Habenula circuit development: Past, present, and future

Frontiers in Neuroscience

Volumn , Issue APR, 2012, Pages

  Beretta, Carlo A ^a   Dross, Nicolas ^a   Guiterrez Triana, Jose A ^b   Ryu, Soojin ^b   Carl, Matthias ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

Author keywords

2PM imaging; Asymmetry; DDC; Epithalamus; Habenula; Neural circuit; Zebrafish

Indexed keywords

BRAIN ASYMMETRY; BRAIN REGION; DORSAL DIENCEPHALIC CONDUCTION SYSTEM; HABENULA; INTERPEDUNCLULAR NUCLEUS; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NEUROANATOMY; NEUROSCIENCE; REVIEW; ZEBRA FISH;

EID: 84862168559     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2012.00051     Document Type: Review

References (84)

1. Agetsuma, M., Aizawa, H., Aoki, T., Nakayama, R., Takahoko, M., Goto, M., Sassa, T., Amo, R., Shiraki, T., Kawakami, K., Hosoya, T., Higashijima, S., and Okamoto, H. (2010). The habenula is crucial for experience-dependent modification of fear responses in zebrafish. Nat. Neurosd. 13, 1354-1356.
2. Aizawa, H., Bianco, I. H., Hamaoka, T., Miyashita, T., Uemura, O., Concha, M. L, Russell, C, Wilson, S. W., and Okamoto, H. (2006). Laterotopic representation of left-right information onto the dorso-ventral axis of a zebrafish mid-brain target nucleus. Curr. Biol. 15, 238-243.
3. Aizawa, H., Goto, M., Sato, T., and Okamoto, H. (2007). Temporally regulated asymmetric neurogenesis causes left-right difference in the zebrafish habenular structures. Dev. Cell 12, 87-98.
4. Aizawa, H., Amo, R., and Okamoto, H. (2011). Phylogeny and ontogeny of the habenular structure. Front. Neurosd. 5, 138.
5. Amo, R., Aizawa, H., Takahoko, M., Kobayashi, M., Takahashi, R., Aoki, T., and Okamoto, H. (2010). Identification of the zebrafish ventral habenula as a homolog of the mammalian lateral habenula. J. Neurosd. 30, 1566-1574.
6. Ando, R., Hama, H., Yamamoto-Hino, M., Mizuno, H., and Miyawaki, A. (2002). An optical marker based on the UV-induced green-to-red photoconversion of a fluorescent protein. Proc. Natl. Acad. Sd. U.S.A. 99, 12651-12656.
7. Aramaki, S., and Hatta, K. (2006). Visualizing neurons one-by-one in vivo: optical dissection and reconstruction of neural networks with reversible fluorescent proteins. Dev. Dyn. 235,2192-2199.
8. Barth, K. A., Miklosi, A., Watkins, J., Bianco, I. H., Wilson, S. W, and Andrew, R. J. (2005). fsi zebrafish show concordant reversal of laterality of viscera, neuroanatomy, and a subset of behavioral responses. Curr. Biol. 15,844-850.
9. Bell, G., and Sons (1897). A Treatise on Painting. London: Elibron Classics.
10. Bianco, I. H., Carl, M., Russell, C, Clarke J.D., and Wilson, S.W. (2008). Brain asymmetry is encoded at the level of axon terminal morphology. Neural Dev. 3, 9.
11. Bianco, I. H., and Wilson, S. W. (2009). The habenular nuclei: a conserved asymmetric relay station in the vertebrate brain. Phil. Trans. R. Soc. B Biol. Sd. 364, 1005-1020.
12. Bisazza, A., Rogers, L. J., and Vallorti-gara, G. (1998). The origins of cerebral asymmetry: a review of evidence of behavioural and brain lateraliza-tion in fishes, reptiles and amphibians. Neurosd. Biobehav. Rev. 22, 411-426.
13. Breasted, J. H. (1980). The Edwin Smith Surgical Papyrus. Chicago: University Press.
14. Broca, P. P. (1861). Remarques sur la siege de la faculte du langage ariticule, suivies d'une observation d'apemie. Bull. Soc. Anatomique 2, 330-357.
15. Brown, T. G. (1914-1915). Note on the physiology of the basal ganglia and midbrain of the anthropoid ape, especially in reference to the act of laughter. J. Physiol. 47, 195-207.
16. Cajal, S. R. Y. (1911). Histologie du Systeme Nerveux de I'homme et des Vertebres, Vol. 2. Parie: Maloine, 270-275.
17. Carl, M., Bianco, I. H., Bajoghli, B., Aghaallaei, N., Czerny, T., and Wilson, S. W (2007). Wnt/Axinl/beta-catenin signaling regulates asymmetric nodal activation, elaboration, and concordance of ens asymmetries. Neuron 55, 393-405.
18. Concha, M. L., Burdine, R. D., Russell, C, Schier, A. E, and Wilson, S. W (2000). A nodal signaling pathway regulates the laterality of neuroanatomical asymmetries in the zebrafish forebrain. Neuron 28, 399-409.
19. Concha, M. L., Russell, C, Regan, J. C, Tawk, M., Sidi, S., Gilmour, D. T., Kapsimali, M., Sumoy, L., Gold-stone, K., Amaya, E., Kimelman, D., Nicolson, T., Griinder, S., Gomperts, M., Clarke, J. D., and Wilson, S. W. (2003). Local tissue interactions across the dorsal midline of the fore-brain establish CNS laterality. Neuron 39, 423-438.
20. Concha, M.L., and Wilson, S.W. (2001). Asymmetry in the epithalamus of vertebrates. J. Anat. 199, 63-84.
21. Cragg, B. G. (1961). The connections of the habenula in the rabbit. Exp. Neurol. 3, 388-409.
22. de Borsetti, N. H., Dean, B. J., Bain, E. J., Clanton, J. A., Taylor, R. W, and Gamse, J. T. (2011). Light and mela-tonin schedule neuronal differentiation in the habenular nuclei. Dev. Biol. 358,251-261.
23. Deguchi, T., Itoh, M., Urawa, H., Mat-sumoto, T., Nakayama, S., Kawasaki, T., Kitano, T., Oda, S., Mitani, H., Takahashi, T., Todo, T., Sato, J., Okada, K., Hatta, K., Yuba, S., and Kamei, Y. (2009). Infrared laser-mediated local gene induction in medaka, zebrafish and Arabidopsis thaliana. Dev. Growth Differ. 51, 769-775.
24. Del Bene, E, and Wyart, C. (2011). Optogenetics: a new enlightenment age for zebrafish neurobiology. Dev. Neurobiol. 72,404-414.
25. Del Bene, E, Wyart, C, Robles, E., Iran, A., Looger, L, Scott, E. K., Isacoff, E. Y., and Baier, H. (2010). Filtering of visual information in the tectum by an identified neural circuit. Science 330, 669-673.
26. Driever, W., Solnica-Krezel, L., Shier, A. E, Neuhaus, S. C. E, Malicki, J., Stemple, D. L., Stanier, D. Y. R., Zwartkruis, E, Abdelilah, S., Rangini, Z., Belak, J., and Boggs, C. (1996). A genetic screen for mutations affecting embryogene-sis in zebrafish. Development 123, 37-46.
27. Facchin, L., Burgess, H. A., Siddiqi, M., Granato, M., and Halpern, M. E. (2009). Determining the function of zebrafish epithalamic asymmetry. Philos. Trans. R. Soc. Lond. B Biol. Set. 364, 1021-1032.
28. Forel, A. (1872). Beitrage zur kennt-niss des thalamus opticus und der ihn umgebenden gebilde bei den saugethieren. Sitzber. k. Akad. Wiss. Wien. 65-66,25-58.
29. Gamse, J. T., Kuan, Y. S., Macu-rak, M., Brosamle, C, Thisse, B., Thisse, C, and Halpern, M. E. (2005). Directional asymmetry of the zebrafish epithalamus guides dorsoventral innervation of the midbrain target. Development 132, 4869-4881.
30. Gamse, J. T., Thisse, C, Thisse, B., and Halpern, M. E. (2003). The para-pineal mediates left-right asymmetry in the zebrafish diencephalon. Development 130, 1059-1068.
31. Gerlai, R. (2010). High-throughput behavioral screens: the first step towards finding genes involved in vertebrate brain function using zebrafish. Molecules 15, 2609-2622.
32. Goronowitsch, N. (1883). Das gehirn und die cranialnerven von Acipenser ruthenus. Morphol. Jahrb. 13, 427-574.
33. Guglielmotti, V., and Cristino, L. (2006). The interplay between the pineal complex and the habenular nuclei in lower vertebrates in the context of the evolution of cerebral asymmetry. Brain Res. Bull. 69, 475-488.
34. Guillery, R. W. (1959). Afferent fibers to the dorso-medial thalamic nucleus in the cat. J. Anat. 93, 403-419.
35. Gutierrez-Ibanez, C, Reddon, A. R., Kreuzer, M. B., Wylie, D. R., and Hurd, P. L. (2011). Variation in asymmetry of the habenular nucleus correlates with behavioural asymmetry in a cichlid fish. Behav. Brain Res. 221, 189-196.
36. Halpern, M. E., Liang, J. O., and Gamse, J. T. (2003). Leaning to the left: laterality in the zebrafish forebrain. Trends Neurosci. 26, 308-313.
37. Hamada, H., Meno, C, Watanabe, D., and Saijoh, Y. (2002). Establishment of vertebrate left-right asymmetry. Nat. Rev. Genet. 3,103-113.
38. Hamill, G. S., and Lenn, N. J. (1984). The subnuclear organization of the rat interpeduncular nucleus: a light and electron microscopic study. J. Comp. Neurol. 222, 396-408.
39. Hattori, T., McGeer, E. G., Singh, V. K., and McGeer, P. L. (1977). Cholinergic synapse of the interpeduncular nucleus. Exp. Neurol. 55, 666-679.
40. Heisenberg, C. P., Houart, C, Take-uchi, M., Rauch, G. J., Young, N., Coutinho, P., Masai, I., Caneparo, L., Concha, M. L, Geisler, R., Dale, T. C, Wilson, S. W., and Stemple, D. L. (2001). A mutation in the Gsk3-binding domain of zebrafish mas-terblind/axinl leads to a fate transformation of telencephalon and eyes to diencephalon. Genes Dev. 15, 1427-1434.
41. Helmchen, E, and Denk, W. (2005). Deep tissue two-photon microscopy. Nat. Methods 2, 932-940.
42. Helmstaedter, M., Briggman, K. L., and Denk, W. (2008). 3D structural imaging of the brain with photons and electrons. Curr. Opin. Neurobiol. 18,633-641.
43. Hendricks, M., and Jesuthasan, S. (2007). Asymmetric innervation of the habenula in zebrafish. J. Comp. Neurol. 502,611-619.
44. Herkenham, M., and Nauta, W. J. H. (1977). 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. 173, 123-146.
45. Higashijima, S., Masino, M. A., Mandel, G., and Fetcho, J. R. (2003). Imaging neuronal activity during zebrafish behavior with a genetically encoded calcium indicator. J. Neurophysiol. 90,3986-3997.
46. Hikosaka, O. (2010). The habenula: from stress evasion to value-based decision-making. Nat. Neurosci. 11, 503-513.
47. Inbal, A., Kim, S. H., Shin, J., and Solnica-Krezel, L. (2007). Six3 represses nodal activity to establish early brain asymmetry in zebrafish. Neuron 55, 407-415.
48. Jhou, T. C, Fields, H. L, Baxter, M. G., Saper, C. B., and Holland, P. C. (2009a). The rostromedial tegmen-tal nucleus (RMTg), a GABAergic afferent to midbrain dopamine neurons, encodes aversive stimuli and inhibits motor responses. Neuron 61, 786-800.
49. Jhou, T. C, Geisler, S., Marinelli, M., DeGarmo, B., and Zahm, D. S. (2009b). The mesopontine rostromedial tegmental nucleus: a structure targeted by the lateral habenula that projects to the ventral tegmental area of Tsai and substan-tia nigra compacta. J. Comp. Neurol. 513,566-596.
50. Kamei, M.,and Weinstein, B. M. (2005). Long-term time-lapse fluorescence imaging of developing zebrafish. Zebrafish 2, 113-123.
51. Kamei, Y, Suzuki, M., Watanabe, K., Fujimori, K., Kawasaki, T., Deguchi, T., Yoneda, Y, Todo, T., Takagi, S., Funatsu, T., and Yuba, S. (2009). Infrared laser-mediated gene induction in targeted single cells in vivo. Nat. Methods 6, 79-81.
52. Kuhar, M. J., DeHaven, R. N., Yama-mura, H. I., Rommel-Spacher, H., and Simon, J. R. (1975). Further evidence for cholinergic habenulo-interpeduncular neurons: pharma-cologic and functional characteristics. Brain Res. 97, 265-275.
53. Lee, A., Mathuru, A. S., Teh, C, Kibat, C, Korzh, V., Penney, T. B., and Jesuthasan, S. (2010). The habenula prevents helpless behavior in larval zebrafish. Curr. Biol. 20, 1-6.
54. Lenn, N. J. (1976). Synapses in the interpeduncular nucleus: Electron microscopy of normal and habenula lesioned rats. J. Comp. Neurol. 166, 73-100.
55. Li, J., Mack, J. A., Souren, M., Yaksi, E., Higashijima, S., Mione, M., Fetcho, J. R.,and Friedrich, R. W (2005). Early development of functional spatial maps in the zebrafish olfactory bulb. J. Neurosci. 25, 5784-5795.
56. Livet, J., Weissman, T. A., Kang, H., Draft, R. W, Lu, J., Bennis, R. A., Sanes, J. R., and Lichtman, J. W (2007). Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 450, 56-62.
57. Milhaud, M., and Pappas, G. D. (1966). The fine structure of neurons and synapses of the habenula of the cat with special reference to subjunctional bodies. Brain Res. 3, 158-173.
58. Mitchell, R. (1963). Connections of the habenula and of the interpeduncular nucleus in the cat. J. Comp. Neurol. 121,441-457.
59. Miyasakan, N., Morimoto, K., Tsub-okawa, T., Higashijima, S., Okamoto, H., and Yoshihara, Y (2009). From the olfactory bulb to higher brain centers: genetic visualization of secondary olfactory pathways in zebrafish. J. Neurosci. 30,1566-1574.
60. Morgane, P. J., Galler, J. R., and Mokler, D. J. (2005). A review of systems and networks of the limbic forebrain/limbic midbrain. Prog. Neurobiol. 75, 143-160.
61. Naumann, E. A., Kampff, A. R., Prober, D. A., Schier, A. F., and Engert, F. (2010). Monitoring neural activity with bioluminescence during nat ural behavior. Nat. Neurosci. 13, 513-520.
62. Pan, Y A., Livet, J., Sanes, J. R., Lichtman, J. W, and Schier, A. E (2011). "Multicolor brainbow imaging in zebrafish," in Imaging in Developmental Biology: A Laboratory Manual, eds R. Wong and J. Sharpe (Cold Spring Harbor: Cold Spring Harbor Laboratory Press), 191-198.
63. Pierce, E. T., Foote, W E., and Hobson, J. A. (1976). The efferent connection of the nucleus raphe dorsalis. Brain Res. 107,137-144.
64. Powell, E. W. (1968). Septohabenular connections in the rat, cat and monkey. J. Comp. Neurol. 134, 145-150.
65. Regan, J. C, Concha, M. L., Roussigne, M., Russell, C, and Wilson, S. W. (2009). An Fgf8-dependent bistable cell migratory event establishes CNS asymmetry. Neuron 61, 27-34.
66. Rodriguez-Esteban, C, Tsukui, T., Yonei, S., Magallon, J., Tamura, K., and Belmonte, J. C. I. (1999). The T-box genes Tbx4 and Tbx5 regulate limb outgrowth and identity. Nature 398,814-818.
67. Roussigne, M., Bianco, I. H., Wilson, S. W, and Blader, P. (2009). Nodal signalling imposes left-right asymmetry upon neurogenesis in the habenular nuclei. Development 136, 1549-1557.
68. Roussigne, M., Blader, P., and Wilson, S.W (2011). The zebrafish epithalamus clears a path through the complexity of brain lateralization. Dev. Neurobiol. 72,269-281.
69. Signore, I. A., Guerrero, N., Loosli, E, Colombo, A., Villalon, A., Wit-tbrodt, J., and Concha, M. L. (2009). Zebrafish and medaka: model organisms for a comparative developmental approach of brain asymmetry. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 991-1003.
70. Smaha, L. A., and Kaelber, W W. (1973). Efferent fiber projections of the habenula and the interpeduncular nucleus. An experimental study in the opossum and cat. Exp. Brain Res. 16,291-308.
71. Snelson, C. D., Santhakumar, K., Halpern, M. E., and Gamse, J. T. (2008). Tbx2b is required for the development of the para-pineal organ. Development 135, 1693-1702.
72. Squirrell, J. M., Wokosin, D. L., White, J. G., and Bavister, B. D. (1999). Long-term two-photon fluorescence imaging of mammalian embryos without compromising viability. Nat. Biotechnol. 17, 763-767.
73. Staines, W. A., Nagy, J. I., Vincent, S. R., and Fibiger, H. C. (1980). Neuro-transmitters contained in the effer-ents of the striatum. Brain Res. 194, 391-402.
74. Subach, O. M., Patterson, G. H., Ting, L.-M., Wang, Y., Con-deelis, J. S., and Verkhusha, V. V. (2011). A photoswitchable orange-to-far-red fluorescent protein, PSmOrange. Nat. Methods 8, 771-777.
75. Sumbre, G., Muto, A., Baier, H., and Poo, M. M. (2008). Entrained rhythmic activities of neuronal ensembles as perceptual memory of time interval. Nature 456,102-106.
76. Sutherland, R. J. (1982). The dorsal diencephalic conduction system: a review of the anatomy and functions of the habenular complex. Neurosci. Biobehav. Rev. 6, 1-13.
77. Svoboda, K., and Yasuda, R. (2006). Principles of two-photon excitation microscopy and its applications to neuroscience. Neuron 50, 823-839.
78. Tsutsui, H., Higashijima, S. I., Miyawaki, A., and Okamura, Y. (2010). Visualizing voltage dynamics in zebraflsh heart. J. Physiol. (Lond.) 588,2017-2021.
79. Vallortigara, G., and Rogers, L. J. (2005). Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav. Brain Sci. 28, 575-633.
80. Vallortigara, G., Rogers, L. J., and Bisazza, A. (1999). Possible evolutionary origins of cognitive brain lateralization. Brain Res. Brain Res. Rev. 30, 164-175.
81. von Staden, H. (2007). Herophilus: The Art of Medicine in Early Alexandria. Cambridge: University Press.
82. Wree, A., Zilles, K., and Schleicher, A. (1981). Growth of fresh volumes and spontaneous cell death in the nuclei habenulae of albino rats during ontogenesis. Anat. Embryol. (Berl.) 161,419-431.
83. Zhong, H., and Lin, S. (2011). Chemical screening with zebraflsh embryos. Methods Mol. Biol. 716, 193-205.
84. Zyo, K., Oki, T., and Ban, T. (1963). Experimental studies on the medial forebrain bundle, medial longitudinal fasciculus and supraoptic decus-sations in the rabbit. Med. J. Osaka Univ. 13,193-239.