1932

Abstract

Although the left and right hemispheres of our brains develop with a high degree of symmetry at both the anatomical and functional levels, it has become clear that subtle structural differences exist between the two sides and that each is dominant in processing specific cognitive tasks. As the result of evolutionary conservation or convergence, lateralization of the brain is found in both vertebrates and invertebrates, suggesting that it provides significant fitness for animal life. This widespread feature of hemispheric specialization has allowed the emergence of model systems to study its development and, in some cases, to link anatomical asymmetries to brain function and behavior. Here, we present some of what is known about brain asymmetry in humans and model organisms as well as what is known about the impact of environmental and genetic factors on brain asymmetry development. We specifically highlight the progress made in understanding the development of epithalamic asymmetries in zebrafish and how this model provides an exciting opportunity to address brain asymmetry at different levels of complexity.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-genet-112414-055322
2015-11-23
2024-06-25
Loading full text...

Full text loading...

/deliver/fulltext/genet/49/1/annurev-genet-112414-055322.html?itemId=/content/journals/10.1146/annurev-genet-112414-055322&mimeType=html&fmt=ahah

Literature Cited

  1. Agetsuma M, Aizawa H, Aoki T, Nakayama R, Takahoko M. 1.  et al. 2010. The habenula is crucial for experience-dependent modification of fear responses in zebrafish. Nat. Neurosci. 13:1354–56 [Google Scholar]
  2. Aizawa H, Bianco IH, Hamaoka T, Miyashita T, Uemura O. 2.  et al. 2005. Laterotopic representation of left-right information onto the dorso-ventral axis of a zebrafish midbrain target nucleus. Curr. Biol. 15:238–43 [Google Scholar]
  3. Aizawa H, Goto M, Sato T, Okamoto H. 3.  2007. Temporally regulated asymmetric neurogenesis causes left-right difference in the zebrafish habenular structures. Dev. Cell 12:87–98 [Google Scholar]
  4. Amo R, Aizawa H, Takahoko M, Kobayashi M, Takahashi R. 4.  et al. 2010. Identification of the zebrafish ventral habenula as a homolog of the mammalian lateral habenula. J. Neurosci. 30:1566–74 [Google Scholar]
  5. Anfora G, Frasnelli E, Maccagnani B, Rogers LJ, Vallortigara G. 5.  2010. Behavioural and electrophysiological lateralization in a social (Apis mellifera) but not in a non-social (Osmia cornuta) species of bee. Behav. Brain Res. 206:2236–39 [Google Scholar]
  6. Annett M. 6.  1979. Family handedness in three generations predicted by the right shift theory. Ann. Hum. Genet. 42:4479–91 [Google Scholar]
  7. Badzakova-Trajkov G, Häberling IS, Roberts RP, Corballis MC. 7.  2010. Cerebral asymmetries: complementary and independent processes. PLOS ONE 5:3e9682 [Google Scholar]
  8. Banks SJ, Sziklas V, Sodums DJ, Jones-Gotman M. 8.  2012. fMRI of verbal and nonverbal memory processes in healthy and epileptogenic medial temporal lobes. Epilepsy Behav. 25:142–49 [Google Scholar]
  9. Barnéoud P, le Moal M, Neveu PJ. 9.  1990. Asymmetric distribution of brain monoamines in left- and right-handed mice. Brain Res. 520:1–2317–21 [Google Scholar]
  10. Barnéoud P, der Loos HV. 10.  1993. Direction of handedness linked to hereditary asymmetry of a sensory system. PNAS 90:83246–50 [Google Scholar]
  11. Barth KA, Miklosi A, Watkins J, Bianco IH, Wilson SW, Andrew RJ. 11.  2005. fsi zebrafish show concordant reversal of laterality of viscera, neuroanatomy, and a subset of behavioral responses. Curr. Biol. 15:844–50 [Google Scholar]
  12. Beretta CA, Dross N, Gutierrez-Triana JA, Ryu S, Carl M. 12.  2012. Habenula circuit development: past, present, and future. Neurogenesis 6:51 [Google Scholar]
  13. Bianco IH, Carl M, Russell C, Clarke JD, Wilson SW. 13.  2008. Brain asymmetry is encoded at the level of axon terminal morphology. Neural Dev. 3:9 [Google Scholar]
  14. Bianco IH, Wilson SW. 14.  2009. The habenular nuclei: a conserved asymmetric relay station in the vertebrate brain. Philos. Trans. R. Soc. Lond. B 364:1005–20 [Google Scholar]
  15. Bisazza A, Cantalupo C, Capocchiano M, Vallortigara G. 15.  2000. Population lateralisation and social behaviour: a study with 16 species of fish. Later. Asymmetries Body Brain Cogn. 5:3269–84 [Google Scholar]
  16. Bisazza A, Facchin L, Pignatti R, Vallortigara G. 16.  1998. Lateralization of detour behaviour in poeciliid fish: the effect of species, gender and sexual motivation. Behav. Brain Res. 91:1–2157–64 [Google Scholar]
  17. Bisgrove BW, Essner JJ, Yost HJ. 17.  2000. Multiple pathways in the midline regulate concordant brain, heart and gut left-right asymmetry. Development 127:3567–79 [Google Scholar]
  18. Bisiach E, Luzzatti C. 18.  1978. Unilateral neglect of representational space. Cortex J. Devoted Study Nerv. Syst. Behav. 14:1129–33 [Google Scholar]
  19. Boorman CJ, Shimeld SM. 19.  2002. The evolution of left-right asymmetry in chordates. BioEssays 24:1004–11 [Google Scholar]
  20. Brandler WM, Morris AP, Evans DM, Scerri TS, Kemp JP. 20.  et al. 2013. Common variants in left/right asymmetry genes and pathways are associated with relative hand skill. PLOS Genet. 9:9e1003751 [Google Scholar]
  21. Brandler WM, Paracchini S. 21.  2014. The genetic relationship between handedness and neurodevelopmental disorders. Trends Mol. Med. 20:283–90 [Google Scholar]
  22. Broca P. 22.  1865. Sur le siège de la faculté du langage articulé (“nous parlons avec l'hémisphère gauche”, p384). Bull. Soc. Anthropol. 6:377–93 [Google Scholar]
  23. Budaev S, Andrew RJ. 23.  2009. Patterns of early embryonic light exposure determine behavioural asymmetries in zebrafish: a habenular hypothesis. Behav. Brain Res. 200:191–94 [Google Scholar]
  24. Bulman-Fleming B, Wainwright PE, Collins RL. 24.  1992. The effects of early experience on callosal development and functional lateralization in pigmented BALB/c mice. Behav. Brain Res. 50:1–231–42 [Google Scholar]
  25. Campione M, Steinbeisser H, Schweickert A, Deissler K, van Bebber F. 25.  et al. 1999. The homeobox gene pitx2: mediator of asymmetric left-right signaling in vertebrate heart and gut looping. Development 126:61225–34 [Google Scholar]
  26. Carl M, Bianco IH, Bajoghli B, Aghaallaei N, Czerny T, Wilson SW. 26.  2007. Wnt/axin1/beta-catenin signaling regulates asymmetric nodal activation, elaboration, and concordance of CNS asymmetries. Neuron 55:393–405 [Google Scholar]
  27. Chatterjee M, Guo Q, Weber S, Scholpp S, Li JY. 27.  2014. Pax6 regulates the formation of the habenular nuclei by controlling the temporospatial expression of Shh in the diencephalon in vertebrates. BMC Biol. 12:113 [Google Scholar]
  28. Clanton JA, Hope KD, Gamse JT. 28.  2013. Fgf signaling governs cell fate in the zebrafish pineal complex. Dev. Camb. Engl. 140:2323–32 [Google Scholar]
  29. Cochet H, Byrne RW. 29.  2013. Evolutionary origins of human handedness: evaluating contrasting hypotheses. Anim. Cogn. 16:4531–42 [Google Scholar]
  30. Colombo A, Palma K, Armijo L, Mione M, Signore IA. 30.  et al. 2013. Daam1a mediates asymmetric habenular morphogenesis by regulating dendritic and axonal outgrowth. Development 140:193997–4007 [Google Scholar]
  31. Concha ML, Bianco IH, Wilson SW. 31.  2012. Encoding asymmetry within neural circuits. Nat. Rev. Neurosci. 13:12832–43 [Google Scholar]
  32. Concha ML, Burdine RD, Russell C, Schier AF, Wilson SW. 32.  2000. A nodal signaling pathway regulates the laterality of neuroanatomical asymmetries in the zebrafish forebrain. Neuron 28:399–409 [Google Scholar]
  33. Concha ML, Russell C, Regan JC, Tawk M, Sidi S. 33.  et al. 2003. Local tissue interactions across the dorsal midline of the forebrain establish CNS laterality. Neuron 39:423–38 [Google Scholar]
  34. Concha ML, Signore IA, Colombo A. 34.  2009. Mechanisms of directional asymmetry in the zebrafish epithalamus. Semin. Cell Dev. Biol. 20:498–509 [Google Scholar]
  35. Concha ML, Wilson SW. 35.  2001. Asymmetry in the epithalamus of vertebrates. J. Anat. 199:1–263–84 [Google Scholar]
  36. Constam DB, Robertson EJ. 36.  2000. SPC4/PACE4 regulates a TGFβ signaling network during axis formation. Genes Dev. 14:91146–55 [Google Scholar]
  37. Corballis MC. 37.  2014. Left brain, right brain: facts and fantasies. PLOS Biol. 12:1e1001767 [Google Scholar]
  38. Dadda M, Bisazza A. 37a.  2006. Does brain asymmetry allow efficient performance of simultaneous tasks?. Anim. Behav. 72:3523–29 [Google Scholar]
  39. Dadda M, Zandona E, Agrillo C, Bisazza A. 38.  2009. The costs of hemispheric specialization in a fish. Proc. Biol. Sci. 276:4399–4407 [Google Scholar]
  40. Dax M. 39.  1865. Lésions de la moitié gauche de l'encéphale coïncident avec l'oubli des signes de la pensée (lu à montpellier en 1936). Gaz. Hebd. Médecine Chir. Tome 2 2:259–62 [Google Scholar]
  41. Dean BJ, Erdogan B, Gamse JT, Wu S-Y. 40.  2014. Dbx1b defines the dorsal habenular progenitor domain in the zebrafish epithalamus. Neural Dev. 9:120 [Google Scholar]
  42. De Borsetti NH, Dean BJ, Bain EJ, Clanton JA, Taylor RW, Gamse JT. 41.  2011. Light and melatonin schedule neuronal differentiation in the habenular nuclei. Dev. Biol. 358:1251–61 [Google Scholar]
  43. deCarvalho TN, Subedi A, Rock J, Harfe BD, Thisse C. 42.  et al. 2014. Neurotransmitter map of the asymmetric dorsal habenular nuclei of zebrafish. Genesis 52:6636–55 [Google Scholar]
  44. Demaree HA, Everhart DE, Youngstrom EA, Harrison DW. 43.  2005. Brain lateralization of emotional processing: historical roots and a future incorporating “dominance.”. Behav. Cogn. Neurosci. Rev. 4:13–20 [Google Scholar]
  45. Dennis EL, Thompson PM. 44.  2013. Mapping connectivity in the developing brain. Int. J. Dev. Neurosci. 31:7525–42 [Google Scholar]
  46. De Schotten MT, Dell'Acqua F, Forkel SJ, Simmons A, Vergani F. 45.  et al. 2011. A lateralized brain network for visuospatial attention. Nat. Neurosci. 14:101245–46 [Google Scholar]
  47. Diamond MC, Johnson RE, Young D, Singh SS. 46.  1983. Age-related morphologic differences in the rat cerebral cortex and hippocampus: male-female; right-left. Exp. Neurol. 81:11–13 [Google Scholar]
  48. Doll CA, Burkart JT, Hope KD, Halpern ME, Gamse JT. 47.  2011. Subnuclear development of the zebrafish habenular nuclei requires ER translocon function. Dev. Biol. 360:144–57 [Google Scholar]
  49. Dragovic M, Hammond G. 48.  2005. Handedness in schizophrenia: a quantitative review of evidence. Acta Psychiatr. Scand. 111:6410–19 [Google Scholar]
  50. Dreosti E, Vendrell Llopis N, Carl M, Yaksi E, Wilson SW. 49.  2014. Left-right asymmetry is required for the habenulae to respond to both visual and olfactory stimuli. Curr. Biol. 24:4440–45 [Google Scholar]
  51. Duboc V, Lapraz F, Besnardeau L, Lepage T. 50.  2008. Lefty acts as an essential modulator of nodal activity during sea urchin oral-aboral axis formation. Dev. Biol. 320:49–59 [Google Scholar]
  52. Duboc V, Rottinger E, Besnardeau L, Lapraz F, Lepage T. 51.  2005. Left-right asymmetry in the sea urchin embryo is regulated by nodal signaling on the right side. Dev. Cell 8:1–12 [Google Scholar]
  53. Ehret G. 52.  1987. Left hemisphere advantage in the mouse brain for recognizing ultrasonic communication calls. Nature 325:6101249–51 [Google Scholar]
  54. Facchin L, Argenton F, Bisazza A. 53.  2009. Lines of Danio rerio selected for opposite behavioural lateralization show differences in anatomical left-right asymmetries. Behav. Brain Res. 197:1157–65 [Google Scholar]
  55. Fagard J. 54.  2013. Early development of hand preference and language lateralization: Are they linked, and if so, how?. Dev. Psychobiol. 55:6596–607 [Google Scholar]
  56. Fink M, Wadsak W, Savli M, Stein P, Moser U. 55.  et al. 2009. Lateralization of the serotonin-1a receptor distribution in language areas revealed by pet. NeuroImage 45:2598–605 [Google Scholar]
  57. Fowler CD, Lu Q, Johnson PM, Marks MJ, Kenny PJ. 56.  2011. Habenular α5 nicotinic receptor subunit signaling controls nicotine intake. Nature 471:7340597–601 [Google Scholar]
  58. Francks C, Maegawa S, Laurén J, Abrahams BS, Velayos-Baeza A. 57.  et al. 2007. Lrrtm1 on chromosome 2p12 is a maternally suppressed gene that is associated paternally with handedness and schizophrenia. Mol. Psychiatry 12:121129–39 [Google Scholar]
  59. Gamse JT, Kuan YS, Macurak M, Brosamle C, Thisse B. 58.  et al. 2005. Directional asymmetry of the zebrafish epithalamus guides dorsoventral innervation of the midbrain target. Development 132:4869–81 [Google Scholar]
  60. Gamse JT, Thisse C, Thisse B, Halpern ME. 59.  2003. The parapineal mediates left-right asymmetry in the zebrafish diencephalon. Development 130:1059–68 [Google Scholar]
  61. Garric L, Ronsin B, Roussigné M, Booton S, Gamse JT. 60.  et al. 2014. Pitx2c ensures habenular asymmetry by restricting parapineal cell number. Development 141:71572–79 [Google Scholar]
  62. Gaub S, Groszer M, Fisher SE, Ehret G. 61.  2010. The structure of innate vocalizations in Foxp2-deficient mouse pups. Genes Brain Behav. 9:4390–401 [Google Scholar]
  63. Gazzaniga MS. 62.  2005. Forty-five years of split-brain research and still going strong. Nat. Rev. Neurosci. 6:8653–59 [Google Scholar]
  64. Gazzaniga MS, Bogen JE, Sperry RW. 63.  1962. Some functional effects of sectioning the cerebral commissures in man. PNAS 48:101765–69 [Google Scholar]
  65. Geschwind N, Galaburda AM. 64.  1985. Cerebral lateralization. Biological mechanisms, associations, and pathology: I. A hypothesis and a program for research. Arch. Neurol. 42:5428–59 [Google Scholar]
  66. Geschwind N, Levitsky W. 65.  1968. Human brain: left-right asymmetries in temporal speech region. Science 161:3837186–87 [Google Scholar]
  67. Glick SD, Ross DA, Hough LB. 66.  1982. Lateral asymmetry of neurotransmitters in human brain. Brain Res. 234:153–63 [Google Scholar]
  68. Goto K, Kurashima R, Gokan H, Inoue N, Ito I, Watanabe S. 67.  2010. Left-right asymmetry defect in the hippocampal circuitry impairs spatial learning and working memory in IV mice. PLOS ONE 5:11e15468 [Google Scholar]
  69. Gotts SJ, Jo HJ, Wallace GL, Saad ZS, Cox RW, Martin A. 68.  2013. Two distinct forms of functional lateralization in the human brain. PNAS 110:36E3435–44 [Google Scholar]
  70. Groothuis TGG, McManus IC, Schaafsma SM, Geuze RH. 69.  2013. The fighting hypothesis in combat: How well does the fighting hypothesis explain human left-handed minorities?. Ann. N. Y. Acad. Sci. 1288:1100–9 [Google Scholar]
  71. Groszer M, Keays DA, Deacon RMJ, de Bono JP, Prasad-Mulcare S. 70.  et al. 2008. Impaired synaptic plasticity and motor learning in mice with a point mutation implicated in human speech deficits. Curr. Biol. 18:5354–62 [Google Scholar]
  72. Haesler S, Rochefort C, Georgi B, Licznerski P, Osten P, Scharff C. 71.  2007. Incomplete and inaccurate vocal imitation after knockdown of FoxP2 in songbird basal ganglia nucleus area X. PLOS Biol. 5:12e321 [Google Scholar]
  73. Haesler S, Wada K, Nshdejan A, Morrisey EE, Lints T. 72.  et al. 2004. FoxP2 expression in avian vocal learners and non-learners. J. Neurosci. 24:133164–75 [Google Scholar]
  74. Halluin C, Madelaine R, Naye F, Leoture S, Peers B, Roussigné M, Blader P. 72a.  2015. Habenular neurogenesis in zebrafish is regulated by a Hedgehog, Pax6, proneural gene cascade. PLOS ONE Submitted [Google Scholar]
  75. Halpern ME, Liang JO, Gamse JT. 73.  2003. Leaning to the left: laterality in the zebrafish forebrain. Trends Neurosci. 26:308–13 [Google Scholar]
  76. Hendricks M, Jesuthasan S. 74.  2007. Asymmetric innervation of the habenula in zebrafish. J. Comp. Neurol. 502:611–19 [Google Scholar]
  77. Hepper PG, Shahidullah S, White R. 75.  1991. Handedness in the human fetus. Neuropsychologia 29:111107–11 [Google Scholar]
  78. Herbert MR, Ziegler DA, Deutsch CK, O'Brien LM, Kennedy DN. 76.  et al. 2005. Brain asymmetries in autism and developmental language disorder: a nested whole-brain analysis. Brain J. Neurol. 128:Pt. 1213–26 [Google Scholar]
  79. Hervé P-Y, Zago L, Petit L, Mazoyer B, Tzourio-Mazoyer N. 77.  2013. Revisiting human hemispheric specialization with neuroimaging. Trends Cogn. Sci. 17:269–80 [Google Scholar]
  80. Hobert O. 78.  2014. Development of left/right asymmetry in the Caenorhabditis elegans nervous system: from zygote to postmitotic neuron. Genesis 52:6528–43 [Google Scholar]
  81. Hong E, Santhakumar K, Akitake CA, Ahn SJ, Thisse C. 79.  et al. 2013. Cholinergic left-right asymmetry in the habenulo-interpeduncular pathway. PNAS 110:5221171–76 [Google Scholar]
  82. Husain M, Rorden C. 80.  2003. Non-spatially lateralized mechanisms in hemispatial neglect. Nat. Rev. Neurosci. 4:126–36 [Google Scholar]
  83. Hüsken U, Carl M. 81.  2013. The Wnt/beta-catenin signaling pathway establishes neuroanatomical asymmetries and their laterality. Mech. Dev. 130:6–8330–35 [Google Scholar]
  84. Hüsken U, Stickney HL, Gestri G, Bianco IH, Faro A. 82.  et al. 2014. Tcf7l2 is required for left-right asymmetric differentiation of habenular neurons. Curr. Biol. 24:192217–27 [Google Scholar]
  85. Ihara A, Hirata M, Fujimaki N, Goto T, Umekawa Y. 83.  et al. 2010. Neuroimaging study on brain asymmetries in situs inversus totalis. J. Neurol. Sci. 288:1–272–78 [Google Scholar]
  86. Kaplan S, Rağbetli , Canan S, Sahin B, Marangoz C. 84.  2003. Numerical density of pyramidal neurons in the hippocampus of 4 and 20 week old male and female rats. Neurosci. Res. Commun. 32:137–48 [Google Scholar]
  87. Karev GB. 85.  2008. Season of birth and parental age in right, mixed and left handers. Cortex 44:179–81 [Google Scholar]
  88. Kemali M, Guglielmotti V, Fiorino L. 86.  1990. The asymmetry of the habenular nuclei of female and male frogs in spring and in winter. Brain Res. 517:1–2251–55 [Google Scholar]
  89. Kennedy DN, O'Craven KM, Ticho BS, Goldstein AM, Makris N, Henson JW. 87.  1999. Structural and functional brain asymmetries in human situs inversus totalis. Neurology 53:61260–65 [Google Scholar]
  90. Kim M-S, Pinto SM, Getnet D, Nirujogi RS, Manda SS. 88.  et al. 2014. A draft map of the human proteome. Nature 509:7502575–81 [Google Scholar]
  91. Klöppel S, Mangin J-F, Vongerichten A, Frackowiak RSJ, Siebner HR. 89.  2010. Nurture versus nature: long-term impact of forced right-handedness on structure of pericentral cortex and basal ganglia. J. Neurosci. 30:93271–75 [Google Scholar]
  92. Knecht S, Dräger B, Deppe M, Bobe L, Lohmann H. 90.  et al. 2000. Handedness and hemispheric language dominance in healthy humans. Brain 123:122512–18 [Google Scholar]
  93. Krishnan S, Mathuru AS, Kibat C, Rahman M, Lupton CE. 91.  et al. 2014. The right dorsal habenula limits attraction to an odor in zebrafish. Curr. Biol. 24:111167–75 [Google Scholar]
  94. Kuan YS, Yu HH, Moens CB, Halpern ME. 92.  2007. Neuropilin asymmetry mediates a left-right difference in habenular connectivity. Development 134:857–86 [Google Scholar]
  95. Lagadec R, Laguerre L, Menuet A, Amara A, Rocancourt C. 93.  et al. 2015. Ancestral role of nodal signalling in breaking L/R symmetry in the vertebrate forebrain. Nat. Commun. 6:6686 [Google Scholar]
  96. Lai CSL, Fisher SE, Hurst JA, Vargha-Khadem F, Monaco AP. 94.  2001. A forkhead-domain gene is mutated in a severe speech and language disorder. Nature 413:6855519–23 [Google Scholar]
  97. Lawson RP, Seymour B, Loh E, Lutti A, Dolan RJ. 95.  et al. 2014. The habenula encodes negative motivational value associated with primary punishment in humans. PNAS 111:3211858–63 [Google Scholar]
  98. Lee A, Mathuru AS, Teh C, Kibat C, Korzh V. 96.  et al. 2010. The habenula prevents helpless behavior in larval zebrafish. Curr. Biol. 20:2211–16 [Google Scholar]
  99. LeMay M. 97.  1976. Morphological cerebral asymmetries of modern man, fossil man, and nonhuman primate. Ann. N. Y. Acad. Sci. 280:1349–66 [Google Scholar]
  100. Letzkus P, Ribi WA, Wood JT, Zhu H, Zhang S-W, Srinivasan MV. 98.  2006. Lateralization of olfaction in the honeybee Apis mellifera. Curr. Biol. 16:141471–76 [Google Scholar]
  101. Liang JO, Etheridge A, Hantsoo L, Rubinstein AL, Nowak SJ. 99.  et al. 2000. Asymmetric nodal signaling in the zebrafish diencephalon positions the pineal organ. Development 127:5101–12 [Google Scholar]
  102. Lindell AK. 100.  2013. Continuities in emotion lateralization in human and non-human primates. Front. Hum. Neurosci. 7:464 [Google Scholar]
  103. Llaurens V, Raymond M, Faurie C. 101.  2009. Why are some people left-handed? An evolutionary perspective. Philos. Trans. R. Soc. Lond. B 364:1519881–94 [Google Scholar]
  104. Long S, Ahmad N, Rebagliati M. 102.  2003. The zebrafish nodal-related gene southpaw is required for visceral and diencephalic left-right asymmetry. Development 130:2303–16 [Google Scholar]
  105. Lyn H, Pierre P, Bennett AJ, Fears S, Woods R, Hopkins WD. 103.  2011. Planum temporale grey matter asymmetries in chimpanzees (Pan troglodytes), vervet (Chlorocebus aethiops sabaeus), rhesus (Macaca mulatta) and bonnet (Macaca radiata) monkeys. Neuropsychologia 49:72004–12 [Google Scholar]
  106. Manning L, Thomas-Antérion C. 104.  2011. Marc Dax and the discovery of the lateralisation of language in the left cerebral hemisphere. Rev. Neurol. 167:12868–72 [Google Scholar]
  107. Manns M, Güntürkün O. 105.  1999. Monocular deprivation alters the direction of functional and morphological asymmetries in the pigeon's (Columba livia) visual system. Behav. Neurosci. 113:61257–66 [Google Scholar]
  108. Martinez-Ferre A, Martinez S. 106.  2009. The development of the thalamic motor learning area is regulated by Fgf8 expression. J. Neurosci. 29:4213389–400 [Google Scholar]
  109. Matsumoto M, Hikosaka O. 107.  2007. Lateral habenula as a source of negative reward signals in dopamine neurons. Nature 447:1111–15 [Google Scholar]
  110. Mazoyer B, Zago L, Jobard G, Crivello F, Joliot M. 108.  et al. 2014. Gaussian mixture modeling of hemispheric lateralization for language in a large sample of healthy individuals balanced for handedness. PLOS ONE 9:6e101165 [Google Scholar]
  111. McManus IC. 109.  1985. Handedness, language dominance and aphasia: a genetic model. Psychol. Med. Monogr. Suppl. 8:1–40 [Google Scholar]
  112. McManus IC. 110.  2005. Symmetry and asymmetry in aesthetics and the arts. Eur. Rev. 13:Suppl. S2157–80 [Google Scholar]
  113. McManus IC, Martin N, Stubbings GF, Chung EMK, Mitchison HM. 111.  2004. Handedness and situs inversus in primary ciliary dyskinesia. Proc. R. Soc. Lond. B 271:15572579–82 [Google Scholar]
  114. McManus IC, Davison A, Armour JAL. 111a.  2013. Multilocus genetic models of handedness resemble single-locus models in explaining family data and are compatible with genome-wide association studies. Ann. N. Y. Acad. Sci. 1288:48–58 [Google Scholar]
  115. Medland SE, Duffy DL, Spurdle AB, Wright MJ, Geffen GM. 112.  et al. 2005. Opposite effects of androgen receptor CAG repeat length on increased risk of left-handedness in males and females. Behav. Genet. 35:6735–44 [Google Scholar]
  116. Miklósi A, Andrew RJ, Savage H. 113.  1997. Behavioural lateralisation of the tetrapod type in the zebrafish (Brachydanio rerio). Physiol. Behav. 63:1127–35 [Google Scholar]
  117. Milenković S, Rock D, Dragović M, Janca A. 114.  2008. Season of birth and handedness in Serbian high school students. Ann. Gen. Psychiatry 7:12 [Google Scholar]
  118. Milner B. 115.  1968. Visual recognition and recall after right temporal-lobe excision in man. Neuropsychologia 6:3191–209 [Google Scholar]
  119. Miyasaka N, Morimoto K, Tsubokawa T, Higashijima S, Okamoto H, Yoshihara Y. 116.  2009. From the olfactory bulb to higher brain centers: genetic visualization of secondary olfactory pathways in zebrafish. J. Neurosci. 29:4756–67 [Google Scholar]
  120. Morokuma J, Ueno M, Kawanishi H, Saiga H, Nishida H. 117.  2002. HrNodal, the ascidian nodal-related gene, is expressed in the left side of the epidermis, and lies upstream of HrPitx. Dev. Genes Evol. 212:9439–46 [Google Scholar]
  121. Namigai EKO, Kenny NJ, Shimeld SM. 118.  2014. Right across the tree of life: the evolution of left-right asymmetry in the bilateria. Genesis 52:6458–70 [Google Scholar]
  122. Neugebauer JM, Yost HJ. 119.  2014. Fgf signaling is required for brain left-right asymmetry and brain midline formation. Dev. Biol. 386:1123–34 [Google Scholar]
  123. Ocklenburg S, Arning L, Gerding WM, Epplen JT, Güntürkün O, Beste C. 120.  2013. Foxp2 variation modulates functional hemispheric asymmetries for speech perception. Brain Lang. 126:3279–84 [Google Scholar]
  124. Ocklenburg S, Beste C, Arning L, Peterburs J, Güntürkün O. 121.  2014. The ontogenesis of language lateralization and its relation to handedness. Neurosci. Biobehav. Rev. 43:191–98 [Google Scholar]
  125. Ocklenburg S, Ströckens F, Güntürkün O. 122.  2013. Lateralisation of conspecific vocalisation in non-human vertebrates. Later. Asymmetries Body Brain Cogn. 18:11–31 [Google Scholar]
  126. Oke A, Lewis R, Adams RN. 123.  1980. Hemispheric asymmetry of norepinephrine distribution in rat thalamus. Brain Res. 188:1269–72 [Google Scholar]
  127. Oliverio M, Digilio MC, Versacci P, Dallapiccola B, Marino B. 124.  2010. Shells and heart: Are human laterality and chirality of snails controlled by the same maternal genes?. Am. J. Med. Genet. A 152A:102419–25 [Google Scholar]
  128. Palmer AR. 125.  2009. Animal asymmetry. Curr. Biol. 19:12R473–77 [Google Scholar]
  129. Pascual A, Huang K-L, Neveu J, Préat T. 126.  2004. Neuroanatomy: brain asymmetry and long-term memory. Nature 427:6975605–6 [Google Scholar]
  130. Pennekamp P, Menchen T, Dworniczak B, Hamada H. 127.  2015. Situs inversus and ciliary abnormalities: 20 years later, what is the connection?. Cilia 4:11 [Google Scholar]
  131. Peters M, Reimers S, Manning JT. 128.  2006. Hand preference for writing and associations with selected demographic and behavioral variables in 255,100 subjects: the BBC internet study. Brain Cogn. 62:2177–89 [Google Scholar]
  132. Piedra ME, Icardo JM, Albajar M, Rodriguez-Rey JC, Ros MA. 129.  1998. Pitx2 participates in the late phase of the pathway controlling left-right asymmetry. Cell 94:3319–24 [Google Scholar]
  133. Pinel P, Fauchereau F, Moreno A, Barbot A, Lathrop M. 130.  et al. 2012. Genetic variants of FOXP2 and KIAA0319/TTRAP/THEM2 locus are associated with altered brain activation in distinct language-related regions. J. Neurosci. 32:3817–25 [Google Scholar]
  134. Previc FH. 131.  1991. A general theory concerning the prenatal origins of cerebral lateralization in humans. Psychol. Rev. 98:3299–334 [Google Scholar]
  135. Price CJ. 132.  2012. A review and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading. Neuroimage 62:2816–47 [Google Scholar]
  136. Raymond M, Pontier D, Dufour A-B, Moller AP. 133.  1996. Frequency-dependent maintenance of left handedness in humans. Proc. R. Soc. Lond. B 263:13771627–33 [Google Scholar]
  137. Regan JC, Concha ML, Roussigné M, Russell C, Wilson SW. 134.  2009. An Fgf8-dependent bistable cell migratory event establishes CNS asymmetry. Neuron 61:127–34 [Google Scholar]
  138. Rogers LJ. 135.  1982. Light experience and asymmetry of brain function in chickens. Nature 297:5863223–25 [Google Scholar]
  139. Rogers LJ. 136.  1990. Light input and the reversal of functional lateralization in the chicken brain. Behav. Brain Res. 38:3211–21 [Google Scholar]
  140. Rogers LJ, Zucca P, Vallortigara G. 136a.  2004. Advantages of having a lateralized brain. Proc. R. Soc. Lond. B 271:Suppl. 6S420–22 [Google Scholar]
  141. Rogers LJ. 137.  2009. Hand and paw preferences in relation to the lateralized brain. Philos. Trans. R. Soc. Lond. B 364:1519943–54 [Google Scholar]
  142. Rogers LJ. 138.  2014. Asymmetry of brain and behavior in animals: its development, function, and human relevance. Genesis 52:6555–71 [Google Scholar]
  143. Rogers LJ, Rigosi E, Frasnelli E, Vallortigara G. 139.  2013. A right antenna for social behaviour in honeybees. Sci. Rep 3:2045 [Google Scholar]
  144. Rogers LJ, Sink HS. 140.  1988. Transient asymmetry in the projections of the rostral thalamus to the visual hyperstriatum of the chicken, and reversal of its direction by light exposure. Exp. Brain Res 70:2378–84 [Google Scholar]
  145. Rogers LJ, Vallortigara G. 141.  2008. From antenna to antenna: lateral shift of olfactory memory recall by honeybees. PLOS ONE 3:6e2340 [Google Scholar]
  146. Rogers LJ, Zucca P, Vallortigara G. 142.  2004. Advantages of having a lateralized brain. Proc. R. Soc. Lond. B 271:Suppl. 6S420–22 [Google Scholar]
  147. Roussigné M, Bianco IH, Wilson SW, Blader P. 143.  2009. Nodal signalling imposes left-right asymmetry upon neurogenesis in the habenular nuclei. Development 136:1549–57 [Google Scholar]
  148. Roussigné M, Blader P, Wilson SW. 144.  2012. Breaking symmetry: the zebrafish as a model for understanding left-right asymmetry in the developing brain. Dev. Neurobiol 72:3269–81 [Google Scholar]
  149. Ryan AK, Blumberg B, Rodriguez-Esteban C, Yonei-Tamura S, Tamura K. 145.  et al. 1998. Pitx2 determines left-right asymmetry of internal organs in vertebrates. Nature 394:6693545–51 [Google Scholar]
  150. Salas R, Sturm R, Boulter J, Biasi MD. 146.  2009. Nicotinic receptors in the habenulo-interpeduncular system are necessary for nicotine withdrawal in mice. J. Neurosci 29:103014–18 [Google Scholar]
  151. Savic I. 147.  2014. Asymmetry of cerebral gray and white matter and structural volumes in relation to sex hormones and chromosomes. Neuroendocr. Sci 8:329 [Google Scholar]
  152. Scerri TS, Brandler WM, Paracchini S, Morris AP, Ring SM. 148.  et al. 2011. PCSK6 is associated with handedness in individuals with dyslexia. Hum. Mol. Genet 20:3608–14 [Google Scholar]
  153. Shu W, Cho JY, Jiang Y, Zhang M, Weisz D. 149.  et al. 2005. Altered ultrasonic vocalization in mice with a disruption in the Foxp2 gene. PNAS 102:279643–48 [Google Scholar]
  154. Slomianka L, West MJ. 150.  1987. Asymmetry in the hippocampal region specific for one of two closely related species of wild mice. Brain Res 436:169–75 [Google Scholar]
  155. Snelson CD, Santhakumar K, Halpern ME, Gamse JT. 151.  2008. Tbx2b is required for the development of the parapineal organ. Development 135:1693–1702 [Google Scholar]
  156. Stoyanov Z, Nikolova P, Pashalieva I. 152.  2011. Season of birth, Geschwind and Galaburda hypothesis, and handedness. Later. Asymmetries Body Brain Cogn 16:5607–19 [Google Scholar]
  157. Sun T, Patoine C, Abu-Khalil A, Visvader J, Sum E. 153.  et al. 2005. Early asymmetry of gene transcription in embryonic human left and right cerebral cortex. Science 308:57291794–98 [Google Scholar]
  158. Sun T, Walsh CA. 154.  2006. Molecular approaches to brain asymmetry and handedness. Nat. Rev. Neurosci 7:655–62 [Google Scholar]
  159. Sun ZY, Klöppel S, Rivière D, Perrot M, Frackowiak R. 155.  et al. 2012. The effect of handedness on the shape of the central sulcus. NeuroImage 60:1332–39 [Google Scholar]
  160. Taylor RW, Hsieh YW, Gamse JT, Chuang CF. 156.  2010. Making a difference together: reciprocal interactions in C. elegans and zebrafish asymmetric neural development. Development 137:681–91 [Google Scholar]
  161. Taylor RW, Qi JY, Talaga AK, Ma TP, Pan L. 157.  et al. 2011. Asymmetric inhibition of Ulk2 causes left-right differences in habenular neuropil formation. J. Neurosci 31:279869–78 [Google Scholar]
  162. Toga AW, Thompson PM. 158.  2003. Mapping brain asymmetry. Nat. Rev. Neurosci 4:137–48 [Google Scholar]
  163. Tonetti L, Adan A, Caci H, Fabbri M, Natale V. 159.  2012. Season of birth and handedness in young adults. Later. Asymmetries Body Brain Cogn 17:5597–601 [Google Scholar]
  164. Tran US, Stieger S, Voracek M. 160.  2014. Latent variable analysis indicates that seasonal anisotropy accounts for the higher prevalence of left-handedness in men. Cortex 57:188–97 [Google Scholar]
  165. Vallar G. 161.  1998. Spatial hemineglect in humans. Trends Cogn. Sci 2:387–97 [Google Scholar]
  166. Vallortigara G, Rogers LJ. 162.  2005. Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav. Brain Sci 28:575–89 discuss. 589–633 [Google Scholar]
  167. Vallortigara G, Rogers LJ, Bisazza A, Lippolis G, Robins A. 163.  1998. Complementary right and left hemifield use for predatory and agonistic behaviour in toads. NeuroReport 9:143341–44 [Google Scholar]
  168. Vandenberg LN, Levin M. 164.  2013. A unified model for left-right asymmetry? Comparison and synthesis of molecular models of embryonic laterality. Dev. Biol 379:11–15 [Google Scholar]
  169. Vigneau M, Beaucousin V, Hervé PY, Duffau H, Crivello F. 165.  et al. 2006. Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing. NeuroImage 30:41414–32 [Google Scholar]
  170. Webb JR, Schroeder MI, Chee C, Dial D, Hana R. 166.  et al. 2013. Left-handedness among a community sample of psychiatric outpatients suffering from mood and psychotic disorders. SAGE Open doi: 10.1177/2158244013503166 [Google Scholar]
  171. Yáñez J, Pombal MA, Anadón R. 167.  1999. Afferent and efferent connections of the parapineal organ in lampreys: a tract tracing and immunocytochemical study. J. Comp. Neurol 403:2171–89 [Google Scholar]
  172. Yoshida K, Saiga H. 168.  2011. Repression of Rx gene on the left side of the sensory vesicle by nodal signaling is crucial for right-sided formation of the ocellus photoreceptor in the development of Ciona intestinalis. Dev. Biol 354:1144–50 [Google Scholar]
  173. Yoshioka H, Meno C, Koshiba K, Sugihara M, Itoh H. 169.  et al. 1998. Pitx2, a bicoid-type homeobox gene, is involved in a lefty-signaling pathway in determination of left-right asymmetry. Cell 94:3299–305 [Google Scholar]
/content/journals/10.1146/annurev-genet-112414-055322
Loading
/content/journals/10.1146/annurev-genet-112414-055322
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error