Asymmetry in the epithalamus of vertebrates (original) (raw)

Abstract

The epithalamus is a major subdivision of the diencephalon constituted by the habenular nuclei and pineal complex. Structural asymmetries in this region are widespread amongst vertebrates and involve differences in size, neuronal organisation, neurochemistry and connectivity. In species that possess a photoreceptive parapineal organ, this structure projects asymmetrically to the left habenula, and in teleosts it is also situated on the left side of the brain. Asymmetries in size between the left and right sides of the habenula are often associated with asymmetries in neuronal organisation, although these two types of asymmetry follow different evolutionary courses. While the former is more conspicuous in fishes (with the exception of teleosts), asymmetries in neuronal organisation are more robust in amphibia and reptiles. Connectivity of the parapineal organ with the left habenula is not always coupled with asymmetries in habenular size and/or neuronal organisation suggesting that, at least in some species, assignment of parapineal and habenular asymmetries may be independent events.

The evolutionary origins of epithalamic structures are uncertain but asymmetry in this region is likely to have existed at the origin of the vertebrate, perhaps even the chordate, lineage. In at least some extant vertebrate species, epithalamic asymmetries are established early in development, suggesting a genetic regulation of asymmetry. In some cases, epigenetic factors such as hormones also influence the development of sexually dimorphic habenular asymmetries. Although the genetic and developmental mechanisms by which neuroanatomical asymmetries are established remain obscure, some clues regarding the mechanisms underlying laterality decisions have recently come from studies in zebrafish. The Nodal signalling pathway regulates laterality by biasing an otherwise stochastic laterality decision to the left side of the epithalamus. This genetic mechanism ensures a consistency of epithalamic laterality within the population. Between species, the laterality of asymmetry is variable and a clear evolutionary picture is missing. We propose that epithalamic structural asymmetries per se and not the laterality of these asymmetries are important for the behaviour of individuals within a species. A consistency of the laterality within a population may play a role in social behaviours between individuals of the species.

Keywords: Epithalamus, habenula, pineal complex, parapineal organ, asymmetry, evolution, genetics

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Selected References

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  1. Adrio F., Anadón R., Rodríguez-Moldes I. Distribution of choline acetyltransferase (ChAT) immunoreactivity in the central nervous system of a chondrostean, the siberian sturgeon (Acipenser baeri). J Comp Neurol. 2000 Oct 30;426(4):602–621. doi: 10.1002/1096-9861(20001030)426:4<602::aid-cne8>3.0.co;2-7. [DOI] [PubMed] [Google Scholar]
  2. Anadón R., Molist P., Rodríguez-Moldes I., López J. M., Quintela I., Cerviño M. C., Barja P., González A. Distribution of choline acetyltransferase immunoreactivity in the brain of an elasmobranch, the lesser spotted dogfish (Scyliorhinus canicula). J Comp Neurol. 2000 May 1;420(2):139–170. doi: 10.1002/(sici)1096-9861(20000501)420:2<139::aid-cne1>3.0.co;2-t. [DOI] [PubMed] [Google Scholar]
  3. Bisazza A, De santi A, Vallortigara G. Laterality and cooperation: mosquitofish move closer to a predator when the companion is on their left side. Anim Behav. 1999 May;57(5):1145–1149. doi: 10.1006/anbe.1998.1075. [DOI] [PubMed] [Google Scholar]
  4. Bisgrove B. W., Essner J. J., Yost H. J. Multiple pathways in the midline regulate concordant brain, heart and gut left-right asymmetry. Development. 2000 Aug;127(16):3567–3579. doi: 10.1242/dev.127.16.3567. [DOI] [PubMed] [Google Scholar]
  5. Braitenberg V., Kemali M. Exceptions to bilateral symmetry in the epithalamus of lower vertebrates. J Comp Neurol. 1970 Feb;138(2):137–146. doi: 10.1002/cne.901380203. [DOI] [PubMed] [Google Scholar]
  6. Burdine R. D., Schier A. F. Conserved and divergent mechanisms in left-right axis formation. Genes Dev. 2000 Apr 1;14(7):763–776. [PubMed] [Google Scholar]
  7. Butler A. B., Northcutt R. G. Architectonic studies of the diencephalon of Iguana iguana (Linnaeus). J Comp Neurol. 1973 Jun 15;149(4):439–462. doi: 10.1002/cne.901490404. [DOI] [PubMed] [Google Scholar]
  8. Butler A. B., Northcutt R. G. The diencephalon of the Pacific herring, Clupea harengus: cytoarchitectonic analysis. J Comp Neurol. 1993 Feb 22;328(4):527–546. doi: 10.1002/cne.903280406. [DOI] [PubMed] [Google Scholar]
  9. Butler A. B., Saidel W. M. Retinal projections in the freshwater butterfly fish, Pantodon buchholzi (Osteoglossoidei). I. Cytoarchitectonic analysis and primary visual pathways. Brain Behav Evol. 1991;38(2-3):127–153. doi: 10.1159/000114383. [DOI] [PubMed] [Google Scholar]
  10. Capdevila J., Vogan K. J., Tabin C. J., Izpisúa Belmonte J. C. Mechanisms of left-right determination in vertebrates. Cell. 2000 Mar 31;101(1):9–21. doi: 10.1016/S0092-8674(00)80619-4. [DOI] [PubMed] [Google Scholar]
  11. Chen H., Bagri A., Zupicich J. A., Zou Y., Stoeckli E., Pleasure S. J., Lowenstein D. H., Skarnes W. C., Chédotal A., Tessier-Lavigne M. Neuropilin-2 regulates the development of selective cranial and sensory nerves and hippocampal mossy fiber projections. Neuron. 2000 Jan;25(1):43–56. doi: 10.1016/s0896-6273(00)80870-3. [DOI] [PubMed] [Google Scholar]
  12. Chen J. N., van Eeden F. J., Warren K. S., Chin A., Nüsslein-Volhard C., Haffter P., Fishman M. C. Left-right pattern of cardiac BMP4 may drive asymmetry of the heart in zebrafish. Development. 1997 Nov;124(21):4373–4382. doi: 10.1242/dev.124.21.4373. [DOI] [PubMed] [Google Scholar]
  13. Cole W. C., Youson J. H. Morphology of the pineal complex of the anadromous sea lamprey, Petromyzon marinus L. Am J Anat. 1982 Oct;165(2):131–163. doi: 10.1002/aja.1001650205. [DOI] [PubMed] [Google Scholar]
  14. Concha M. L., Burdine R. D., Russell C., Schier A. F., Wilson S. W. A nodal signaling pathway regulates the laterality of neuroanatomical asymmetries in the zebrafish forebrain. Neuron. 2000 Nov;28(2):399–409. doi: 10.1016/s0896-6273(00)00120-3. [DOI] [PubMed] [Google Scholar]
  15. Cruce J. A. A cytoarchitectonic study of the diencephalon of the tegu lizard, Tupinambis nigropunctatus. J Comp Neurol. 1974 Feb 1;153(3):215–238. doi: 10.1002/cne.901530302. [DOI] [PubMed] [Google Scholar]
  16. Diamond M. C., Johnson R. E., Young D., Singh S. S. Age-related morphologic differences in the rat cerebral cortex and hippocampus: male-female; right-left. Exp Neurol. 1983 Jul;81(1):1–13. doi: 10.1016/0014-4886(83)90153-x. [DOI] [PubMed] [Google Scholar]
  17. Díaz C., Puelles L. Afferent connections of the habenular complex in the lizard Gallotia galloti. Brain Behav Evol. 1992;39(5):312–324. doi: 10.1159/000114128. [DOI] [PubMed] [Google Scholar]
  18. Díaz C., Puelles L. In vitro HRP-labeling of the fasciculus retroflexus in the lizard Gallotia galloti. Brain Behav Evol. 1992;39(5):305–311. doi: 10.1159/000114127. [DOI] [PubMed] [Google Scholar]
  19. EDINGER T. Paired pineal organs. Prog Neurobiol. 1956;(2):121–129. [PubMed] [Google Scholar]
  20. Ekström P., Borg B., van Veen T. Ontogenetic development of the pineal organ, parapineal organ, and retina of the three-spined stickleback, Gasterosteus aculeatus L. (Teleostei). Development of photoreceptors. Cell Tissue Res. 1983;233(3):593–609. doi: 10.1007/BF00212227. [DOI] [PubMed] [Google Scholar]
  21. Ekström P., Ebbesson S. O. The left habenular nucleus contains a discrete serotonin-immunoreactive subnucleus in the coho salmon (Oncorhynchus kisutch). Neurosci Lett. 1988 Aug 31;91(2):121–125. doi: 10.1016/0304-3940(88)90754-9. [DOI] [PubMed] [Google Scholar]
  22. Ekström P., Foster R. G., Korf H. W., Schalken J. J. Antibodies against retinal photoreceptor-specific proteins reveal axonal projections from the photosensory pineal organ in teleosts. J Comp Neurol. 1987 Nov 1;265(1):25–33. doi: 10.1002/cne.902650103. [DOI] [PubMed] [Google Scholar]
  23. Eldred W. D., Finger T. E., Nolte J. Central projections of the frontal organ of Rana pipiens, as demonstrated by the anterograde transport of horseradish peroxidase. Cell Tissue Res. 1980;211(2):215–222. doi: 10.1007/BF00236444. [DOI] [PubMed] [Google Scholar]
  24. Engbretson G. A., Brecha N., Reiner A. Substance P-like immunoreactivity in the parietal eye visual system of the lizard Uta stansburiana. Cell Tissue Res. 1982;227(3):543–554. doi: 10.1007/BF00204784. [DOI] [PubMed] [Google Scholar]
  25. Engbretson G. A., Reiner A., Brecha N. Habenular asymmetry and the central connections of the parietal eye of the lizard. J Comp Neurol. 1981 May 1;198(1):155–165. doi: 10.1002/cne.901980113. [DOI] [PubMed] [Google Scholar]
  26. FRONTERA J. G. A study of the anuran diencephalon. J Comp Neurol. 1952 Feb;96(1):1–69. doi: 10.1002/cne.900960102. [DOI] [PubMed] [Google Scholar]
  27. Farner H. P. Untersuchungen zur Embryonalentwicklung des Gehirns von Scyliorhinus canicula (L.). I. Bildung der Hirngestalt, Migrationsmodi und -phasen, Bau des Zwischenhirns. J Hirnforsch. 1978;19(4):313–332. [PubMed] [Google Scholar]
  28. Fernald R. D., Shelton L. C. The organization of the diencephalon and the pretectum in the cichlid fish, Haplochromis burtoni. J Comp Neurol. 1985 Aug 8;238(2):202–217. doi: 10.1002/cne.902380207. [DOI] [PubMed] [Google Scholar]
  29. Guglielmotti V., Fiorino L. Nitric oxide synthase activity reveals an asymmetrical organization of the frog habenulae during development: A histochemical and cytoarchitectonic study from tadpoles to the mature Rana esculenta, with notes on the pineal complex. J Comp Neurol. 1999 Aug 30;411(3):441–454. doi: 10.1002/(sici)1096-9861(19990830)411:3<441::aid-cne7>3.0.co;2-n. [DOI] [PubMed] [Google Scholar]
  30. Gugliemotti V., Fiorino L. Asymmetry in the left and right habenulo-interpeduncular tracts in the frog. Brain Res Bull. 1998;45(1):105–110. doi: 10.1016/s0361-9230(97)00315-8. [DOI] [PubMed] [Google Scholar]
  31. Gundy G. C., Ralph C. L., Wurst G. Z. Parietal eyes in lizards: zoogeographical correlates. Science. 1975 Nov 14;190(4215):671–673. doi: 10.1126/science.1237930. [DOI] [PubMed] [Google Scholar]
  32. Gurusinghe C. J., Ehrlich D. Sex-dependent structural asymmetry of the medial habenular nucleus of the chicken brain. Cell Tissue Res. 1985;240(1):149–152. doi: 10.1007/BF00217568. [DOI] [PubMed] [Google Scholar]
  33. Gurusinghe C. J., Zappia J. V., Ehrlich D. The influence of testosterone on the sex-dependent structural asymmetry of the medial habenular nucleus in the chicken. J Comp Neurol. 1986 Nov 8;253(2):153–162. doi: 10.1002/cne.902530203. [DOI] [PubMed] [Google Scholar]
  34. Güntürkün O., Diekamp B., Manns M., Nottelmann F., Prior H., Schwarz A., Skiba M. Asymmetry pays: visual lateralization improves discrimination success in pigeons. Curr Biol. 2000 Sep 7;10(17):1079–1081. doi: 10.1016/s0960-9822(00)00671-0. [DOI] [PubMed] [Google Scholar]
  35. HOLMGREN U. ON THE ONTOGENY OF THE PINEAL- AND PARAPINEAL ORGANS IN TELEOST FISHES. Prog Brain Res. 1965;10:172–182. [PubMed] [Google Scholar]
  36. Hafeez M. A., Merhige M. E. Light and electron microscopic study on the pineal complex of the coelacanth, Latimeria chalumnae Smith. Cell Tissue Res. 1977 Mar 9;178(2):249–265. doi: 10.1007/BF00219052. [DOI] [PubMed] [Google Scholar]
  37. Herkenham M., Nauta W. J. Afferent connections of the habenular nuclei in the rat. A horseradish peroxidase study, with a note on the fiber-of-passage problem. J Comp Neurol. 1977 May 1;173(1):123–146. doi: 10.1002/cne.901730107. [DOI] [PubMed] [Google Scholar]
  38. Herkenham M., Nauta W. J. Efferent connections of the habenular nuclei in the rat. J Comp Neurol. 1979 Sep 1;187(1):19–47. doi: 10.1002/cne.901870103. [DOI] [PubMed] [Google Scholar]
  39. KAPPERS J. A. SURVEY OF THE INNERVATION OF THE EPIPHYSIS CEREBRI AND THE ACCESSORY PINEAL ORGANS OF VERTEBRATES. Prog Brain Res. 1965;10:87–153. doi: 10.1016/s0079-6123(08)63448-2. [DOI] [PubMed] [Google Scholar]
  40. Kemali M., Agrelli I. The habenulo-interpeduncular nuclear system of a reptilian representative Lacerta sicula. Z Mikrosk Anat Forsch. 1972;85(3):325–333. [PubMed] [Google Scholar]
  41. Kemali M., Guglielmotti V. An electron microscope observation of the right and the two left portions of the habenular nuclei of the frog. J Comp Neurol. 1977 Nov 15;176(2):133–148. doi: 10.1002/cne.901760202. [DOI] [PubMed] [Google Scholar]
  42. Kemali M., Guglielmotti V., Fiorino L. The asymmetry of the habenular nuclei of female and male frogs in spring and in winter. Brain Res. 1990 May 28;517(1-2):251–255. doi: 10.1016/0006-8993(90)91034-e. [DOI] [PubMed] [Google Scholar]
  43. Kemali M., Guglielmotti V. The distribution of substance P in the habenulo-interpeduncular system of the frog shown by an immunohistochemical method. Arch Ital Biol. 1984 Dec;122(4):269–280. [PubMed] [Google Scholar]
  44. Kemali M., Miralto A., Sada E. Asymmetry of the habenulae in the elasmobranch "Scyllium stellare". I. Light microscopy. Z Mikrosk Anat Forsch. 1980;94(5):794–800. [PubMed] [Google Scholar]
  45. Kemali M., Miralto A. The habenular nuclei of the elasmobranch "Scyllium stellare": myelinated perikarya. Am J Anat. 1979 May;155(1):147–152. doi: 10.1002/aja.1001550112. [DOI] [PubMed] [Google Scholar]
  46. Kemali M. Morphological asymmetry of the habenulae of a macrosmatic mammal, the mole. Z Mikrosk Anat Forsch. 1984;98(6):951–954. [PubMed] [Google Scholar]
  47. Korf H. W., Wagner U. Nervous connections of the parietal eye in adult Lacerta s. sicula Rafinesque as demonstrated by anterograde and retrograde transport of horseradish peroxidase. Cell Tissue Res. 1981;219(3):567–583. doi: 10.1007/BF00209995. [DOI] [PubMed] [Google Scholar]
  48. Liang J. O., Etheridge A., Hantsoo L., Rubinstein A. L., Nowak S. J., Izpisúa Belmonte J. C., Halpern M. E. Asymmetric nodal signaling in the zebrafish diencephalon positions the pineal organ. Development. 2000 Dec;127(23):5101–5112. doi: 10.1242/dev.127.23.5101. [DOI] [PubMed] [Google Scholar]
  49. Lipp H. P., Collins R. L., Nauta W. J. Structural asymmetries in brains of mice selected for strong lateralization. Brain Res. 1984 Sep 24;310(2):393–396. doi: 10.1016/0006-8993(84)90168-9. [DOI] [PubMed] [Google Scholar]
  50. Maler L., Sas E., Johnston S., Ellis W. An atlas of the brain of the electric fish Apteronotus leptorhynchus. J Chem Neuroanat. 1991 Jan-Feb;4(1):1–38. doi: 10.1016/0891-0618(91)90030-g. [DOI] [PubMed] [Google Scholar]
  51. Masai I., Heisenberg C. P., Barth K. A., Macdonald R., Adamek S., Wilson S. W. floating head and masterblind regulate neuronal patterning in the roof of the forebrain. Neuron. 1997 Jan;18(1):43–57. doi: 10.1016/s0896-6273(01)80045-3. [DOI] [PubMed] [Google Scholar]
  52. Meiniel A., Collin J. P. Le complexe pinéal de l'ammocète (Lampetra planeri, Bl). IIdentification du ganglion sous-jacent a l'orane parapinéal et relations épithalamiques des organes pinéal et parapinéal. Z Zellforsch Mikrosk Anat. 1971;117(3):354–380. [PubMed] [Google Scholar]
  53. Meiniel A. Présence d'indolamines dans les organes pinéal et parapinéal de Lampetra planeri (Pétromyzontoïdes). C R Acad Sci Hebd Seances Acad Sci D. 1978 Sep 11;287(4):313–316. [PubMed] [Google Scholar]
  54. Melone J. H., Teitelbaum S. A., Johnson R. E., Diamond M. C. The rat amygdaloid nucleus: a morphometric right-left study. Exp Neurol. 1984 Nov;86(2):293–302. doi: 10.1016/0014-4886(84)90187-0. [DOI] [PubMed] [Google Scholar]
  55. Meyer-Rochow V. B., Stewart D. A light- and electron-microscopic study of the pineal complex of the ammocoete larva of the southern lamprey Geotria australis. Microsc Electron Biol Celular. 1992 Jun;16(1):69–85. [PubMed] [Google Scholar]
  56. Miklósi A., Andrew R. J. Right eye use associated with decision to bite in zebrafish. Behav Brain Res. 1999 Nov 15;105(2):199–205. doi: 10.1016/s0166-4328(99)00071-6. [DOI] [PubMed] [Google Scholar]
  57. Miklósi A., Andrew R. J., Savage H. Behavioural lateralisation of the tetrapod type in the zebrafish (Brachydanio rerio). Physiol Behav. 1997 Dec 31;63(1):127–135. doi: 10.1016/s0031-9384(97)00418-6. [DOI] [PubMed] [Google Scholar]
  58. Miralto A., Kemali M. Asymmetry of the habenulae in the elasmobranch "Scyllium stellare". II. Electron microscopy. Z Mikrosk Anat Forsch. 1980;94(5):801–813. [PubMed] [Google Scholar]
  59. Morgan M. J., O'Donnell J. M., Oliver R. F. Development of left-right asymmetry in the habenular nuclei of Rana temporaria. J Comp Neurol. 1973 May 15;149(2):203–214. doi: 10.1002/cne.901490206. [DOI] [PubMed] [Google Scholar]
  60. Murphy G. M., Jr Volumetric asymmetry in the human striate cortex. Exp Neurol. 1985 May;88(2):288–302. doi: 10.1016/0014-4886(85)90192-x. [DOI] [PubMed] [Google Scholar]
  61. Nieuwenhuys R., Bodenheimer T. S. The diencephalon of the primitive bony fish Polypterus in the light of the problem of homology. J Morphol. 1966 Mar;118(3):415–449. doi: 10.1002/jmor.1051180309. [DOI] [PubMed] [Google Scholar]
  62. Nieuwenhuys R. The brain of the lamprey in a comparative perspective. Ann N Y Acad Sci. 1977 Sep 30;299:97–145. doi: 10.1111/j.1749-6632.1977.tb41902.x. [DOI] [PubMed] [Google Scholar]
  63. Nishida H. Cell lineage analysis in ascidian embryos by intracellular injection of a tracer enzyme. III. Up to the tissue restricted stage. Dev Biol. 1987 Jun;121(2):526–541. doi: 10.1016/0012-1606(87)90188-6. [DOI] [PubMed] [Google Scholar]
  64. Nishida H., Satoh N. Determination and regulation in the pigment cell lineage of the ascidian embryo. Dev Biol. 1989 Apr;132(2):355–367. doi: 10.1016/0012-1606(89)90232-7. [DOI] [PubMed] [Google Scholar]
  65. Nordeen E. J., Yahr P. Hemispheric asymmetries in the behavioral and hormonal effects of sexually differentiating mammalian brain. Science. 1982 Oct 22;218(4570):391–394. doi: 10.1126/science.7123240. [DOI] [PubMed] [Google Scholar]
  66. OKSCHE A. SURVEY OF THE DEVELOPMENT AND COMPARATIVE MORPHOLOGY OF THE PINEAL ORGAN. Prog Brain Res. 1965;10:3–29. doi: 10.1016/s0079-6123(08)63445-7. [DOI] [PubMed] [Google Scholar]
  67. Oksche A., Hartwig H. G. Pineal sense organs--components of photoneuroendocrine systems. Prog Brain Res. 1979;52:113–130. doi: 10.1016/S0079-6123(08)62917-9. [DOI] [PubMed] [Google Scholar]
  68. doi: 10.1098/rstb.1998.0347. [DOI] [PMC free article] [Google Scholar]
  69. Peter R. E., Gill V. E. A stereotaxic atlas and technique for forebrain nuclei of the goldfish, Carassius auratus. J Comp Neurol. 1975 Jan 1;159(1):69–101. doi: 10.1002/cne.901590106. [DOI] [PubMed] [Google Scholar]
  70. Peter R. E., Macey M. J., Gill V. E. A stereotaxic atlas and technique for forebrain nuclei of the killfish, Fundulus heteroclitus. J Comp Neurol. 1975 Jan 1;159(1):103–127. doi: 10.1002/cne.901590107. [DOI] [PubMed] [Google Scholar]
  71. Rodriguez-Moldes I., Timmermans J. P., Adriaensen D., De Groodt-Lasseel M. H., Scheuermann D. W., Anadon R. Asymmetric distribution of calbindin-D28K in the ganglia habenulae of an elasmobranch fish. Anat Embryol (Berl) 1990;181(4):389–391. doi: 10.1007/BF00186911. [DOI] [PubMed] [Google Scholar]
  72. Rogers L. J. Evolution of hemispheric specialization: advantages and disadvantages. Brain Lang. 2000 Jun 15;73(2):236–253. doi: 10.1006/brln.2000.2305. [DOI] [PubMed] [Google Scholar]
  73. Rubenstein J. L., Shimamura K., Martinez S., Puelles L. Regionalization of the prosencephalic neural plate. Annu Rev Neurosci. 1998;21:445–477. doi: 10.1146/annurev.neuro.21.1.445. [DOI] [PubMed] [Google Scholar]
  74. Ruiz S., Anadón R. The fine structure of lamellate cells in the brain of amphioxus (Branchiostoma lanceolatum, Cephalochordata). Cell Tissue Res. 1991 Mar;263(3):597–600. doi: 10.1007/BF00327295. [DOI] [PubMed] [Google Scholar]
  75. STEYN W., WEBB M. The pineal complex in the fish Labeo umbratus. Anat Rec. 1960 Feb;136:79–85. doi: 10.1002/ar.1091360202. [DOI] [PubMed] [Google Scholar]
  76. Sandyk R. Relevance of the habenular complex to neuropsychiatry: a review and hypothesis. Int J Neurosci. 1991 Dec;61(3-4):189–219. doi: 10.3109/00207459108990738. [DOI] [PubMed] [Google Scholar]
  77. Schnitzlein H. N., Crosby E. C. The epithalamus and thalamus of the lungfish, protopterus. J Hirnforsch. 1968;10(4):351–371. [PubMed] [Google Scholar]
  78. Shanmugalingam S., Houart C., Picker A., Reifers F., Macdonald R., Barth A., Griffin K., Brand M., Wilson S. W. Ace/Fgf8 is required for forebrain commissure formation and patterning of the telencephalon. Development. 2000 Jun;127(12):2549–2561. doi: 10.1242/dev.127.12.2549. [DOI] [PubMed] [Google Scholar]
  79. Solessio E., Engbretson G. A. Antagonistic chromatic mechanisms in photoreceptors of the parietal eye of lizards. Nature. 1993 Jul 29;364(6436):442–445. doi: 10.1038/364442a0. [DOI] [PubMed] [Google Scholar]
  80. Solessio E., Engbretson G. A. Electroretinogram of the parietal eye of lizards: photoreceptor, glial, and lens cell contributions. Vis Neurosci. 1999 Sep-Oct;16(5):895–907. doi: 10.1017/s095252389916509x. [DOI] [PubMed] [Google Scholar]
  81. Stein S., Kessel M. A homeobox gene involved in node, notochord and neural plate formation of chick embryos. Mech Dev. 1995 Jan;49(1-2):37–48. doi: 10.1016/0925-4773(94)00300-c. [DOI] [PubMed] [Google Scholar]
  82. Striedter G. F. The diencephalon of the channel catfish, Ictalurus punctatus. I. Nuclear organization. Brain Behav Evol. 1990;36(6):329–354. doi: 10.1159/000115318. [DOI] [PubMed] [Google Scholar]
  83. Sutherland R. J. The dorsal diencephalic conduction system: a review of the anatomy and functions of the habenular complex. Neurosci Biobehav Rev. 1982 Spring;6(1):1–13. doi: 10.1016/0149-7634(82)90003-3. [DOI] [PubMed] [Google Scholar]
  84. Tamotsu S., Korf H. W., Morita Y., Oksche A. Immunocytochemical localization of serotonin and photoreceptor-specific proteins (rod-opsin, S-antigen) in the pineal complex of the river lamprey, Lampetra japonica, with special reference to photoneuroendocrine cells. Cell Tissue Res. 1990 Nov;262(2):205–216. doi: 10.1007/BF00309875. [DOI] [PubMed] [Google Scholar]
  85. VAN DE KAMER J. C. HISTOLOGICAL STRUCTURE AND CYTOLOGY OF THE PINEAL COMPLEX IN FISHES, AMPHIBIANS AND REPTILES. Prog Brain Res. 1965;10:30–48. doi: 10.1016/s0079-6123(08)63446-9. [DOI] [PubMed] [Google Scholar]
  86. Vallortigara G., Rogers L. J., Bisazza A. Possible evolutionary origins of cognitive brain lateralization. Brain Res Brain Res Rev. 1999 Aug;30(2):164–175. doi: 10.1016/s0165-0173(99)00012-0. [DOI] [PubMed] [Google Scholar]
  87. Van Eden C. G., Uylings H. B., Van Pelt J. Sex-difference and left-right asymmetries in the prefrontal cortex during postnatal development in the rat. Brain Res. 1984 Jan;314(1):146–153. doi: 10.1016/0165-3806(84)90186-x. [DOI] [PubMed] [Google Scholar]
  88. Vigh-Teichmann I., Ali M. A., Szél A., Vigh B. Ultrastructure and opsin immunocytochemistry of the pineal complex of the larval Arctic charr Salvelinus alpinus: a comparison with the retina. J Pineal Res. 1991;10(4):196–209. doi: 10.1111/j.1600-079x.1991.tb00816.x. [DOI] [PubMed] [Google Scholar]
  89. Vigh-Teichmann I., Korf H. W., Nürnberger F., Oksche A., Vigh B., Olsson R. Opsin-immunoreactive outer segments in the pineal and parapineal organs of the lamprey (Lampetra fluviatilis), the eel (Anguilla anguilla), and the rainbow trout (Salmo gairdneri). Cell Tissue Res. 1983;230(2):289–307. doi: 10.1007/BF00213806. [DOI] [PubMed] [Google Scholar]
  90. Vigh-Teichmann I., Röhlich P., Vigh B., Aros B. Comparison of the pineal complex, retina and cerebrospinal fluid contacting neurons by immunocytochemical antirhodopsin reaction. Z Mikrosk Anat Forsch. 1980;94(4):623–640. [PubMed] [Google Scholar]
  91. Wang R. Y., Aghajanian G. K. Physiological evidence for habenula as major link between forebrain and midbrain raphe. Science. 1977 Jul 1;197(4298):89–91. doi: 10.1126/science.194312. [DOI] [PubMed] [Google Scholar]
  92. Wicht H., Northcutt R. G. The forebrain of the Pacific hagfish: a cladistic reconstruction of the ancestral craniate forebrain. Brain Behav Evol. 1992;40(1):25–64. doi: 10.1159/000108540. [DOI] [PubMed] [Google Scholar]
  93. Wiechmann A. F., Wirsig-Wiechmann C. R. Distribution of melatonin receptors in the brain of the frog Rana pipiens as revealed by in vitro autoradiography. Neuroscience. 1993 Jan;52(2):469–480. doi: 10.1016/0306-4522(93)90173-d. [DOI] [PubMed] [Google Scholar]
  94. Wisniewski A. B. Sexually-dimorphic patterns of cortical asymmetry, and the role for sex steroid hormones in determining cortical patterns of lateralization. Psychoneuroendocrinology. 1998 Jul;23(5):519–547. doi: 10.1016/s0306-4530(98)00019-5. [DOI] [PubMed] [Google Scholar]
  95. Wree A., Zilles K., Schleicher A. Growth of fresh volumes and spontaneous cell death in the nuclei habenulae of albino rats during ontogenesis. Anat Embryol (Berl) 1981;161(4):419–431. doi: 10.1007/BF00316052. [DOI] [PubMed] [Google Scholar]
  96. Xiang M., Gan L., Zhou L., Klein W. H., Nathans J. Targeted deletion of the mouse POU domain gene Brn-3a causes selective loss of neurons in the brainstem and trigeminal ganglion, uncoordinated limb movement, and impaired suckling. Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11950–11955. doi: 10.1073/pnas.93.21.11950. [DOI] [PMC free article] [PubMed] [Google Scholar]
  97. Yañez J., Anadon R. Afferent and efferent connections of the habenula in the larval sea lamprey (Petromyzon marinus L.): an experimental study. J Comp Neurol. 1994 Jul 1;345(1):148–160. doi: 10.1002/cne.903450112. [DOI] [PubMed] [Google Scholar]
  98. Yañez J., Anadón R. Afferent and efferent connections of the habenula in the rainbow trout (Oncorhynchus mykiss): an indocarbocyanine dye (DiI) study. J Comp Neurol. 1996 Sep 2;372(4):529–543. doi: 10.1002/(SICI)1096-9861(19960902)372:4<529::AID-CNE3>3.0.CO;2-6. [DOI] [PubMed] [Google Scholar]
  99. Yáez J., Meissl H., Anadón R. Central projections of the parapineal organ of the adult rainbow trout (Oncorhynchus mykiss). Cell Tissue Res. 1996 Jul;285(1):69–74. doi: 10.1007/s004410050621. [DOI] [PubMed] [Google Scholar]
  100. Yáez J., Pombal M. A., Anadón R. Afferent and efferent connections of the parapineal organ in lampreys: a tract tracing and immunocytochemical study. J Comp Neurol. 1999 Jan 11;403(2):171–189. doi: 10.1002/(sici)1096-9861(19990111)403:2<171::aid-cne3>3.0.co;2-m. [DOI] [PubMed] [Google Scholar]
  101. Zhu M., Yu X., Ahlberg P. E. A primitive sarcopterygian fish with an eyestalk. Nature. 2001 Mar 1;410(6824):81–84. doi: 10.1038/35065078. [DOI] [PubMed] [Google Scholar]
  102. Zilles K., Schleicher A., Wingert F. Quantitative Analyse des Wachstums der Frischvolumina limbischer Kerngebiete im Diencephalon und Mesencephalon einer ontogenetischen Reihe von Albinomäusen. I. Nucleus habenulare. J Hirnforsch. 1976;17(1):1–10. [PubMed] [Google Scholar]
  103. van Veen T., Ekström P., Borg B., Møller M. The pineal complex of the three-spined stickleback, Gasterosteus aculeatus L.: a light-, electron microscopic and fluorescence histochemical investigation. Cell Tissue Res. 1980;209(1):11–28. doi: 10.1007/BF00219919. [DOI] [PubMed] [Google Scholar]
  104. van Veen T., Ostholm T., Gierschik P., Spiegel A., Somers R., Korf H. W., Klein D. C. alpha-Transducin immunoreactivity in retinae and sensory pineal organs of adult vertebrates. Proc Natl Acad Sci U S A. 1986 Feb;83(4):912–916. doi: 10.1073/pnas.83.4.912. [DOI] [PMC free article] [PubMed] [Google Scholar]
  105. van Veen T. The parapineal and pineal organs of the elver (glass eel), Anguilla anguilla L. Cell Tissue Res. 1982;222(2):433–444. doi: 10.1007/BF00213223. [DOI] [PubMed] [Google Scholar]
  106. von Dassow G., Schmidt J. E., Kimelman D. Induction of the Xenopus organizer: expression and regulation of Xnot, a novel FGF and activin-regulated homeo box gene. Genes Dev. 1993 Mar;7(3):355–366. doi: 10.1101/gad.7.3.355. [DOI] [PubMed] [Google Scholar]