Colateralization of Broca’s area and the visual word form area in left-handers: fMRI evidence

Language production has been found to be lateralized in the left hemisphere (LH) for 95% of right-handed people and about 75% of left-handers. The prevalence of atypical right hemispheric (RH) or bilateral lateralization for reading and colateralization of production with word reading laterality has never been tested in a large sample. In this study, we scanned 57 left-handers who had previously been identified as being clearly left (N=30), bilateral (N=7) or clearly right (N=20) dominant for speech on the basis of fMRI activity in the inferior frontal gyrus (pars opercularis/pars triangularis) during a silent word generation task. They were asked to perform a lexical decision task, in which words were contrasted against checkerboards, to test the lateralization of reading in the ventral occipitotemporal region. Lateralization indices for both tasks correlated significantly (r=0.59). The majority of subjects showed most activity during lexical decision in the hemisphere that was identified as their word production dominant hemisphere. However, more than half of the sample (N=31) had bilateral activity for the lexical decision task without a clear dominant role for either the LH or RH, and three showed a crossed frontotemporal lateralization pattern. These findings have consequences for neurobiological models relating phonological and orthographic processes, and for lateralization measurements for clinical purposes.

[1]  S. Dehaene,et al.  Beyond Hemispheric Dominance: Brain Regions Underlying the Joint Lateralization of Language and Arithmetic to the Left Hemisphere , 2010, Journal of Cognitive Neuroscience.

[2]  Vincent Schmithorst,et al.  A combined bootstrap/histogram analysis approach for computing a lateralization index from neuroimaging data , 2006, NeuroImage.

[3]  E. T. Possing,et al.  Functional MRI and Wada studies in patients with interhemispheric dissociation of language functions , 2008, Epilepsy & Behavior.

[4]  Peter Hagoort,et al.  Reflections on the neurobiology of syntax , 2009 .

[5]  Paul M Matthews,et al.  The Role of the Posterior Fusiform Gyrus in Reading , 2006, Journal of Cognitive Neuroscience.

[6]  Mohamed L. Seghier,et al.  Laterality index in functional MRI: methodological issues☆ , 2008, Magnetic resonance imaging.

[7]  K. Rastle,et al.  Masked phonological priming effects in English: Are they real? Do they matter? , 2006, Cognitive Psychology.

[8]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[9]  Cathy J. Price,et al.  Top-down modulation of ventral occipito-temporal responses during visual word recognition , 2011, NeuroImage.

[10]  A. W. Ellis,et al.  Divided opinions on the split fovea , 2010, Neuropsychologia.

[11]  John S. Duncan,et al.  Hemispheric asymmetries in language-related pathways: A combined functional MRI and tractography study , 2006, NeuroImage.

[12]  E. Ringelstein,et al.  Handedness and hemispheric language dominance in healthy humans. , 2000, Brain : a journal of neurology.

[13]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[14]  Fabrice Crivello,et al.  Left planum temporale: an anatomical marker of left hemispheric specialization for language comprehension. , 2003, Brain research. Cognitive brain research.

[15]  K. Rayner Eye movements in reading and information processing: 20 years of research. , 1998, Psychological bulletin.

[16]  M. Carreiras,et al.  Phonology by itself: Masked phonological priming effects with and without orthographic overlap , 2011 .

[17]  J. Grainger,et al.  Phonology and Orthography in Visual Word Recognition: Evidence from Masked Non-Word Priming , 1992, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[18]  Joseph T Devlin,et al.  The myth of the visual word form area , 2003, NeuroImage.

[19]  Cathy J. Price,et al.  Lateralization is Predicted by Reduced Coupling from the Left to Right Prefrontal Cortex during Semantic Decisions on Written Words , 2010, Cerebral cortex.

[20]  Michael I. G. Simpson,et al.  The neural basis of the right visual field advantage in reading: An MEG analysis using virtual electrodes , 2011, Brain and Language.

[21]  Matthew F Glasser,et al.  DTI tractography of the human brain's language pathways. , 2008, Cerebral cortex.

[22]  R. C. Oldfield THE ASSESSMENT AND ANALYSIS OF HANDEDNESS , 1971 .

[23]  M. Brysbaert,et al.  Further fMRI validation of the visual half field technique as an indicator of language laterality: A large-group analysis , 2011, Neuropsychologia.

[24]  A. Raymer,et al.  Broca's Area , 2003 .

[25]  N. Geschwind,et al.  Human Brain: Left-Right Asymmetries in Temporal Speech Region , 1968, Science.

[26]  Marc Brysbaert,et al.  Cerebral Lateralization of Frontal Lobe Language Processes and Lateralization of the Posterior Visual Word Processing System , 2008, Journal of Cognitive Neuroscience.

[27]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[28]  Karl J. Friston,et al.  Analysis of functional MRI time‐series , 1994, Human Brain Mapping.

[29]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[30]  G Jobard,et al.  Evaluation of the dual route theory of reading: a metanalysis of 35 neuroimaging studies , 2003, NeuroImage.

[31]  Joseph T. Devlin,et al.  Investigating Occipito-temporal Contributions to Reading with TMS , 2010, Journal of Cognitive Neuroscience.

[32]  Marc Brysbaert,et al.  The left ventral occipito-temporal response to words depends on language lateralization but not on visual familiarity. , 2010, Cerebral cortex.

[33]  Robert Lindenberg,et al.  “Broca’s area” as a collective term? , 2007, Brain and Language.

[34]  F Crivello,et al.  Interindividual variability in the hemispheric organization for speech , 2004, NeuroImage.

[35]  M Deppe,et al.  Successive activation of both cerebral hemispheres during cued word generation , 1996, Neuroreport.

[36]  S Lehéricy,et al.  The visual word form area: spatial and temporal characterization of an initial stage of reading in normal subjects and posterior split-brain patients. , 2000, Brain : a journal of neurology.

[37]  Ferath Kherif,et al.  r Human Brain Mapping 32:1602–1614 (2011) r Regional and Hemispheric Determinants of Language Laterality: Implications for Preoperative fMRI , 2022 .

[38]  Kewei Chen,et al.  Cerebral asymmetry in children when reading Chinese characters. , 2005, Brain research. Cognitive brain research.

[39]  Karl J. Friston,et al.  Dynamic causal modeling , 2010, Scholarpedia.

[40]  M. Sigman,et al.  Opinion TRENDS in Cognitive Sciences Vol.9 No.7 July 2005 The neural code for written words: a proposal , 2022 .

[41]  S. Dehaene,et al.  Functional Neuroimaging of Speech Perception in Infants , 2002, Science.

[42]  S. Kuriki,et al.  Dissociated expressive and receptive language functions on magnetoencephalography, functional magnetic resonance imaging, and amobarbital studies. Case report and review of the literature. , 2006, Journal of neurosurgery.

[43]  Zoë R. Hunter,et al.  Visual half-field experiments are a good measure of cerebral language dominance if used properly: Evidence from fMRI , 2008, Neuropsychologia.

[44]  I. Mcmanus,et al.  Handedness , language dominance and aphasia : a genetic model , 2001 .

[45]  J. M. Watson,et al.  Functional MRI reveals an interhemispheric dissociation of frontal and temporal language regions in a patient with focal epilepsy , 2003, Epilepsy & Behavior.

[46]  Bruce D. McCandliss,et al.  The visual word form area: expertise for reading in the fusiform gyrus , 2003, Trends in Cognitive Sciences.

[47]  Anthony B. Waites,et al.  fMRI assessment of language lateralization: An objective approach , 2010, NeuroImage.

[48]  J B Poline,et al.  Letter Binding and Invariant Recognition of Masked Words , 2004, Psychological science.

[49]  Marko Wilke,et al.  LI-tool: A new toolbox to assess lateralization in functional MR-data , 2007, Journal of Neuroscience Methods.

[50]  C. Price,et al.  The Interactive Account of ventral occipitotemporal contributions to reading , 2011, Trends in Cognitive Sciences.

[51]  S. Kosslyn Seeing and imagining in the cerebral hemispheres: a computational approach. , 1987, Psychological review.

[52]  Marc Brysbaert,et al.  Split fovea theory and the role of the two cerebral hemispheres in reading: A review of the evidence , 2010, Neuropsychologia.

[53]  C. Walsh,et al.  Molecular approaches to brain asymmetry and handedness , 2006, Nature Reviews Neuroscience.

[54]  Isabelle S. Häberling,et al.  Cerebral Asymmetries: Complementary and Independent Processes , 2010, PloS one.

[55]  Michael S C Thomas,et al.  Multiple Routes from Occipital to Temporal Cortices during Reading , 2011, The Journal of Neuroscience.

[56]  Interhemispheric dissociation of language regions in a healthy subject. , 2006, Archives of neurology.