Beyond Hemispheric Dominance: Brain Regions Underlying the Joint Lateralization of Language and Arithmetic to the Left Hemisphere

Language and arithmetic are both lateralized to the left hemisphere in the majority of right-handed adults. Yet, does this similar lateralization reflect a single overall constraint of brain organization, such an overall “dominance” of the left hemisphere for all linguistic and symbolic operations? Is it related to the lateralization of specific cerebral subregions? Or is it merely coincidental? To shed light on this issue, we performed a “colateralization analysis” over 209 healthy subjects: We investigated whether normal variations in the degree of left hemispheric asymmetry in areas involved in sentence listening and reading are mirrored in the asymmetry of areas involved in mental arithmetic. Within the language network, a region-of-interest analysis disclosed partially dissociated patterns of lateralization, inconsistent with an overall “dominance” model. Only two of these areas presented a lateralization during sentence listening and reading which correlated strongly with the lateralization of two regions active during calculation. Specifically, the profile of asymmetry in the posterior superior temporal sulcus during sentence processing covaried with the asymmetry of calculation-induced activation in the intraparietal sulcus, and a similar colateralization linked the middle frontal gyrus with the superior posterior parietal lobule. Given recent neuroimaging results suggesting a late emergence of hemispheric asymmetries for symbolic arithmetic during childhood, we speculate that these colateralizations might constitute developmental traces of how the acquisition of linguistic symbols affects the cerebral organization of the arithmetic network.

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

[2]  F. Gilles,et al.  Left-right asymmetries of the temporal speech areas of the human fetus. , 1977, Archives of neurology.

[3]  Elizabeth K. Warrington,et al.  Arithmetic Skills in Patients with Unilateral Cerebral Lesions , 1986, Cortex.

[4]  D. Pandya,et al.  Association fiber pathways to the frontal cortex from the superior temporal region in the rhesus monkey , 1988, The Journal of comparative neurology.

[5]  C. B. Cave,et al.  Evidence for two types of spatial representations: hemispheric specialization for categorical and coordinate relations. , 1989, Journal of experimental psychology. Human perception and performance.

[6]  B. MacWhinney,et al.  Language Development , 2015 .

[7]  Karen Wynn,et al.  Addition and subtraction by human infants , 1992, Nature.

[8]  F Lucchelli,et al.  Primary dyscalculia after a medial frontal lesion of the left hemisphere. , 1993, Journal of neurology, neurosurgery, and psychiatry.

[9]  A. Damasio,et al.  Cortical systems for retrieval of concrete knowledge: The convergence zone framework , 1994 .

[10]  Joel L. Davis,et al.  Large-Scale Neuronal Theories of the Brain , 1994 .

[11]  L. Katz,et al.  Sex differences in the functional organization of the brain for language , 1995, Nature.

[12]  Richard S. J. Frackowiak,et al.  Functional anatomy of a common semantic system for words and pictures , 1996, Nature.

[13]  Jeffrey Bisanz,et al.  Selection of Procedures in Mental Addition: Reassessing the Problem Size Effect in Adults , 1996 .

[14]  Helen J. Neville,et al.  Language comprehension and cerebral specialization from 13 to 20 months , 1997 .

[15]  S. Carey,et al.  Knowledge of Number: Its Evolution and Ontogeny , 1998, Science.

[16]  M. Posner,et al.  Brain mechanisms of quantity are similar in 5-year-old children and adults. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[17]  M. Petrides,et al.  Functional organization of spatial and nonspatial working memory processing within the human lateral frontal cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[18]  J. Pujol,et al.  Cerebral lateralization of language in normal left-handed people studied by functional MRI , 1999, Neurology.

[19]  S. Dehaene,et al.  Differential Contributions of the Left and Right Inferior Parietal Lobules to Number Processing , 1999, Journal of Cognitive Neuroscience.

[20]  D. Kimura Sex and cognition , 1999 .

[21]  V Menon,et al.  Functional optimization of arithmetic processing in perfect performers. , 2000, Brain research. Cognitive brain research.

[22]  S. Dehaene,et al.  Understanding dissociations in dyscalculia: a brain imaging study of the impact of number size on the cerebral networks for exact and approximate calculation. , 2000, Brain : a journal of neurology.

[23]  D. Poeppel,et al.  Towards a functional neuroanatomy of speech perception , 2000, Trends in Cognitive Sciences.

[24]  S. Dehaene,et al.  Language and calculation within the parietal lobe: a combined cognitive, anatomical and fMRI study , 2000, Neuropsychologia.

[25]  E. T. Possing,et al.  Human temporal lobe activation by speech and nonspeech sounds. , 2000, Cerebral cortex.

[26]  Elizabeth Bates,et al.  LANGUAGE DEVELOPMENT IN CHILDREN WITH UNILATERAL BRAIN INJURY , 2000 .

[27]  D. LeBihan,et al.  Modulation of Parietal Activation by Semantic Distance in a Number Comparison Task , 2001, NeuroImage.

[28]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[29]  Marinella Cappelletti,et al.  Spared numerical abilities in a case of semantic dementia , 2001, Neuropsychologia.

[30]  C. Nelson,et al.  Handbook of Developmental Cognitive Neuroscience , 2001 .

[31]  Elizabeth S Spelke,et al.  Language and number: a bilingual training study , 2001, Cognition.

[32]  S. Dehaene,et al.  Topographical Layout of Hand, Eye, Calculation, and Language-Related Areas in the Human Parietal Lobe , 2002, Neuron.

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

[34]  Avishai Henik,et al.  The development of internal representations of magnitude and their association with Arabic numerals. , 2002, Journal of experimental child psychology.

[35]  A. Toga,et al.  Mapping brain asymmetry , 2003, Nature Reviews Neuroscience.

[36]  M. Corbetta,et al.  Functional Organization of Human Intraparietal and Frontal Cortex for Attending, Looking, and Pointing , 2003, The Journal of Neuroscience.

[37]  M. Delazer,et al.  Learning complex arithmetic--an fMRI study. , 2003, Brain research. Cognitive brain research.

[38]  M. Tervaniemi,et al.  Lateralization of auditory-cortex functions , 2003, Brain Research Reviews.

[39]  A. Kleinschmidt,et al.  A Supramodal Number Representation in Human Intraparietal Cortex , 2003, Neuron.

[40]  J. Mehler,et al.  Sounds and silence: An optical topography study of language recognition at birth , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[41]  Caroline Prunier,et al.  Presymptomatic diagnosis of experimental Parkinsonism with 123I-PE2I SPECT , 2003, NeuroImage.

[42]  S. Dehaene,et al.  THREE PARIETAL CIRCUITS FOR NUMBER PROCESSING , 2003, Cognitive neuropsychology.

[43]  Stanislas Dehaene,et al.  Distinct unimodal and multimodal regions for word processing in the left temporal cortex , 2004, NeuroImage.

[44]  Mary K. Hoard,et al.  Strategy choices in simple and complex addition: Contributions of working memory and counting knowledge for children with mathematical disability. , 2004, Journal of experimental child psychology.

[45]  P. Gordon Numerical Cognition Without Words: Evidence from Amazonia , 2004, Science.

[46]  Philippe Pinel,et al.  Distributed and Overlapping Cerebral Representations of Number, Size, and Luminance during Comparative Judgments , 2004, Neuron.

[47]  Philippe Pinel,et al.  Tuning Curves for Approximate Numerosity in the Human Intraparietal Sulcus , 2004, Neuron.

[48]  S. Dehaene,et al.  Exact and Approximate Arithmetic in an Amazonian Indigene Group , 2004, Science.

[49]  Working memory as a predictor of addition skills and addition strategies in children , 2004 .

[50]  André Aleman,et al.  Do women really have more bilateral language representation than men? A meta-analysis of functional imaging studies. , 2004, Brain : a journal of neurology.

[51]  Wim Fias,et al.  Representation of Number in Animals and Humans: A Neural Model , 2004, Journal of Cognitive Neuroscience.

[52]  A. Alexander,et al.  Diffusion tensor imaging of cerebral white matter: a pictorial review of physics, fiber tract anatomy, and tumor imaging patterns. , 2004, AJNR. American journal of neuroradiology.

[53]  Jean-Francois Mangin,et al.  Automatized clustering and functional geometry of human parietofrontal networks for language, space, and number , 2004, NeuroImage.

[54]  Stanislas Dehaene,et al.  Specialization within the ventral stream: the case for the visual word form area , 2004, NeuroImage.

[55]  K. Wynn,et al.  Large-Number Addition and Subtraction by 9-Month-Old Infants , 2004, Psychological science.

[56]  B. Argall,et al.  Unraveling multisensory integration: patchy organization within human STS multisensory cortex , 2004, Nature Neuroscience.

[57]  Julie L. Booth,et al.  Development of numerical estimation in young children. , 2004, Child development.

[58]  Michael Siegal,et al.  Agrammatic but numerate. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[59]  Karl J. Friston,et al.  Dissociating Reading Processes on the Basis of Neuronal Interactions , 2005, Journal of Cognitive Neuroscience.

[60]  B. Butterworth The development of arithmetical abilities. , 2005, Journal of child psychology and psychiatry, and allied disciplines.

[61]  S. Dehaene,et al.  Interactions between number and space in parietal cortex , 2005, Nature Reviews Neuroscience.

[62]  Chad J. Marsolek,et al.  Does a causal relation exist between the functional hemispheric asymmetries of visual processing subsystems? , 2005, Brain and Cognition.

[63]  G. Vallortigara,et al.  survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization , 2005, Behavioral and Brain Sciences.

[64]  V Menon,et al.  Cerebral Cortex doi:10.1093/cercor/bhi055 Developmental Changes in Mental Arithmetic: Evidence for Increased Functional Specialization in the Left Inferior Parietal Cortex , 2005 .

[65]  Hilary Barth,et al.  Abstract number and arithmetic in preschool children. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[66]  Derek K. Jones,et al.  Perisylvian language networks of the human brain , 2005, Annals of neurology.

[67]  Michael W. L. Chee,et al.  Neural correlates of symbolic and non-symbolic arithmetic , 2005, Neuropsychologia.

[68]  C. Semenza,et al.  Is math lateralised on the same side as language? Right hemisphere aphasia and mathematical abilities , 2006, Neuroscience Letters.

[69]  T. Klingberg Development of a superior frontal–intraparietal network for visuo-spatial working memory , 2006, Neuropsychologia.

[70]  Michael W. L. Chee,et al.  Effect of Language Switching on Arithmetic: A Bilingual fMRI Study , 2006, Journal of Cognitive Neuroscience.

[71]  L.M. Balsamo,et al.  Language lateralization and the role of the fusiform gyrus in semantic processing in young children , 2006, NeuroImage.

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

[73]  Brian Butterworth,et al.  Exact and Approximate Judgements of Visual and Auditory Numerosity: an Fmri Study , 2006 .

[74]  Andreas Nieder,et al.  Temporal and Spatial Enumeration Processes in the Primate Parietal Cortex , 2006, Science.

[75]  M. Eckert,et al.  Exploiting human anatomical variability as a link between genome and cognome , 2006, Genes, brain, and behavior.

[76]  Yumiko Yamazaki,et al.  The study of hemispheric specialization for categorical and coordinate spatial relations in animals , 2006, Neuropsychologia.

[77]  E. Donnemiller,et al.  Knowing 7×8, but not the meaning of ‘elephant’: Evidence for the dissociation between numerical and non-numerical semantic knowledge , 2006, Neuropsychologia.

[78]  Christopher A Walsh,et al.  Genomic and evolutionary analyses of asymmetrically expressed genes in human fetal left and right cerebral cortex. , 2006, Cerebral cortex.

[79]  Daniel Ansari,et al.  Age-related Changes in the Activation of the Intraparietal Sulcus during Nonsymbolic Magnitude Processing: An Event-related Functional Magnetic Resonance Imaging Study , 2006, Journal of Cognitive Neuroscience.

[80]  D. Geschwind,et al.  Genome-wide analyses of human perisylvian cerebral cortical patterning , 2007, Proceedings of the National Academy of Sciences.

[81]  D. Pandya,et al.  Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. , 2007, Brain : a journal of neurology.

[82]  S. Dehaene,et al.  A Magnitude Code Common to Numerosities and Number Symbols in Human Intraparietal Cortex , 2007, Neuron.

[83]  B. Thirion,et al.  Fast reproducible identification and large-scale databasing of individual functional cognitive networks , 2007, BMC Neuroscience.

[84]  Marc Brysbaert,et al.  Foveal Word Reading Requires Interhemispheric Communication , 2007, Journal of Cognitive Neuroscience.

[85]  P. Dupont,et al.  Word reading and posterior temporal dysfunction in amnestic mild cognitive impairment. , 2006, Cerebral cortex.

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

[87]  S. Dehaene Symbols and quantities in parietal cortex: elements of a mathematical theory of number representation and manipulation , 2007 .

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

[89]  Stanislas Dehaene,et al.  Distinct Cerebral Pathways for Object Identity and Number in Human Infants , 2008, PLoS biology.

[90]  F. Lazeyras,et al.  Mapping the early cortical folding process in the preterm newborn brain. , 2008, Cerebral cortex.

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

[92]  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.

[93]  Melissa E. Libertus,et al.  Comment on "Log or Linear? Distinct Intuitions of the Number Scale in Western and Amazonian Indigene Cultures" , 2009, Science.

[94]  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.

[95]  Michael Andres,et al.  Role of distinct parietal areas in arithmetic: An fMRI-guided TMS study , 2011, NeuroImage.

[96]  S. Dehaene,et al.  The unique role of the visual word form area in reading , 2011, Trends in Cognitive Sciences.

[97]  C. Semenza,et al.  Good division, but bad addition, subtraction and multiplication. A “leftmost-first” bug? , 2011, Cortex.

[98]  Brian Butterworth,et al.  Neural basis of mathematical cognition , 2011, Current Biology.

[99]  Marc Brysbaert,et al.  Colateralization of Broca’s area and the visual word form area in left-handers: fMRI evidence , 2012, Brain and Language.