Right hand, left brain: genetic and evolutionary bases of cerebral asymmetries for language and manual action.

Most people are right-handed and left-cerebrally dominant for language. This pattern of asymmetry, as well as departures from it, have been reasonably accommodated in terms of a postulated gene with two alleles, one disposing to this common pattern and the other leaving the direction of handedness and language asymmetry to chance. There are some leads as to the location of the gene or genes concerned, but no clear resolution; one possibility is that the chance factor is achieved by epigenetic cancelling of the lateralizing gene rather than through a chance allele. Neurological evidence suggests that the neural basis of manual praxis, including pantomime and tool use, is more closely associated with cerebral asymmetry for language than with handedness, and is homologous with the so-called "mirror system" in the primate brain, which is specialized for manual grasping. The evidence reviewed supports the theory that language itself evolved within the praxic system, and became lateralized in humans, and perhaps to a lesser extent in our common ancestry with the great apes. WIREs Cogn Sci 2012, 3:1-17. doi: 10.1002/wcs.158 For further resources related to this article, please visit the WIREs website.

[1]  A. Klar A single locus, RGHT, specifies preference for hand utilization in humans. , 1996, Cold Spring Harbor symposia on quantitative biology.

[2]  S. Arver,et al.  Deficits in inhibitory executive functions in Klinefelter (47, XXY) syndrome , 2011, Psychiatry Research.

[3]  Michael C. Corballis,et al.  FOXP2 and the mirror system , 2004, Trends in Cognitive Sciences.

[4]  Michael S. Gazzaniga,et al.  A Dissociation between the Representation of Tool-use Skills and Hand Dominance: Insights from Left- and Right-handed Callosotomy Patients , 2005, Journal of Cognitive Neuroscience.

[5]  M. Corballis The gestural origins of language. , 2010, Wiley interdisciplinary reviews. Cognitive science.

[6]  C. Deng,et al.  Silencing of unsynapsed meiotic chromosomes in the mouse , 2005, Nature Genetics.

[7]  G Rizzolatti,et al.  When pliers become fingers in the monkey motor system , 2008, Proceedings of the National Academy of Sciences.

[8]  J A Wada,et al.  Cerebral hemispheric asymmetry in humans. Cortical speech zones in 100 adults and 100 infant brains. , 1975, Archives of neurology.

[9]  A. R. Palmer Symmetry Breaking and the Evolution of Development , 2004, Science.

[10]  A. Klar An epigenetic hypothesis for human brain laterality, handedness, and psychosis development. , 2004, Cold Spring Harbor symposia on quantitative biology.

[11]  D. Bishop,et al.  Hemispheric division of function is the result of independent probabilistic biases , 2009, Neuropsychologia.

[12]  C. Boesch Handedness in wild chimpanzees , 1991, International Journal of Primatology.

[13]  J. Vauclair,et al.  Captive chimpanzees use their right hand to communicate with each other: Implications for the origin of the cerebral substrate for language , 2010, Cortex.

[14]  C. Francks,et al.  Parent-of-origin effects on handedness and schizophrenia susceptibility on chromosome 2p12-q11. , 2003, Human molecular genetics.

[15]  S. Ghirlanda,et al.  The evolution of brain lateralization: a game-theoretical analysis of population structure , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[16]  D. Geschwind,et al.  High-throughput analysis of promoter occupancy reveals direct neural targets of FOXP2, a gene mutated in speech and language disorders. , 2007, American journal of human genetics.

[17]  S G Kim,et al.  Functional activation in motor cortex reflects the direction and the degree of handedness. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[18]  B Milner,et al.  THE ROLE OF EARLY LEFT‐BRAIN INJURY IN DETERMINING LATERALIZATION OF CEREBRAL SPEECH FUNCTIONS , 1977, Annals of the New York Academy of Sciences.

[19]  J. Gurd,et al.  Crossed cerebral lateralization for verbal and visuo‐spatial function in a pair of handedness discordant monozygotic twins: MRI and fMRI brain imaging , 2008, Journal of anatomy.

[20]  Michael A. Arbib,et al.  The syntactic motor system , 2005 .

[21]  Jorge Sepulcre,et al.  Evidence from intrinsic activity that asymmetry of the human brain is controlled by multiple factors , 2009, Proceedings of the National Academy of Sciences.

[22]  T. Crow,et al.  Location of the handedness gene on the X and Y chromosomes , 1996, Schizophrenia Research.

[23]  T. Crow,et al.  Relative hand skill predicts academic ability: global deficits at the point of hemispheric indecision , 1998, Neuropsychologia.

[24]  P. Hepper,et al.  Lateralised behaviour in first trimester human foetuses , 1998, Neuropsychologia.

[25]  R. Kahn,et al.  Language lateralization in monozygotic twin pairs concordant and discordant for handedness. , 2002, Brain : a journal of neurology.

[26]  U. Castiello,et al.  Cortical Activations in Humans Grasp-Related Areas Depend on Hand Used and Handedness , 2008, PloS one.

[27]  M. Nicholls,et al.  Nature’s experiment? Handedness and early childhood development , 2009, Demography.

[28]  M. Corballis Language as gesture. , 2009, Human movement science.

[29]  A. Schleicher,et al.  Asymmetry in the Human Motor Cortex and Handedness , 1996, NeuroImage.

[30]  W. McGrew,et al.  Etho-Archaeology of Manual Laterality: Well Digging by Wild Chimpanzees , 2007, Folia Primatologica.

[31]  F. Vargha-Khadem,et al.  Behavioural analysis of an inherited speech and language disorder: comparison with acquired aphasia. , 2002, Brain : a journal of neurology.

[32]  T. Crow,et al.  A theory of the origin of cerebral asymmetry: Epigenetic variation superimposed on a fixed right-shift , 2010, Laterality.

[33]  D. Loring,et al.  The occurrence of depressive symptoms in the preclinical phase of AD , 1999, Neurology.

[34]  T. Insel,et al.  Differential expansion of neural projection systems in primate brain evolution. , 1999, Neuroreport.

[35]  A. Monaco,et al.  Recent advances in the genetics of language impairment , 2010, Genome Medicine.

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

[37]  S. F. Witelson Hand and sex differences in the isthmus and genu of the human corpus callosum. A postmortem morphological study. , 1989, Brain : a journal of neurology.

[38]  A. Monaco,et al.  Molecular evolution of FOXP2, a gene involved in speech and language , 2002, Nature.

[39]  H. Lausberg,et al.  Callosal disconnection syndrome in a left-handed patient due to infarction of the total length of the corpus callosum , 1999, Neuropsychologia.

[40]  Philip L. F. Johnson,et al.  A Draft Sequence of the Neandertal Genome , 2010, Science.

[41]  R. Plomin,et al.  Allelic skewing of DNA methylation is widespread across the genome. , 2010, American journal of human genetics.

[42]  S Coren,et al.  Fifty centuries of right-handedness: the historical record. , 1977, Science.

[43]  J. Thome,et al.  Digit ratio (2D:4D), salivary testosterone, and handedness , 2011, Laterality.

[44]  W. Hopkins,et al.  Asymmetric Broca's area in great apes , 2001, Nature.

[45]  Isabelle S. Häberling,et al.  Cerebral asymmetries in monozygotic twins: An fMRI study , 2010, Neuropsychologia.

[46]  K. Hugdahl,et al.  Left-handedness and old age: Do left-handers die earlier? , 1993, Neuropsychologia.

[47]  A. Morris,et al.  PCSK6 is associated with handedness in individuals with dyslexia , 2010, Human molecular genetics.

[48]  V. van de Ven,et al.  Reduced Laterality as a Trait Marker ofSchizophrenia—Evidence from Structural and Functional Neuroimaging , 2010, The Journal of Neuroscience.

[49]  Stian Reimers,et al.  Hand preference for writing and associations with selected demographic and behavioral variables in 255,100 subjects: The BBC internet study , 2006, Brain and Cognition.

[50]  Gregory Króliczak,et al.  A common network in the left cerebral hemisphere represents planning of tool use pantomimes and familiar intransitive gestures at the hand-independent level. , 2009, Cerebral cortex.

[51]  Leonardo Fogassi,et al.  Mirror systems. , 2011, Wiley interdisciplinary reviews. Cognitive science.

[52]  Jamie L. Russell,et al.  Factors influencing the prevalence and handedness for throwing in captive chimpanzees (Pan troglodytes). , 2005, Journal of comparative psychology.

[53]  G. Geffen,et al.  Genetic influences on handedness: Data from 25,732 Australian and Dutch twin families , 2009, Neuropsychologia.

[54]  D. Constam,et al.  Extraembryonic proteases regulate Nodal signalling during gastrulation , 2002, Nature Cell Biology.

[55]  Kenneth Hugdahl,et al.  The two halves of the brain : information processing in the cerebral hemispheres , 2010 .

[56]  A. Braun,et al.  Asymmetry of chimpanzee planum temporale: humanlike pattern of Wernicke's brain language area homolog. , 1998, Science.

[57]  Susan Goldin-Meadow,et al.  Gesturing Saves Cognitive Resources When Talking About Nonpresent Objects , 2010, Cogn. Sci..

[58]  G Schlaug,et al.  Brain (A) symmetry in monozygotic twins. , 1995, Cerebral cortex.

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

[60]  A. Braun,et al.  Activation of Broca’s area during the production of spoken and signed language: a combined cytoarchitectonic mapping and PET analysis , 2003, Neuropsychologia.

[61]  R. Passingham,et al.  Oral Dyspraxia in Inherited Speech and Language Impairment and Acquired Dysphasia , 2000, Brain and Language.

[62]  F. Nottebohm,et al.  Primate Communication and the Gestural Origin of Language [and Comments and Reply] , 1973, Current Anthropology.

[63]  Michael C. Corballis,et al.  Callosal tracts and patterns of hemispheric dominance: A combined fMRI and DTI study , 2011, NeuroImage.

[64]  E. Warrington,et al.  Language laterality in left-handers assessed by unilateral E.C.T. , 1973, Neuropsychologia.

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

[66]  Y. Huang,et al.  Sex but no hand difference in the isthmus of the corpus callosum , 1992, Neurology.

[67]  H. Mitchison,et al.  Handedness and situs inversus in primary ciliary dyskinesia , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[68]  K. Hugdahl,et al.  What is left is right: How speech asymmetry shaped the brain. , 2009 .

[69]  R. Williamson,et al.  Parametric and non-parametric linkage analysis of several candidate regions for genes for human handedness , 2002, European Journal of Human Genetics.

[70]  Charles H. Goldsmith,et al.  The relationship of hand preference to anatomy of the corpus callosum in men , 1991, Brain Research.

[71]  J. McGough,et al.  Mixed-Handedness Is Linked to Mental Health Problems in Children and Adolescents , 2010, Pediatrics.

[72]  A. P. Georgopoulos,et al.  Functional magnetic resonance imaging of motor cortex: hemispheric asymmetry and handedness. , 1993, Science.

[73]  Timothy J. Crow,et al.  Directional asymmetry is the key to the origin of modern Homo sapiens (the Broca‐Annett axiom): A reply to Rogers' review of The Speciation of Modern Homo Sapiens , 2004 .

[74]  W F McKeever,et al.  A new family handedness sample with findings consistent with X-linked transmission. , 2000, British journal of psychology.

[75]  M. Corballis The genetics and evolution of handedness. , 1997, Psychological review.

[76]  W. Hopkins,et al.  Wild chimpanzees show population-level handedness for tool use. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[77]  P. Hof,et al.  Wernicke's area homologue in chimpanzees (Pan troglodytes) and its relation to the appearance of modern human language , 2010, Proceedings of the Royal Society B: Biological Sciences.

[78]  Kenneth Hugdahl,et al.  Hemispheric asymmetry: contributions from brain imaging. , 2011, Wiley interdisciplinary reviews. Cognitive science.

[79]  E. Zaidel,et al.  Anatomical-behavioral relationships: Corpus callosum morphometry and hemispheric specialization , 1994, Behavioural Brain Research.

[80]  M. Gazzaniga Cerebral specialization and interhemispheric communication: does the corpus callosum enable the human condition? , 2000, Brain : a journal of neurology.

[81]  J. Régis,et al.  Effects of handedness and sex on the morphology of the corpus callosum: A study with brain magnetic resonance imaging , 1991, Brain and Cognition.

[82]  J. Finnerty,et al.  Origins of Bilateral Symmetry: Hox and Dpp Expression in a Sea Anemone , 2004, Science.

[83]  F. Kennedy STOCK‐BRAINEDNESS, THE CAUSATIVE FACTOR IN THE SO‐CALLED “CROSSED APHASIAS.” , 1916 .

[84]  Susan Goldin-Meadow,et al.  Gesture Paves the Way for Language Development , 2005, Psychological science.

[85]  K. Heilman,et al.  Apraxic agraphia with neglect-induced paragraphia. , 1979, Archives of neurology.

[86]  M. Mishkin,et al.  Language fMRI abnormalities associated with FOXP2 gene mutation , 2003, Nature Neuroscience.

[87]  Sergiu Groppa,et al.  Manual activity shapes structure and function in contralateral human motor hand area , 2011, NeuroImage.

[88]  M. Arbib From monkey-like action recognition to human language: An evolutionary framework for neurolinguistics , 2005, Behavioral and Brain Sciences.

[89]  H. Burbano,et al.  The Derived FOXP2 Variant of Modern Humans Was Shared with Neandertals , 2007, Current Biology.

[90]  T. Matsuzawa,et al.  Laterality in hand use across four tool‐use behaviors among the wild chimpanzees of Bossou, Guinea, West Africa , 2009, American journal of primatology.

[91]  G. Hammond,et al.  Correlates of human handedness in primary motor cortex: a review and hypothesis , 2002, Neuroscience & Biobehavioral Reviews.

[92]  G. Rizzolatti,et al.  The functional role of the parieto-frontal mirror circuit: interpretations and misinterpretations , 2010, Nature Reviews Neuroscience.

[93]  W. Hopkins Chimpanzee handedness revisited: 55 years since Finch (1941) , 1996, Psychonomic bulletin & review.

[94]  M. Levin Left-right asymmetry and the chick embryo. , 1998, Seminars in cell & developmental biology.

[95]  Marcus R Munafò,et al.  Sex differences in left-handedness: a meta-analysis of 144 studies. , 2008, Psychological bulletin.

[96]  William D. Hopkins,et al.  Planum temporale surface area and grey matter asymmetries in chimpanzees (Pan troglodytes): The effect of handedness and comparison with findings in humans , 2010, Behavioural Brain Research.

[97]  T. Nagylaki,et al.  A model for the genetics of handedness. , 1972, Genetics.

[98]  Noam Chomsky,et al.  The faculty of language: what is it, who has it, and how did it evolve? , 2002, Science.

[99]  J. Mazziotta,et al.  Handedness in twins: a meta-analysis. , 1999, Laterality.

[100]  W. M. Layton Random determination of a developmental process: reversal of normal visceral asymmetry in the mouse. , 1976, The Journal of heredity.

[101]  M. Mishkin,et al.  FOXP2 and the neuroanatomy of speech and language , 2005, Nature Reviews Neuroscience.

[102]  G. Coop,et al.  The Timing of Selection at the Human FOXP2 Gene , 2008, Molecular biology and evolution.

[103]  K. Heilman,et al.  Crossed Apraxia: Implications for Handedness * * Portions of this paper were presented at meetings of the Society for Neuroscience, Washington, D.C., November, 1996, and the International Neuropsychological Society, Orlando, FL, February, 1997. , 1999, Cortex.

[104]  Jaakko Kaprio,et al.  Origins of handedness: A nationwide study of 30161 adults , 2009, Neuropsychologia.

[105]  Patrice Y. Simard,et al.  Time is of the essence: a conjecture that hemispheric specialization arises from interhemispheric conduction delay. , 1994, Cerebral cortex.

[106]  Peter G. Hepper,et al.  Handedness in the human fetus , 1991, Neuropsychologia.

[107]  G. Vallortigara,et al.  Brain asymmetry (animal). , 2011, Wiley interdisciplinary reviews. Cognitive science.

[108]  M. P. Bryden,et al.  Patterns of cerebral organization , 1983, Brain and Language.

[109]  Lutz Jäncke,et al.  Anatomical left‐right asymmetry of language‐related temporal cortex is different in left‐ and right‐handers , 1991, Annals of neurology.

[110]  William D Hopkins,et al.  Neuroanatomical Correlates of Handedness for Tool Use in Chimpanzees (Pan Troglodytes) , 2007, Psychological science.

[111]  Scott H. Frey,et al.  Human Anterior Intraparietal and Ventral Premotor Cortices Support Representations of Grasping with the Hand or a Novel Tool , 2010, Journal of Cognitive Neuroscience.

[112]  Adrian Bird,et al.  Perceptions of epigenetics , 2007, Nature.

[113]  Dora Biro,et al.  Ontogeny and Cultural Propagation of Tool Use by Wild Chimpanzees at Bossou, Guinea: Case Studies in Nut Cracking and Leaf Folding , 2006 .

[114]  C. Kennard,et al.  The anatomy of visual neglect , 2003 .

[115]  Cerebral Asymmetry: a Question of Balance , 2006, Cortex.

[116]  D. Geschwind,et al.  LRRTM1 on chromosome 2p12 is a maternally suppressed gene that is associated paternally with handedness and schizophrenia , 2007, Molecular Psychiatry.

[117]  S. Frey Tool use, communicative gesture and cerebral asymmetries in the modern human brain , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[118]  René Westerhausen,et al.  Effects of handedness and gender on macro- and microstructure of the corpus callosum and its subregions: a combined high-resolution and diffusion-tensor MRI study. , 2004, Brain research. Cognitive brain research.

[119]  Joseph A Maldjian,et al.  Diffusion anisotropy in the corpus callosum. , 2002, AJNR. American journal of neuroradiology.

[120]  M. Annett Cerebral asymmetry in twins: predictions of the right shift theory , 2003, Neuropsychologia.

[121]  J. Torgersen Situs inversus, asymmetry, and twinning. , 1950, American journal of human genetics.

[122]  A. Braun,et al.  Symbolic gestures and spoken language are processed by a common neural system , 2009, Proceedings of the National Academy of Sciences.

[123]  U. Waldenström,et al.  Fetal origins of child non-right-handedness and mental health. , 2008, Journal of child psychology and psychiatry, and allied disciplines.

[124]  Richard B. Fletcher,et al.  Handedness and intellectual achievement: An even-handed look , 2008, Neuropsychologia.

[125]  T. Crow Genetic hypotheses for schizophrenia. , 2007, The British journal of psychiatry : the journal of mental science.

[126]  H. Möller,et al.  Handedness and corpus callosum morphology , 2002, Psychiatry Research: Neuroimaging.