Effect of familial sinistrality on planum temporale surface and brain tissue asymmetries

Cerebral Cortex

Volumn 20, Issue 6, 2010, Pages 1476-1485

  Tzourio Mazoyer, Nathalie ^a   Simon, Gregory ^a   Crivello, Fabrice ^a   Jobard, Gael ^a   Zago, Laure ^a   Perchey, Guy ^a,b   Hervé, Pierre Yves ^a   Joliot, Marc ^a   Petit, Laurent ^a   Mellet, Emmanuel ^a   Mazoyer, Bernard ^a,c  

^a UNIVERSITÉ DE CAEN   (France)

^b CAEN UNIVERSITY HOSPITAL   (France)

^c INSTITUT UNIVERSITAIRE DE FRANCE   (France)

Author keywords

Familial sinistrality; Handedness; Hemispheric specialization; Language; Planum temporale

Indexed keywords

ADULT; ARTICLE; BRAIN CORTEX; CHILD; FEMALE; GRAY MATTER; HAND STRENGTH; HUMAN; HUMAN TISSUE; LANGUAGE; LEFT HANDEDNESS; MALE; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PLANUM TEMPORALE; PRIORITY JOURNAL; RIGHT HEMISPHERE; SCHOOL CHILD; SEX DIFFERENCE; WHITE MATTER;

ADOLESCENT; ADULT; AUDITORY CORTEX; AUDITORY PERCEPTION; BRAIN MAPPING; CORPUS CALLOSUM; DOMINANCE, CEREBRAL; FEMALE; FUNCTIONAL LATERALITY; HUMANS; LANGUAGE; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEURAL PATHWAYS; SPEECH PERCEPTION; VERBAL BEHAVIOR; YOUNG ADULT;

EID: 77952827046     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhp209     Document Type: Article

References (97)

1. Abrahams BS, Tentler D, Perederiy JV, Oldham MC, Coppola G, Geschwind DH. 2007. Genome-wide analyses of human perisylvian cerebral cortical patterning. Proc Natl Acad Sci USA. 104:17849-17854.
2. Anneken K, Konrad C, Drager B, Breitenstein C, Kennerknecht I, Ringelstein EB, Knecht S. 2004. Familial aggregation of strong hemispheric language lateralization. Neurology. 63:2433-2435.
3. Annett M. 1998. Handedness and cerebral dominance: the right shift theory. J Neuropsychiatry. 10:459-469.
4. Barrick TR, Mackay CE, Prima S, Maes F, Vandermeulen D, Crow TJ, Roberts N. 2005. Automatic analysis of cerebral asymmetry: an exploratory study of the relationship between brain torque and planum temporale asymmetry. NeuroImage. 24:678-691.
5. Binder JR, Frost JA, Hammeke TA, Bellgowan PSF, Springer JA, Kaufman JN, Possing ET. 2000. Human temporal lobe activation by speech and nonspeech sounds. Cereb Cortex. 10:512-528.
6. Binder JR, Frost JA, Hammeke TA, Rao SM, Cox RW. 1996. Function of the left planum temporale in auditory and linguistic processing. Brain. 119:1239-1247.
7. Boemio A, Fromm S, Braun A, Poeppel D. 2005. Hierarchical and asymmetric temporal sensitivity in human auditory cortices. Nat Neurosci. 8:389-395.
8. Broca P. 1861. Remarques sur le siege de la faculte du language articule, suivies d'une observation d'aphemie (perte de la parole). Bull Mem Soc Anatom Paris. 36:330-357.
9. Bryden MP, Hecaen H, DeAgostini M. 1983. Patterns of cerebral organization. Brain Lang. 20:249-262.
10. Casey MB, Nuttall RL, Pezaris E. 1997. Mediators of gender differences in mathematics college entrance test scores: a comparison of spatial skills with internalized beliefs and anxieties. Dev. Psychol. 33:669-680.
11. Casey MB, Pezaris E, Nuttall RL. 1992. Spatial ability as a predictor of math achievement: the importance of sex and handedness patterns. Neuropsychologia. 30:35-45.
12. Corballis MC. 2008. Review. The evolution and genetics of cerebral asymmetry. Philos Trans R Soc Lond B Biol Sci. 364:867-879.
13. Corballis MC. 2009. The evolution and genetics of cerebral asymmetry. Philos Trans R Soc Lond B Biol Sci. 364:867-879.
14. Corey DM, Foundas AL. 2005. Measuring familial sinistrality: problems with dichotomous classification. Laterality. 10:321-335.
15. Crow TJ. 2002. Handedness, language lateralisation and anatomical asymmetry: relevance of protocadherin XY to hominid speciation and the aetiology of psychosis. Point of view. Br. J. Psychiatry. 181:295-297.
16. Crow TJ. 2009. A theory of the origin of cerebral asymmetry: epigenetic variation superimposed on a fixed right-shift. Laterality. 1-15.
17. Crow TJ, Crow LR, Done DJ, Leask S. 1998. Relative hand skill predicts academic ability: global deficits at the point of hemispheric indecision. Neuropsychologia. 36:1275-1282.
18. D'Andrea EA, Spiers MV. 2005. The effect of familial sinistrality and academic experience on cognition in right-handed women. Neuropsychology. 19:657-663.
19. Diallo B, Dolidon F, Travere J-M, Mazoyer B. 1998. VoxeLine: a software for 3D real-time visualization of biomedical images. Comput Med Imaging Graph. 22:275-289.
20. Eckert MA, Leonard CM, Possing ET, Binder JR. 2006. Uncoupled leftward asymmetries for planum morphology and functional language processing. Brain Lang. 98:102-111.
21. Filipek PA. 1995. Neurobiologic correlates of developmental dyslexia: how do dyslexics brain differ from those of normal readers? J Child Neurol. 10:S62-S69.
22. Foundas AL, Leonard CM, Hanna-Pladdy B. 2002. Variability in the anatomy of the planum temporale and posterior ascending ramus: do right-and left handers differ? Brain Lang. 83:403-424.
23. Foundas AL, Leonard CM, Heilman KM. 1995. Morphological asymmetries and handedness. The pars triangularis and planum temporale. Arch Neurol. 52:501-508.
24. Francks C, DeLisi LE, Shaw SH, Fisher SE, Richardson AJ, Stein JF, Monaco AP. 2003. Parent-of-origin effects on handedness and schizophrenia susceptibility on chromosome 2p12-q11. Hum Mol Genet. 12:3225-3230.
25. Francks C, Fisher SE, MacPhie IL, Richardson AJ, Marlow AJ, Stein JF, Monaco AP. 2002. A genomewide linkage screen for relative hand skill in sibling pairs. Am J Hum Genet. 70:800-805.
26. Francks C, Maegawa S, Lauren J, Abrahams BS, Velayos-Baeza A, Medland SE, Colella S, Groszer M, McAuley EZ, Caffrey TM, et al. 2007. LRRTM1 on chromosome 2p12 is a maternally suppressed gene that is associated paternally with handedness and schizophrenia. Mol Psychiatry. 12:10571129-10571139.
27. Galaburda AM, Sanides F, Geschwind N. 1978. Human brain. Cytoarch-itectonic left-right asymmetries in the temporal speech region. Arch Neurol. 35:812-817.
28. Geschwind N, Levitsky W. 1968. Human brain left-right asymmetries in temporal speech region. Science. 161:186-187.
29. Griffiths TD, Warren JD. 2002. The planum temporale as a computational hub. Trends Neurosci. 25:348-353.
30. Habib M. 2000. The neurological basis of developmental dyslexia\an overview and working hypothesis. Brain. 123:2373-2399.
31. Habib M, Gayraud D, Oliva A, Regis J, Salamon G, Khalil R. 1991. Effects of handedness and sex on the morphology of the corpus callosum: a study with brain magnetic resonance imaging. Brain Cogn. 16:41-61.
32. Habib M, Robichon F, Levrier O, Khalil R, Salamon G. 1995. Diverging asymmetries of temporo-parietal cortical areas: a reappraisal of Geschwind-Galaburda theory. Brain Lang. 48:238-258.
33. Halpern DF. 1996. Sex, brains hand and spatial cognition. Dev Rev. 16:261-270.
34. Hardyck C, Petrinovich LF. 1977. Left-handedness. Psychol Bull. 84:385-404.
35. Hecaen H, De Agostini M, Monzon-Montes A. 1981. Cerebral organization in left-handers. Brain Lang. 12:261-284.
36. Hecaen H, Sauguet J. 1971. Cerebral dominance in left-handed subjects. Cortex. 7:19-48.
37. Heiervang E, Hugdahl K, Steinmetz H, Inge SA, Stevenson J, Lund A, Ersland L, Lundervold A. 2000. Planum temporale, planum parietale and dichotic listening in dyslexia. Neuropsychologia. 38: 1704-1713.
38. Herve PY, Crivello F, Perchey G, Mazoyer B, Tzourio-Mazoyer N. 2006. Handedness and cerebral anatomical asymmetries in young adult males. NeuroImage. 29:1066-1079.
39. Herve PY, Mazoyer B, Crivello F, Perchey G, Tzourio-Mazoyer N. 2005. Finger tapping, handedness and grey matter amount in the Rolando's genu area. NeuroImage. 25:1133-1145.
40. Hund-Georgiadis M, Lex U, Friederici AD, von Cramon DY. 2002. Non-invasive regime for language lateralization in right-and left-handers by means of functional MRI and dichotic listening. Exp Brain Res. 145:166-176.
41. Hund-Georgiadis M, Lex U, von Cramon DY. 2001. Language dominance assessment by means of fMRI: contributions from task design, performance, and stimulus modality. J Magn Reson Imaging. 13:668-675.
42. Jancke L, Buchanan TW, Lutz K, Shah NJ. 2001. Focused and nonfocused attention in verbal and emotional dichotic listening: an FMRI study. Brain Lang. 78:349-363.
43. Jancke L, Steinmetz H. 1993. Auditory lateralization and planum temporale asymmetry. Neuroreport. 5:169-172.
44. Jancke L, Wustenberg T, Scheich H, Heinze HJ. 2002. Phonetic perception and the temporal cortex. Neuroimage. 15:733-746.
45. Jancke L, Wustenberg T, Schulze K, Heinze HJ. 2002. Asymmetric hemodynamic responses of the human auditory cortex to monaural and binaural stimulation. Hear Res. 170:166.
46. Jerningan TL, Hesselink JR, Sowell E, Tallal PA. 1991. Cerebral structure on magnetic resonance imaging in language-and learning-impaired children. Arch Neurol. 48:539-545.
47. Johnson MB, Kawasawa YI, Mason CE, Krsnik Z, Coppola G, Bogdanovic D, Geschwind DH, Mane SM, State MW, Sestan N. 2009. Functional and evolutionary insights into human brain development through global transcriptome analysis. Neuron. 62: 494-509.
48. Jones GV, Martin M. 2006. Handedness, left/right: genetics. In: Wiley & Sons, editor. Encyclopedia of life sciences. Available from: URL http://www.mrw.interscience.wiley.com/emrw/9780470015902/els/article/a0005961/ current/abstract?hd=All,handedness.
49. Josse G, Herve PY, Crivello F, Mazoyer B, Tzourio-Mazoyer N. 2006. Hemispheric specialization for language: brain volume matters. Brain Res. 1068:184-193.
50. Klar AJ. 1999. Genetic models for handedness, brain lateralization, schizophrenia, and manic-depression. Schizophr Res. 39:207-218.
51. Knaus TA, Bollich AM, Corey DM, Lemen LC, Foundas AL. 2004. Sex-linked differences in the anatomy of the perisylvian language cortex: a volumetric MRI study of gray matter volumes. Neuropsy-chology. 18:738-747.
52. Knaus TA, Bollich AM, Corey DM, Lemen LC, Foundas AL. 2006. Variability in perisylvian brain anatomy in healthy adults. Brain Lang. 97:219-232.
53. Knecht S, Drager B, Deppe M, Bobe L, Lohmann H, Floel A, Ringelstein EB, Henningsen H. 2000. Handedness and hemispheric language dominance in healthy humans. Brain. 123:2512-2518.
54. Kulynych JJ, Vladar K, Jones DW, Weinberger DR. 1993. Three-dimentional surface rendering in MRI morphometry: a study of the planum temporale. J Comput Assist Tomogr. 17:529-535.
55. Kulynych JJ, Vladar K, Jones DW, Weinberger DR. 1994. Gender differences in the normal lateralization of the supratemporal cortex: MRI surface-rendering morphometry of Heschl's gyrus and the planum temporale. Cereb Cortex. 4:107-118. (Pubitemid 24127821)
56. Kushch A, Gross-Glenn K, Jallad B, Lubs H, Rabin M, Feldman E, Duara R. 1993. Temporal lobe surface area measurements on MRI in normal and dyslexics readers. Neuropsychologia. 31:811-821.
57. Larsen JP, Hqien T, Lundberg I, Ædegaard H. 1990. MRI evaluation of the size and symmetry of the planum temporale in adolescents with developmental dyslexia. Brain Lang. 39:289-301.
58. Leonard C, Eckert M, Given B, Virginia B, Eden G. 2006. Individual differences in anatomy predict reading and oral language impairments in children. Brain. 129:3329-3342.
59. Leonard CM, Eckert MA, Lombardino LJ, Oakland T, Kranzler J, Mohr CM, King WM, Freeman A. 2001. Anatomical risk factors for phonological dyslexia. Cereb.Cortex. 11:148-157.
60. Leonard CM, Puranik C, Kuldau JM, Lombardino LJ. 1998. Normal variation in the frequency and location of human auditory cortex landmarks. Heschl's gyrus: where is it? Cereb Cortex. 8:397-406.
61. Leonard CM, Towler S, Welcome S, Halderman LK, Otto R, Eckert MA, Chiarello C. 2008. Size matters: cerebral volume influences sex differences in neuroanatomy. Cereb Cortex. 18:2920-2931.
62. Luders E, Steinmetz H, Jancke L. 2002. Brain size and grey matter volume in the healthy human brain. Neuroreport. 13:2371-2374.
63. McKeever WF, Cerone LJ, Chase-Carmichael C. 2000. Developmental instability and right shift theory hypotheses concerning correlates of familial sinistrality: negative findings. Laterality. 5:97-110.
64. McManus IC, Bryden MP. 1991. Geshwind's theory of cerebral lateralization: developing a formal causal model. Psychol Bull. 110:237-253.
65. Moffat SD, Hampson E, Lee DH. 1998. Morphology of the planum temporale and corpus callosum in left handers with evidence of left and right hemisphere speech representation. Brain. 121:2369-2379.
66. Morgan AE, Hynd GW. 1998. Dyslexia, neurolinguistic ability, and anatomical variation of the planum temporale. Neuropsychol Rev. 8:79-93.
67. Morosan P, Rademacher J, Schleicher A, Amunts K, Schormann T, Zilles K. 2001. Human primary auditory cortex: cytoarchitectonic subdivisions and mapping into a spatial reference system. Neuroimage. 13:684-701.
68. Oldfield RC. 1971. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 9:97-113.
69. Ono M, Kubik S, Abernathey CD. 1990. Atlas of the cerebral sulci. New York: Thieme Medical Publishers, Inc.
70. Orsini DL, Satz P, Soper HV, Light RK. 1985. The role of familial sinistrality in cerebral organization. Neuropsychologia. 23:223-232.
71. Penhune VB, Zatorre RJ, MacDonald JD, Evans AC. 1996. Interhemi-spheric anatomical differences in human primary auditory cortex: probabilistic mapping and volume measurement from magnetic resonance scans. Cereb Cortex. 6:661-672.
72. Peters M, Durding BM. 1978. Handedness measured by finger tapping: a continuous variable. Can J Psychol. 32:257-261.
73. Peters M, Reimers S, Manning JT. 2006. Hand preference for writing and associations with selected demographic and behavioral variables in 255,100 subjects: the BBC internet study. Brain Cogn. 62:177-189.
74. Ringo JL, Doty RW, Demeter S, Simard PY. 1994. Time is of the essence: a conjecture that hemispheric specialization arises from interhemi-spheric conduction delay. Cereb Cortex. 4:331-343. (Pubitemid 24228839)
75. Rumsey JM, Donohue BC, Brady DR, Nace K, Giedd JN, Andreason P. 1997. A magnetic resonance imaging study of planum temporale asymmetry in men with developmental dyslexia. Arch Neurol. 54:1481-1489.
76. Rumsey JM, Dorwart RD, Vermess M, Denckla MB, Kruesi MJP, Rapoport JL. 1986. Magnetic resonance of brain anatomy in severe developmental dyslexia. Arch Neurol. 43:1045-1046.
77. Satz P. 1979. A test of some models of hemispheric speech organization in the left-and right-handed. Science. 203:1131-1133.
78. Schluter ND, Krams M, Rushworth MFS, Passingham RE. 2001. Cerebral dominance for action in the human brain: the selection of actions. Neuropsychologia. 39:105-113.
79. Sequeira SS, Woerner W, Walter C, Kreuder F, Lueken U, Westerhausen R, Wittling RA, Schweiger E, Wittling W. 2006. Handedness, dichotic-listening ear advantage, and gender effects on planum temporale asymmetry-a volumetric investigation using structural magnetic resonance imaging. Neuropsychologia. 44:622-636.
80. Shah NJ, Steinhoff S, Mirzazade S, Zafiris O, Grosse-Ruyken ML, Jancke L, Zilles K. 2000. The effect of sequence repeat time on auditory cortex stimulation during phonetic discrimination. NeuroImage. 12:100-108.
81. Shapleske J, Rossell SL, Woodruff PW, David AS. 1999. The planum temporale: a systematic, quantitative review of its structural, functional and clinical significance. Brain Res Rev. 29:26-49.
82. Sommer IE, Aleman A, Somers M, Boks MP, Kahn RS. 2008. Sex differences in handedness, asymmetry of the planum temporale and functional language lateralization. Brain Res. 1206:76-88.
83. Sowell ER, Thompson PM, Tessner KD, Toga AW. 2001. Mapping continued brain growth and gray matter density reduction in dorsal frontal cortex: Inverse relationships during postadolescent brain maturation. J Neurosci. 21:8819-8829.
84. Spiegler BJ, Yeni-Komshian GH. 1983. Incidence of left-handed writing in a college population with reference to family patterns of hand preference. Neuropsychologia. 21:651-659.
85. Steinmetz H, Rademacher J, Huang Y, Hefter H, Zilles K, Thron A, Freund H-J. 1989. Cerebral asymmetry: MR planimetry of the human planum temporale. J Comput Assist Tomogr. 13:996-1005.
86. Steinmetz H, Rademacher J, Jancke L, Huang Y, Thron A, Zilles K. 1990. Total surface of temporoparietal intrasylvian cortex: diverging left-right asymmetries. Brain Lang. 39:357-372.
87. Steinmetz H, Volkmann J, Jancke L, Freund H-J. 1991. Anatomical left-right asymmetry of language-related temporal cortex is different in left-and right-handers. Ann Neurol. 29:315-319.
88. Sun T, Patoine C, bu-Khalil A, Visvader J, Sum E, Cherry TJ, Orkin SH, Geschwind DH, Walsh CA. 2005. Early asymmetry of gene transcription between embryonic human left and right cerebral cortex. Science. 308:1794-1798.
89. Teszner D, Tzavaras A, Gruner J, Hecaen H. 1972. Right-left asymmetry of the planum temporale; apropos of the anatomical study of 100 brains. Rev Neurol. 126:444-449.
90. Tzourio N, Nkanga-Ngila B, Mazoyer B. 1998. Left planum temporale surface correlates with functional dominance during story listening. Neuroreport. 9:829-833.
91. Van Agtmael T, Forrest SM, Williamson R. 2002. Parametric and non-parametric linkage analysis of several candidate regions for genes for human handedness. Eur J Hum Genet. 10:623-630.
92. Wallentin M. 2009. Putative sex differences in verbal abilities and language cortex: a critical review. Brain Lang. 108:175-183.
93. Warrier C, Wong P, Penhune V, Zatorre R, Parrish T, Abrams D, Kraus N. 2009. Relating structure to function: Heschl's gyrus and acoustic processing. J Neurosci. 29:61-69.
94. Watkins KE, Paus T, Lerch JP, Zijdenbos A, Collins DL, Neelin P, Taylor J, Worsley KJ, Evans AC. 2001. Structural asymmetries in the human brain: a voxel-based statistical analysis of 142 mri scans. Cereb Cortex. 11:868-877.
95. Witelson SF. 1977. Anatomic asymmetry in the temporal lobes: its documentation, phylogenesis, and relationship to functional asymmetry. Ann N Y Acad Sci. 299:328-354.
96. Wong PC, Warrier CM, Penhune VB, Roy AK, Sadehh A, Parrish TB, Zatorre RJ. 2008. Volume of left Heschl's gyrus and linguistic pitch learning. Cereb Cortex. 18:828-836.
97. Zatorre RJ, Evans AE, Meyer E, Gjedde A. 1992. Lateralization of phonetic and pitch discrimination in speech processing. Science. 256:846-847.