatomical risk factors that distinguish dyslexia from SLI predict reading skill in normal children. J Commun Disord 2002; 35: 501-31. (Pubitemid 35292089)
68. Lié geois F, Baldeweg T, Connelly A, Gadian DG, Mishkin M, Vargha-Kadem F. Language fMRI abnormalities associated with FOXP2 gene mutation. Nat Neurosci 2003; 6: 1230-37.
69. Lou HC, Henriksen L, Bruhn P. Focal cerebral hypoperfusion in children with dysphasia and/or attention deficit disorder. Arch Neurol 1984; 41: 825-9. (Pubitemid 14091724)
70. Maisog JM, Einbinder ER, Flowers DL, Turkeltaub PE, Eden GF. A meta-analysis of functional neuroimaging studies of dyslexia. Ann N Y Acad Sci 2008; 1145: 237-59.
71. Medina LS, Bernal B, Ruiz J. Role of functional MR in determining language dominance in epilepsy and nonepilepsy populations: a Bayesian analysis. Radiology 2007; 242: 94-100. (Pubitemid 44956013)
72. Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971; 9: 97-113.
73. Ors M, Ryding E, Lindgren M, Gustafsson P, Blennow G, Rosen I. SPECT findings in children with specific language impairment. Cortex 2005; 41: 316-26. (Pubitemid 40561455)
74. O'Shaughnessy ES, Berl MM, Moore EN, Gaillard WD. Pediatric functional magnetic resonance imaging (fMRI): issues and applications. J Child Neurol 2008; 23: 791-801. (Pubitemid 351998168)
75. Parisse C, Maillart C. Specific language impairment as systemic developmental disorders. J Neuroling 2009; 22: 109-22.
76. Paulesu E, Frith U, Snowling M, Gallagher A, Morton J, Frackowiak RS, et al. Is developmental dyslexia a disconnection syndrome? Evidence from PET scanning. Brain 1996; 119: 143-57. (Pubitemid 26077561)
77. Plante E, Swisher L, Vance R. fMRI findings in boys with specific language impairment. Brain Lang 1991; 41: 52-66.
78. Preibisch C, Neumann K, Raab P, Euler HA, von Gudenberg AW, Lanfermann H, et al. Evidence for compensation for stuttering by the right frontal operculum. Neuroimage 2003; 20: 1356-64. (Pubitemid 37268153)
79. Preis S, Jä ncke L, Schittler P, Huanq Y, Steinmetz H. Normal intrasylvian anatomical asymmetry in children with developmental language disorder. Neuropsychologia 1998; 36: 849-55. (Pubitemid 28404312)
80. Price CJ. The anatomy of language: a review of 100 fMRI studies published in 2009. Ann N Y Acad Sci 2010; 1191: 62-88.
81. Ramsey NF, Sommer I, Rutten GJ, Kahn R. Combined analysis of language tasks in fMRI improves assessment of hemispheric dominance for language functions in individual subjects. Neuroimage 2001; 13: 719-33. (Pubitemid 34184993)
82. Ramus F, Szenkovits G. What phonological deficit? Q J Exp Psychol 2008; 61: 129-41.
83. Rapin I, Allen DA. Developmental language disorders: nosological considerations. In: Kirk U, editor. Neuropsychology of language, reading and spelling. New York: Academic Press; 1983. p. 155-84.
84. Rapin I, Dunn M, Allen DA. Developmental language disorders. In: Segalowitz SJ, Rapin I, editors. Handbooks of neuropsychology. Vol. 8, Part II. Amsterdam: Elsevier; 2003. p. 593-630.
85. Richlan F, Kronbichler M, Wimmer H. Functional abnormalities in the dyslexic brain: a quantitative meta-analysis of neuroimaging studies. Hum Brain Mapp 2009; 30: 3299-308.
86. Roux FE, Boulanouar K, Lotterie JA, Mejdoubi M, Le Sage JP, Berry I. Language functional magnetic resonance imaging in preoperative assessment of language areas: correlation with direct cortical stimulation. Neurosurgery 2003; 52: 1335-47. (Pubitemid 36666949)
87. Rutten GJ, Ramsey NF, van Rijen PC, van Veelen CW. Reproducibility of fMRI-determined language lateralization in individual subjects. Brain Lang 2002; 80: 421-37. (Pubitemid 34921332)
88. Schulz E, Maurer U, van der Mark S, Bucher K, Brem S, Martin E, et al. Impaired semantic processing during sentence reading in children with dyslexia: combined fMRI and ERP evidence. Neuroimage 2008; 41: 153-68.
89. Shaywitz SE, Shaywitz BA. Paying attention to reading: the neurobiology of reading and dyslexia. Dev Psychopathol 2008; 20: 1329-49.
90. Soriano-Mas C, Pujol J, Ortiz H, Deus J, Ló pez-Sala A, Sans A. Age-related brain structural alterations in children with specific language impairment. Hum Brain Mapp 2009; 30: 1626-36.
91. Steinbrink C, Ackermann H, Lachmann T, Riecker A. Contribution of the anterior insula to temporal auditory processing deficits in developmental dyslexia. Hum Brain Mapp 2009; 30: 2401-11.
92. Stothard SE, Snowling MJ, Bishop DV, Chipchase BB, Kaplan CA. Language-impaired preschoolers: a follow-up into adolescence. J Speech Lang Hear Res 1998; 41: 407-18. (Pubitemid 28178201)
93. Szaflarski JP, Binder JR, Possing ET. Language lateralization in left-handed and ambidextrous people. fMRI data. Neurology 2002; 59: 238-44. (Pubitemid 34779184)
94. Tie Y, Whalen S, Suarez RO, Golby AJ. Group independent component analysis of language fMRI from word generation tasks. Neuroimage 2008; 42: 1214-25.
95. Tomblin JB, Records NL, Zhang W. A system for the diagnosis of specific language impairment in kindergarten children. J Speech Lang Hear Res 1996; 39: 1284-94.
96. Tzourio N, Heim H, Zilbovicius M, Gerard C, Mazoyer BM. Abnormal regional CBF response in left hemisphere of dysphasic children during a language task. Pediatr Neurol 1994; 10: 20-6. (Pubitemid 24096716)
97. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 2002; 15: 273-89. (Pubitemid 34852226)
98. Uddin LQ, Menon V. The anterior insula in autism: under-connected and under-examined. Neurosci Biobehav Rev 2009; 33: 1198-203.
99. Van der Lely HKJ. Domain-specific cognitive systems: insight from grammatical specific language impairment. Trends Cogn Sci 2005; 9: 53-9.
100. Van Hout A. Acquired aphasia in childhood. In: Segalowitz SJ, Rapin I, editors. Handbooks of neuropsychology. Vol. 8, Part II. Amsterdam: Elsevier; 2003. p. 631-58.
101. Vargha-Khadem F, Gadian DG, Copp A, Mishkin M. FOXP2 and the neuroanatomy of speech and language. Nat Rev Neurosci 2005; 6: 131-8. (Pubitemid 40188947)
102. Vargha-Khadem F, Watkins KE, Price CJ, Ashburner J, Alcock KJ, Connelly A, et al. Neural basis of an inherited speech and language disorder. Proc Natl Acad Sci USA 1998; 95: 12695-700. (Pubitemid 28483827)
103. Voets NL, Adcock JE, Flitney DE, Behrens TEJ, Hart Y, Stacey R, et al. Distinct right frontal lobe activation in language processing following left hemisphere injury. Brain 2006; 129: 754-66. (Pubitemid 43278237)
104. Watkins KE, Smith SM, Davis S, Howell P. Structural and functional abnormalities of the motor system in developmental stuttering. Brain 2008; 131: 50-9.
105. Watkins KE, Vargha-Khadem F, Ashburner J, Passingham R, Connelly A, Friston K, et al. MRI analysis of an inherited speech and language disorder: Structural brain abnormalities. Brain 2002; 125: 465-78. (Pubitemid 34194403)
106. Webster RI, Shevell MI. Neurobiology of specific language impairment. J Child Neurol 2004; 19: 471-81. (Pubitemid 39481245)
107. Wechsler D. WAIS-III administration and scoring manual. San Antonio, TX: The Psychological Corporation; 1997.
108. Wechsler D. Wechsler Intelligence Scale for Children-Fourth Edition. San Antonio, TX: Psychological Corporation; 2003.
109. Whitehouse JO, Bishop DV. Cerebral dominance for language function in adults with specific language impairment or autism. Brain 2008; 131: 3193-200.
110. Wilke M, Holland SK, Altaye M, Gaser C. Template-O-Matic: a toolbox for creating customized pediatric templates. NeuroImage 2008; 41: 903-13.
111. Wilke M, Lidzba KJ. LI-tool: a new toolbox to assess lateralization in functional MR-data. J Neurosci Methods 2007; 163: 128-36. (Pubitemid 46660122)
112. Wilke M, Lidzba KJ, Staudt M, Buchenau K, Grodd W, Krägeloh-Mann I. An fMRI task battery for assessing hemispheric language dominance in children. Neuroimage 2006; 32: 400-10.
113. Wilke M, Schmithorst VJ, Holland SK. Normative pediatric brain data for spatial normalization and segmentation differs from standard adult data. Magn Reson Med 2003a; 50: 749-57. (Pubitemid 37187840)
114. Wilke M, Sohn JH, Byars AW, Holland SK. Bright spots: correlations of gray matter volume with IQ in a normal pediatric population. Neuroimage 2003b; 20: 202-15. (Pubitemid 37188510)