Neurotransmitter map of the asymmetric dorsal habenular nuclei of zebrafish.

Tagide N deCarvalho, Abhignya Subedi, Jason Rock, Brian D Harfe, Christine Thisse, Bernard Thisse, Marnie E Halpern, Elim Hong
Author Information
  1. Tagide N deCarvalho: Department of Embryology, Carnegie Institution for Science, Baltimore, Maryland.

Abstract

The role of the habenular nuclei in modulating fear and reward pathways has sparked a renewed interest in this conserved forebrain region. The bilaterally paired habenular nuclei, each consisting of a medial/dorsal and lateral/ventral nucleus, can be further divided into discrete subdomains whose neuronal populations, precise connectivity, and specific functions are not well understood. An added complexity is that the left and right habenulae show pronounced morphological differences in many non-mammalian species. Notably, the dorsal habenulae of larval zebrafish provide a vertebrate genetic model to probe the development and functional significance of brain asymmetry. Previous reports have described a number of genes that are expressed in the zebrafish habenulae, either in bilaterally symmetric patterns or more extensively on one side of the brain than the other. The goal of our study was to generate a comprehensive map of the zebrafish dorsal habenular nuclei, by delineating the relationship between gene expression domains, comparing the extent of left-right asymmetry at larval and adult stages, and identifying potentially functional subnuclear regions as defined by neurotransmitter phenotype. Although many aspects of habenular organization appear conserved with rodents, the zebrafish habenulae also possess unique properties that may underlie lateralization of their functions.

Keywords

References

  1. PLoS One. 2011 Mar 25;6(3):e18180 [PMID: 21464954]
  2. Brain Res. 1987 Aug 25;418(2):273-86 [PMID: 2445413]
  3. Cell Tissue Res. 1990 Sep;261(3):493-500 [PMID: 2245450]
  4. Neuroscience. 2009 Jul 7;161(3):827-37 [PMID: 19362132]
  5. Neuron. 2003 Jul 31;39(3):423-38 [PMID: 12895418]
  6. J Comp Neurol. 1981 Dec 1;203(2):173-88 [PMID: 6118382]
  7. Gene Expr Patterns. 2010 Jan;10(1):75-85 [PMID: 19822223]
  8. J Comp Neurol. 2002 Nov 18;453(3):292-304 [PMID: 12378589]
  9. Gene Expr Patterns. 2011 Oct;11(7):395-400 [PMID: 21628002]
  10. J Comp Neurol. 1970 Feb;138(2):137-46 [PMID: 4189834]
  11. PLoS One. 2012;7(4):e35256 [PMID: 22523578]
  12. Dev Biol. 2011 Dec 1;360(1):44-57 [PMID: 21945073]
  13. J Comp Neurol. 1999 Apr 28;407(1):130-50 [PMID: 10213193]
  14. J Comp Neurol. 1977 May 1;173(1):123-46 [PMID: 845280]
  15. Neurobiol Dis. 2010 Oct;40(1):93-101 [PMID: 20600915]
  16. J Neurosci. 2010 Jan 27;30(4):1566-74 [PMID: 20107084]
  17. Arch Ital Biol. 1984 Dec;122(4):269-80 [PMID: 6084986]
  18. Nat Rev Neurosci. 2010 Jul;11(7):503-13 [PMID: 20559337]
  19. J Histochem Cytochem. 2007 Mar;55(3):301-11 [PMID: 17164411]
  20. Front Hum Neurosci. 2013 Dec 10;7:826 [PMID: 24339810]
  21. Philos Trans R Soc Lond B Biol Sci. 2009 Apr 12;364(1519):1005-20 [PMID: 19064356]
  22. Curr Biol. 2010 Dec 21;20(24):2211-6 [PMID: 21145744]
  23. J Comp Neurol. 1995 Oct 2;360(4):555-70 [PMID: 8801249]
  24. J Neurotrauma. 2010 May;27(5):959-72 [PMID: 20102264]
  25. Development. 2003 Mar;130(6):1059-68 [PMID: 12571098]
  26. Dev Dyn. 2013 Nov;242(11):1236-49 [PMID: 23908157]
  27. J Neurochem. 2008 Mar;104(5):1364-71 [PMID: 18036148]
  28. Dev Biol. 2014 Jan 1;385(1):13-22 [PMID: 24184636]
  29. Endocrinology. 2011 Apr;152(4):1527-40 [PMID: 21325050]
  30. Gen Comp Endocrinol. 2010 Apr 1;166(2):346-55 [PMID: 19941865]
  31. Endocrinology. 2009 Feb;150(2):821-31 [PMID: 18927220]
  32. Endocrinology. 2012 May;153(5):2398-407 [PMID: 22454151]
  33. Neuroscience. 1998 Jul;85(2):475-86 [PMID: 9622245]
  34. Neuron. 2007 Aug 2;55(3):393-405 [PMID: 17678853]
  35. J Comp Neurol. 1993 Sep 8;335(2):252-66 [PMID: 8227517]
  36. Front Hum Neurosci. 2014 Jan 17;7:931 [PMID: 24478666]
  37. Gen Comp Endocrinol. 2004 Oct;139(1):72-84 [PMID: 15474538]
  38. Genome Biol. 2009;10(9):R99 [PMID: 19765300]
  39. Dev Biol. 1983 Aug;98(2):349-72 [PMID: 6873459]
  40. Brain Res. 1978 Jun 30;149(2):413-29 [PMID: 352479]
  41. Int Rev Neurobiol. 1986;28:157-82 [PMID: 2433243]
  42. Brain Res Mol Brain Res. 1993 Jan;17(1-2):59-69 [PMID: 8381910]
  43. Brain Res Bull. 2012 Jul 1;88(4):345-53 [PMID: 22472058]
  44. J Anat. 2001 Jul-Aug;199(Pt 1-2):63-84 [PMID: 11523830]
  45. J Chem Neuroanat. 2013 May;50-51:66-74 [PMID: 23474224]
  46. J Comp Neurol. 2013 May 1;521(7):1533-60 [PMID: 23047810]
  47. Neurosci Biobehav Rev. 1982 Spring;6(1):1-13 [PMID: 7041014]
  48. PLoS Genet. 2012;8(12):e1003116 [PMID: 23284293]
  49. Exp Brain Res. 1983;53(1):193-6 [PMID: 6201381]
  50. J Comp Neurol. 2012 Dec 15;520(18):4051-66 [PMID: 22700183]
  51. Front Neurosci. 2012 Apr 23;6:51 [PMID: 22536170]
  52. J Biol Chem. 2005 Jun 10;280(23):22540-8 [PMID: 15824111]
  53. Dev Dyn. 2008 Mar;237(3):788-99 [PMID: 18224707]
  54. Dev Neurobiol. 2012 Mar;72(3):386-94 [PMID: 21567982]
  55. Nature. 2010 May 13;465(7295):231-5 [PMID: 20400944]
  56. BMC Dev Biol. 2007 Jul 25;7:89 [PMID: 17651502]
  57. Cell Tissue Res. 1980;211(2):215-22 [PMID: 6968242]
  58. Nat Rev Neurosci. 2012 Jan 18;13(2):94-106 [PMID: 22251956]
  59. Mol Cell Neurosci. 2008 Dec;39(4):592-604 [PMID: 18822380]
  60. Neural Dev. 2008 Mar 31;3:9 [PMID: 18377638]
  61. Front Neural Circuits. 2013 May 21;7:98 [PMID: 23734103]
  62. J Comp Neurol. 2003 Mar 24;458(1):78-97 [PMID: 12577324]
  63. Neuron. 2013 May 8;78(3):537-44 [PMID: 23602500]
  64. PLoS One. 2012;7(6):e37593 [PMID: 22768035]
  65. Dev Cell. 2007 Jan;12(1):87-98 [PMID: 17199043]
  66. PLoS One. 2013 Nov 27;8(11):e80491 [PMID: 24312227]
  67. J Comp Neurol. 2008 Dec 1;511(4):521-42 [PMID: 18839395]
  68. J Comp Neurol. 2011 Jun 1;519(8):1435-54 [PMID: 21452234]
  69. J Comp Neurol. 2006 Apr 20;495(6):769-87 [PMID: 16506201]
  70. Neurosci Biobehav Rev. 2007;31(5):658-72 [PMID: 17379307]
  71. Dev Dyn. 2008 Oct;237(10):2987-95 [PMID: 18816841]
  72. Brain Res Bull. 1984 Jul;13(1):203-4 [PMID: 6478267]
  73. Proc Natl Acad Sci U S A. 2009 Dec 22;106(51):21942-7 [PMID: 19966231]
  74. J Comp Neurol. 2009 Dec 10;517(5):695-710 [PMID: 19827161]
  75. PLoS One. 2011;6(9):e25111 [PMID: 21966429]
  76. Brain Res. 2001 May 18;901(1-2):117-27 [PMID: 11368958]
  77. Neuroscience. 1987 Apr;21(1):253-70 [PMID: 2439945]
  78. J Comp Neurol. 1979 Sep 1;187(1):19-47 [PMID: 226566]
  79. J Comp Neurol. 2006 Oct 10;498(5):593-610 [PMID: 16917825]
  80. J Biol Chem. 2012 Jan 27;287(5):2971-83 [PMID: 22128150]
  81. J Comp Neurol. 2006 Oct 20;498(6):796-809 [PMID: 16927269]
  82. J Biol Chem. 2013 Aug 23;288(34):24848-56 [PMID: 23843457]
  83. Mol Cell Neurosci. 2008 Feb;37(2):271-83 [PMID: 18060805]
  84. Dev Dyn. 2013 Dec;242(12):1427-41 [PMID: 24038627]
  85. J Comp Neurol. 1999 Apr 19;406(4):503-47 [PMID: 10205026]
  86. J Comp Neurol. 1989 Dec 22;290(4):502-15 [PMID: 2613941]
  87. Curr Biol. 2005 Feb 8;15(3):238-43 [PMID: 15694307]
  88. J Neurochem. 2006 Aug;98(3):951-61 [PMID: 16771836]
  89. J Comp Neurol. 2014 Aug 1;522(11):2650-62 [PMID: 24478034]
  90. PLoS One. 2012;7(11):e48911 [PMID: 23133663]
  91. Neuron. 2010 Oct 6;68(1):87-98 [PMID: 20920793]
  92. Dev Genes Evol. 2005 Nov;215(11):564-74 [PMID: 16193321]
  93. J Neurosci. 2011 Jul 6;31(27):9869-78 [PMID: 21734278]
  94. PLoS One. 2007 Jun 27;2(6):e573 [PMID: 17593972]
  95. Brain Res Bull. 2006 May 15;69(5):475-88 [PMID: 16647576]
  96. J Comp Neurol. 2007 Apr 10;501(5):703-15 [PMID: 17299752]
  97. J Neurosci. 2009 Nov 11;29(45):14309-22 [PMID: 19906978]
  98. Mol Cell Neurosci. 2009 Apr;40(4):401-9 [PMID: 19041397]
  99. Nat Neurosci. 2010 Nov;13(11):1354-6 [PMID: 20935642]
  100. J Comp Neurol. 1997 Jun 16;382(4):499-534 [PMID: 9184996]
  101. Dev Biol. 2008 Nov 1;323(1):31-40 [PMID: 18755178]
  102. J Neurosci. 2008 Nov 12;28(46):11825-9 [PMID: 19005047]
  103. Med Sci Monit. 2004 Nov;10(11):RA261-73 [PMID: 15507867]
  104. Development. 2005 Nov;132(21):4869-81 [PMID: 16207761]
  105. Proc Natl Acad Sci U S A. 2013 Dec 24;110(52):21171-6 [PMID: 24327734]
  106. Dev Dyn. 2008 Jan;237(1):233-46 [PMID: 18095341]
  107. Proc Natl Acad Sci U S A. 2012 Jun 26;109(26):10269-74 [PMID: 22689988]
  108. J Comp Neurol. 1977 Feb 1;72(3):319-44 [PMID: 319124]
  109. Gene Expr Patterns. 2006 Oct;6(8):777-82 [PMID: 16516559]
  110. Dev Biol. 2007 Jul 1;307(1):127-41 [PMID: 17531969]
  111. Development. 2009 May;136(9):1549-57 [PMID: 19363156]
  112. Dev Biol. 2009 Jun 15;330(2):406-26 [PMID: 19371731]
  113. J Neurosci. 2009 Apr 15;29(15):4756-67 [PMID: 19369545]
  114. Development. 2007 Mar;134(5):857-65 [PMID: 17251263]
  115. Dev Dyn. 2009 Mar;238(3):746-54 [PMID: 19235732]
  116. PLoS One. 2011;6(6):e20974 [PMID: 21687630]

Grants

  1. T32 GM007231/NIGMS NIH HHS
  2. F32 MH09198/NIMH NIH HHS
  3. R01 HD042215/NICHD NIH HHS
  4. F32 MH091980/NIMH NIH HHS
  5. F32 HL009198/NHLBI NIH HHS

MeSH Term

Animals
Animals, Genetically Modified
Gene Expression
Gene Expression Profiling
Gene Expression Regulation, Developmental
Genes, Reporter
Habenula
Immunohistochemistry
Neurons
Neurotransmitter Agents
Organ Specificity
Phenotype
Zebrafish

Chemicals

Neurotransmitter Agents

Word Cloud

Created with Highcharts 10.0.0habenularzebrafishnucleihabenulaedorsalasymmetryconservedbilaterallynucleusfunctionsmanylarvalfunctionalbrainmapleft-rightrolemodulatingfearrewardpathwayssparkedrenewedinterestforebrainregionpairedconsistingmedial/dorsallateral/ventralcandivideddiscretesubdomainswhoseneuronalpopulationspreciseconnectivityspecificwellunderstoodaddedcomplexityleftrightshowpronouncedmorphologicaldifferencesnon-mammalianspeciesNotablyprovidevertebrategeneticmodelprobedevelopmentsignificancePreviousreportsdescribednumbergenesexpressedeithersymmetricpatternsextensivelyonesidegoalstudygeneratecomprehensivedelineatingrelationshipgeneexpressiondomainscomparingextentadultstagesidentifyingpotentiallysubnuclearregionsdefinedneurotransmitterphenotypeAlthoughaspectsorganizationappearrodentsalsopossessuniquepropertiesmayunderlielateralizationNeurotransmitterasymmetricano2epithalamusgng8habenulainterpeduncularmbnl3somatostatin

Similar Articles

Cited By