Early differences in epithalamic left-right asymmetry influence lateralization and personality of adult zebrafish

Behavioural Brain Research

Volumn 206, Issue 2, 2010, Pages 208-215

  Dadda, Marco ^a   Domenichini, Alice ^a   Piffer, Laura ^a   Argenton, Francesco ^a   Bisazza, Angelo ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

Asymmetry; Lateralization; Personality; Zebrafish

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; COPING BEHAVIOR; EMBRYO; EPITHALAMUS; EYE DOMINANCE; FEMALE; HABENULA; HEMISPHERIC DOMINANCE; HORMONE RESPONSE; LEARNING; LEFT HEMISPHERE; MALE; MOTOR PERFORMANCE; NERVOUS SYSTEM DEVELOPMENT; NEUROANATOMY; NONHUMAN; OPEN FIELD TEST; PERSONALITY; PINEAL BODY; PREDATOR AVOIDANCE; PRIORITY JOURNAL; RIGHT HEMISPHERE; SEX DIFFERENCE; SOCIAL DISTANCE; SOCIAL ISOLATION; STRESS; ZEBRA FISH;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BEHAVIOR, ANIMAL; EPITHALAMUS; FEMALE; FUNCTIONAL LATERALITY; GREEN FLUORESCENT PROTEINS; MALE; MOTOR ACTIVITY; SOCIAL BEHAVIOR; VIDEO RECORDING; ZEBRAFISH;

EID: 70350340469     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2009.09.019     Document Type: Article

References (71)

1. Brown C., Gardner C., and Braithwaite V.A. Population variation in lateralized eye use in the poeciliid Brachyraphis episcopi. Proc R Soc B 271 (2004) S455-S457
2. Knecht S., Drager B., Deppe M., Bobe L., Lohmann H., Floel A., et al. Handedness and hemispheric language dominance in healthy humans. Brain 123 (2000) 2512-2518
3. Crow T.J., Crow L.R., Done D.J., and Leask S. Relative hand skill predicts academic ability: global deficits at the point of hemispheric indecision. Neuropsychologia 36 (1998) 1275-1282
4. Quaranta A., Siniscalchi M., Frate A., and Vallortigara G. Paw preference in dogs: relations between lateralised behaviour and immunity. Behav Brain Res 153 (2004) 521-525
5. Neveu P.J. Lateralization and stress responses in mice: interindividual differences in the association of brain, neuroendocrine, and immune responses. Behav Genet 26 (1996) 373-377
6. Pascual A., Huang K.L., Neveu J., and Preat T. Brain asymmetry and long-term memory: fruitflies that have structurally similar brain hemispheres forget within a matter of hours. Nature 427 (2004) 605-606
7. Rogers L.J., Zucca P., and Vallortigara G. Advantages of having a lateralized brain. Proc R Soc B 271 (2004) S420-S422
8. Bisazza A., and Dadda M. Enhanced schooling performance in lateralized fishes. Proc R Soc B 272 (2005) 1677-1681
9. Dadda M., and Bisazza A. Does brain asymmetry allow efficient performance of simultaneous tasks?. Anim Behav 72 (2006) 523-529
10. Gunturkun O., Diekamp B., Manns M., Nottelmann F., Prior H., Schwarz A., et al. Asymmetry pays: visual lateralization improves discrimination success in pigeons. Curr Biol 10 (2000) 1079-1081
11. McGrew W.C., and Marchant L.F. Laterality of hand use pays off in foraging success for wild chimpanzees. Primates 40 (1999) 509-513
12. Geschwind N., and Behan P. Left-handedness: association with immune disease, migraine, and developmental learning disorder. Proc Natl Acad Sci USA 79 (1982) 5097-5100
13. Lengen C., Regard M., Joller H., Landis T., and Lalive P. Anomalous brain dominance and the immune system: do left-handers have specific immunological patterns?. Brain Cogn 69 (2009) 188-193
14. Demaree H.A., Everhart D.E., Youngstrom E.A., and Harrison D.W. Brain lateralization of emotional processing: historical roots and a future incorporating "dominance". Behav Cogn Neurosci Rev 4 (2005) 3-20
15. Galaburda A.M., Menard M.T., and Rosen G.D. Evidence for aberrant auditory anatomy in developmental dyslexia. Proc Natl Acad Sci USA 91 (1994) 8010-8013
16. Heim S., Kissler J., Elbert T., and Rockstroh B. Cerebral lateralization in schizophrenia and dyslexia: neuromagnetic responses to auditory stimuli. Neuropsychologia 42 (2004) 692-697
17. Crow T.J. Is schizophrenia the price that Homo sapiens pays for language?. Schizophr Res 28 (1997) 127-141
18. Herbert M.R., Ziegler D.A., Deutsch C.K., O'Brien L.M., Kennedy D.N., Filipek P.A., et al. Brain asymmetries in autism and developmental language disorder: a nested whole-brain analysis. Brain 128 (2005) 213-226
19. Barth K.A., Miklosi A., Watkins J., Bianco I.H., Wilson S.W., and Andrew R.J. Fsi zebrafish show concordant reversal of laterality of viscera, neuroanatomy, and a subset of behavioral responses. Curr Biol 15 (2005) 844-850
20. Facchin L., Argenton F., and Bisazza A. Lines of Danio rerio selected for opposite behavioural lateralization show differences in anatomical left-right asymmetries. Behav Brain Res 197 (2009) 157-165
21. Collins R.L. Asymmetry and lateralization in the mouse - a genetic perspective. Behav Genet 20 (1990) 711-712
22. Nielsen D.M., Visker K.E., Cunningham M.J., Keller R.W., Glick S.D., and Carlson J.N. Paw preference, rotation, and dopamine function in collins HI and LO mouse strains. Physiol Behav 61 (1997) 525-535
23. Anneken K., Konrad C., Drager B., Breitenstein C., Kennerknecht I., Ringelstein E.B., et al. Familial aggregation of strong hemispheric language lateralization. Neurology 63 (2004) 2433-2435
24. Hopkins W.D., Dahl J.F., and Pilcher D. Genetic influence on the expression of hand preferences in Chimpanzees (Pan troglodytes): evidence in support of the right-shift theory and developmental instability. Psychol Sci 12 (2001) 299-303
25. Hamada H., Meno C., Watanabe D., and Saijoh Y. Establishment of vertebrate left-right asymmetry. Nat Rev Genet 3 (2002) 103-113
26. Long S., Ahmad N., and Rebagliati M. The zebrafish Nodal-related gene southpaw is required for visceral and diencephalic left-right asymmetry. Development 130 (2003) 2303-2316
27. Concha M.L., Burdine R.D., Russell C., Schier A.F., and Wilson S.W. A Nodal signaling pathway regulates the laterality of neuroanatomical asymmetries in the zebrafish forebrain. Neuron 28 (2000) 399-409
28. Concha M.L., Russell C., Regan J.C., Tawk M., Sidi S., Gilmour D.T., et al. Local tissue interactions across the dorsal midline of the forebrain establish CNS laterality. Neuron 39 (2003) 423-438
29. Concha M.L., and Wilson S.W. Asymmetry in the epithalamus of vertebrates. J Anat 199 (2001) 63-84
30. Sutherland R.J. The dorsal diencephalic conduction system: a review of the anatomy and functions of the habenular complex. Neurosci Biobehav Rev 6 (1982) 1-13
31. Sandyk R. Relevance of the habenular complex to neuropsychiatry: a review and hypothesis. Int J Neurosci 61 (1991) 189-219
32. Klemm W.R. Habenular and interpeduncularis nuclei: shared components in multiple-function networks. Med Sci Monit 10 (2004) RA261-RA273
33. Gamse J.T., Thisse C., Thisse B., and Halpern M.E. The parapineal mediates left-right asymmetry in the zebrafish diencephalon. Development 130 (2003) 1059-1068
34. Gamse J.T., Kuan Y.S., Macurak M., Brosamle C., Thisse B., Thisse C., et al. Directional asymmetry of the zebrafish epithalamus guides dorsoventral innervation of the midbrain target. Development 132 (2005) 4869-4880
35. Kuan Y.S., Yu H.H., Moens C.B., and Halpern M.E. Neuropilin asymmetry mediates a left-right difference habenular connectivity. Development 134 (2007) 857-865
36. Hendricks M., and Jesuthasan S. Asymmetric innervation of the habenula in zebrafish. J Comp Neurol 502 (2007) 611-619
37. Dall S.R.X., Houston A.I., and McNamara J.M. The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecol Lett 7 (2004) 734-739
38. Sih A., Bell A., and Johnson J.C. Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evolut 19 (2004) 372-378
39. Andrew R.J. Partial reversal and the functions of lateralisation. Behav Brain Sci 28 (2005) 589-590
40. Andrew R.J. Partial reversal of the brain generates new behavioural phenotypes. Cortex 42 (2006) 110-112
41. Reddon A.R., and Hurd P.L. Aggression, sex and individual differences in cerebral lateralization in a cichlid fish. Biol Lett 4 (2008) 338-340
42. Dadda M., Zandonà E., and Bisazza A. Emotional responsiveness in fish from lines artificially selected for a high or low degree of laterality. Physiol Behav 92 (2007) 764-772
43. Gilmour D.T., Maischein H.M., and Nusslein-Volhard C. Migration and function of a glial subtype in the vertebrate peripheral nervous system. Neuron 34 (2002) 577-588
44. Westerfield M. The zebrafish book: a guide for the laboratory use of zebrafish (Danio rerio) (1995), University of Oregon Press, Eugene, Oregon
45. Bisazza A., Dadda M., and Cantalupo C. Further evidence for mirror-reversed laterality in lines of fish selected for leftward or rightward turning when facing a predator model. Behav Brain Res 156 (2005) 165-171
46. Bilotta J., and Saszik S. The zebrafish as a model visual system. Int J Dev Neurosci 19 (2001) 621-629
47. Moretz J.A., Martins E.P., and Robison B.D. Behavioral syndromes and the evolution of correlated behavior in zebrafish. Behav Ecol 18 (2007) 556-562
48. Bale T.L., Picetti R., Contarino A., Koob G.F., Vale W.W., and Lee K.F. Mice deficient for both corticotropin-releasing factor receptor 1 (CRFR1) and CRFR2 have an impaired stress response and display sexually dichotomous anxiety-like behavior. J Neurosci 22 (2002) 193-199
49. Carola V., D'Olimpio F., Brunamonti E., Mangia F., and Renzi P. Evaluation of the elevated plus-maze and open-field tests for the assessment of anxiety-related behaviour in inbred mice. Behav Brain Res 134 (2002) 49-57
50. Facchin L., Burgess H.A., Siddiqi M., Granato M., and Halpern M.E. Determining the function of zebrafish epithalamic asymmetry. Philos Trans R Soc Lond B 364 (2009) 1021-1032
51. Facchin L., Bisazza A., and Vallortigara G. What causes lateralization of detour behavior in fish? Evidence for asymmetries in eye use. Behav Brain Res 103 (1999) 229-234
52. Clark M.M., Robertson R.K., and Galef Jr. B.G. Intrauterine position effects on sexually dimorphic asymmetries of Mongolian gerbils: testosterone, eye opening, and paw preference. Dev Psychobiol 26 (1993) 185-194
53. Rogers L.J., and Deng C. Corticosterone treatment of the chick embryo affects light-stimulated development of the thalamofugal visual pathway. Behav Brain Res 159 (2005) 63-71
54. Schwabl H. Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci USA 90 (1993) 11446-11450
55. McCormick M.I. Behaviorally induced maternal stress in a fish influences progeny quality by a hormonal mechanism. Ecology 79 (1998) 1873-1883
56. Rougeot C., Krim A., Mandiki S.N.M., Kestemont P., and Melard C. Sex steroid dynamics during embryogenesis and sexual differentiation in Eurasian perch, Perca fluviatilis. Theriogenology 67 (2007) 1046-1052
57. Reddon A.R., Gutirrez-Ibanez C., Wylie D.R., and Hurd P.L. The relationship between growth, brain asymmetry and behavioural lateralization in a cichlid fish. Behav Brain Res 201 (2009) 223-228
58. Andrew R.J., Dharmaretnam M., Gyori B., Miklosi A., Watkins J.A.S., and Sovrano V.A. Precise endogenous control of involvement of right and left visual structures in assessment by zebrafish. Behav Brain Res 196 (2009) 99-105
59. Budaev S., and Andrew R.J. Patterns of early embryonic light exposure determine behavioural asymmetries in zebrafish: a habenular hypothesis. Behav Brain Res 200 (2009) 91-94
60. Rogers L.J., and Workman L. Light exposure during incubation affects competitive behaviour in domestic chicks. Appl Anim Behav Sci 23 (1989) 187-198
61. Andrew R.J. Origins of asymmetry in the CNS. Semin Cell Dev Biol 20 (2009) 485-490
62. Bianco I.H., Carl M., Russell C., Clarke J.D.W., and Wilson S.W. Brain asymmetry is encoded at the level of axon terminal morphology. Neural Dev 3 (2008) 9
63. Hopkins W.D., Russell J.L., and Cantalupo C. Neuroanatomical correlates of handedness for tool use in chimpanzees (Pan troglodytes): implication for theories on the evolution of language. Psychol Sci 18 (2007) 971-977
64. Cantalupo C., and Hopkins W.D. Asymmetric broca's area in great apes: a region of the ape brain is uncannily similar to one linked with speech in humans. Nature 414 (2001) 505
65. Phillips K.A., and Hopkins W.D. Exploring the relationship between cerebellar asymmetry and handedness in chimpanzees (Pan troglodytes) and capuchins (Cebus apella). Neuropsychologia 45 (2007) 2333-2339
66. Wilson D.S., Clark A.B., Coleman K., and Dearstyne T. Shyness and boldness in humans and other animals. Trends Ecol Evol 9 (1994) 442-446
67. Brown C., Burgess F., and Braithwaite V.A. Heritable and experiential effects on boldness in a tropical poeciliid. Behav Ecol Sociobiol 62 (2007) 237-243
68. Smith B.R., and Blumstein D.T. Fitness consequences of personality: a meta-analysis. Behav Ecol 19 (2008) 448-455
69. Biro P.A., and Stamps J.A. Are animal personality traits linked to life-history productivity?. Trends Ecol Evol 23 (2008) 361-368
70. Rogers L.J., and Andrew R.J. Comparative vertebrate lateralization (2002), Cambridge University Press, Cambridge
71. Reddon A.R., and Hurd P.L. Individual differences in cerebral lateralization are associated with shy-bold variation in the convict cichlid. Anim Behav 77 (2009) 189-193