Cerebellar output in zebrafish: An analysis of spatial patterns and topography in eurydendroid cell projections

Frontiers in Neural Circuits

Volumn , Issue MAR, 2013, Pages

  Heap, Lucy ^a   Goh, Chi Ching ^a,b   Kassahn, Karin S ^a   Scott, Ethan K ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Cerebellum; Eurydendroid; Gal4; Optic tectum; Thalamus; Topography; Zebrafish

Indexed keywords

GREEN FLUORESCENT PROTEIN; TRANSCRIPTION FACTOR GAL4;

ANIMAL CELL; ARTICLE; BRAIN FUNCTION; CAUDAL TECTUM; CELL LABELING; CELL SUBPOPULATION; CELLULAR DISTRIBUTION; CEREBELLAR OUTPUT; CEREBELLUM; CONNECTOME; CRISTA CEREBELLARIS; EMBRYO; EURYDENDROID CELL; LARVA; LATERAL CORPUS CEREBELLI; NERVE CELL; NERVE PROJECTION; NERVOUS SYSTEM PARAMETERS; NEURITE; NEUROANATOMICAL TRACT TRACING; NONHUMAN; PERIKARYON; PROTEIN EXPRESSION; PURKINJE CELL; RHOMBENCEPHALON; ROSTRAL TECTAL NEUROPIL; ROSTRAL TECTUM; SYNAPTOSOME; TECTUM; THALAMUS; ZEBRA FISH;

EID: 84875014070     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2013.00053     Document Type: Article

References (92)

1. Ahrens, M.B., Li, J.M., Orger, M.B., Robson, D.N., Schier, A.F., Engert, F., and Portugues, R. (2012). Brain-wide neuronal dynamics during motor adaptation in zebrafish. Nature 485, 471-477.
2. Aizenberg, M., and Schuman, E.M. (2011). Cerebellar-dependent learning in larval zebrafish. JNeurosci 31, 8708-8712.
3. Albus, J.S. (1971). A theory of cerebellar function. Mathematical Biosciences 10, 25-61.
4. 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 Sci U S A 99, 12651-12656.
5. Andrezik, J.A., Dormer, K.J., Foreman, R.D., and Person, R.J. (1984). Fastigial nucleus projections to the brain stem in beagles: pathways for autonomic regulation. Neuroscience 11, 497-507.
6. Armstrong, B.D., and Harvey, R.J. (1966). Responses in the inferior olive to stimulation of the cerebellar and cerebral cortices in the cat. J Physiol 187, 553-574.
7. Asakawa, K., Suster, M.L., Mizusawa, K., Nagayoshi, S., Kotani, T., Urasaki, A., Kishimoto, Y., Hibi, M., and Kawakami, K. (2008). Genetic dissection of neural circuits by Tol2 transposon-mediated Gal4 gene and enhancer trapping in zebrafish. Proc Natl Acad Sci USA 105, 1255-1260.
8. Aumann, T.D., Rawson, J.A., Finkelstein, D.I., and Horne, M.K. (1994). Projections from the lateral and interposed cerebellar nuclei to the thalamus of the rat: a light and electron microscopic study using single and double anterograde labelling. J Comp Neurol 349,165-181.
9. Bae, Y.K., Kani, S., Shimizu, T., Tanabe, K., Nojima, H., Kimura, Y., Higashijima, S., and Hibi, M. (2009). Anatomy of zebrafish cerebellum and screen for mutations affecting its development. Dev Biol 330, 406-426.
10. Bass, A.H. (1982) Evolution of the vestibulolateral lobe of the cerebellum in electroreceptive and nonelectroreceptive teleosts. J Morphology 174:335-348
11. Becanovic, K., Pouladi, M.A., Lim, R.S., Kuhn, A., Pavlidis, P., Luthi-Carter, R., Hayden, M.R., and Leavitt, B.R. (2010). Transcriptional changes in Huntington disease identified using genome-wide expression profiling and cross-platform analysis. Hum Mol Genet 19, 1438-1452.
12. Blakemore, S.J., Wolpert, D.M., and Frith, C.D. (1998). Central cancellation of selfproduced tickle sensation. Nat Neurosci 1, 635-640.
13. Brand, A.H., and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
14. Carey, M.R. (2011). Synaptic mechanisms of sensorimotor learning in the cerebellum. Curr Opin Neurobiol 21, 609-615.
15. Collin, S.P., and Pettigrew, J.D. (1988). Retinal topography in reef teleosts. I.Some species with well-developed areae but poorly-developed streaks. Brain Behav Evol 31, 269-282.
16. Davison, J.M., Akitake, C.M., Goll, M.G., Rhee, J.M., Gosse, N., Baier, H., Halpern, M.E., Leach, S.D., and Parsons, M.J. (2007). Transactivation from Gal4-VP16 transgenic insertions for tissue-specific cell labeling and ablation in zebrafish. Developmental Biology 304, 811-824.
17. Del Bene, F., Wyart, C., Robles, E., Tran, 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.
18. Distel, M., Wullimann, M.F., and Koster, R.W. (2009). Optimized Gal4 genetics for permanent gene expression mapping in zebrafish. Proc Natl Acad Sci USA 106, 13365-13370.
19. Donarum, E.A., Stephan, D.A., Larkin, K., Murphy, E.J., Gupta, M., Senephansiri, H., Switzer, R.C., Pearl, P.L., Snead, O.C., Jakobs, C., and Gibson, K.M. (2006). Expression profiling reveals multiple myelin alterations in murine succinate semialdehyde dehydrogenase deficiency. JInheritMetab Dis 29, 143-156.
20. Dow, R.S., and Moruzzi, G. (1958). The Physiology and Pathology of the Cerebellum. Minneapolis, United States of America: The University of Minnesota Press.
21. Emmenlauer, M., Ronneberger, O., Ponti, A., Schwarb, P., Griffa, A., Filippi, A., Nitschke, R., Driever, W., and Burkhardt, H. (2009). XuvTools: free, fast and reliable stitching of large 3D datasets. JMicrosc 233, 42-60.
22. Feng, G., Mellor, R.H., Bernstein, M., Keller-Peck, C., Nguyen, Q.T., Wallace, M.,Nerbonne, J.M., Lichtman, J.W., and Sanes, J.R. (2000). Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28, 41-51.
23. Fiebig, E., Ebbesson, S.O.E., and Meyerm, D.L. (1983). Afferent connections of the optic tectum in the piranha (Serrasalmus nattereri). Cell Tissue Research 231, 55-72.
24. Finger, T.E. (1983). Organization of the teleost cerebellum. Fish Neurobiology 1, 261-284.
25. Folgueira, M., Anadon, R., and Yanez, J. (2006). Afferent and efferent connections of the cerebellum of a salmonid, the rainbow trout (Oncorhynchus mykiss): a tract-tracing study. J Comp Neurol 497, 542-565.
26. Folgueira, M., Sueiro, C., Rodriguez-Moldes, I., Yanez, J., and Anadon, R. (2007).Organization of the torus longitudinalis in the rainbow trout (Oncorhynchus mykiss): an immunohistochemical study of the GABAergic system and a DiI tract-tracing study. J Comp Neurol 503, 348-370.
27. Friedrich, R.W., Jacobson, G.A., and Zhu, P. (2010). Circuit neuroscience in zebrafish. Curr Biol 20, R371-381.
28. Gallay, M.N., Jeanmonod, D., Liu, J., and Morel, A. (2008). Human pallidothalamic and cerebellothalamic tracts: anatomical basis for functional stereotactic neurosurgery. Brain Struct Funct 212, 443-463.
29. Glickstein, M., Sultan, F., and Voogd, J. (2011). Functional localization in the cerebellum. Cortex 47, 59-80.
30. Hepp, K., Henn, V., and Jaeger, J. (1982). Eye movement related neurons in the cerebellar nuclei of the alert monkey. Exp Brain Res 45, 253-264.
31. Hibi, M., and Shimizu, T. (2010). Development of the cerebellum and cerebellar neural circuits. Developmental Neurobiology, 282-301.
32. Hoebeek, F.E., Witter, L., Ruigrok, T.J., and De Zeeuw, C.I. (2010). Differential olivocerebellar cortical control of rebound activity in the cerebellar nuclei. Proc Natl Acad Sci USA 107, 8410-8415.
33. Ikenaga, T., Yoshida, M., and Uematsu, K. (2002). Efferent connections of the cerebellum of the goldfish, Carassius auratus. Brain Behav Evol 60, 36-51.
34. Ikenaga, T., Yoshida, M., and Uematsu, K. (2005). Morphology and immunohistochemistry of efferent neurons of the goldfish corpus cerebelli. J Comp Neurol 487, 300-311.
35. Ikenaga, T., Yoshida, M., and Uematsu, K. (2006). Cerebellar efferent neurons in teleost fish. Cerebellum 5, 268-274.
36. Ito, H., and Yamamoto, N. (2009). Non-laminar cerebral cortex in teleost fishes? Biol Lett 5, 117-121.
37. Jay, M.F., and Sparks, D.L. (1987a). Sensorimotor integration in the primate superior colliculus. I. Motor convergence. J Neurophysiol 57, 22-34.
38. Jay, M.F., and Sparks, D.L. (1987b). Sensorimotor integration in the primate superior colliculus. II. Coordinates of auditory signals. J Neurophysiol 57, 35-55.
39. Kani, S., Bae, Y.K., Shimizu, T., Tanabe, K., Satou, C., Parsons, M.J., Scott, E.,Higashijima, S., and Hibi, M. (2010). Proneural gene-linked neurogenesis in zebrafish cerebellum. Dev Biol 343, 1-17.
40. Kawakami, K. (2004). Transgenesis and gene trap methods in zebrafish by using the Tol2 transposable element. Methods Cell Biol 77, 201-222.
41. Kinoshita, M., Ito, E., Urano, A., Ito, H., and Yamamoto, N. (2006). Periventricular efferent neurons in the optic tectum of rainbow trout. J Comp Neurol 499, 546-564.
42. Kotani, T., Nagayoshi, S., Urasaki, A., and Kawakami, K. (2006). Transposon-mediated gene trapping in zebrafish. Methods 39, 199-206.
43. Kwan, K.M., Fujimoto, E., Grabher, C., Mangum, B.D., Hardy, M.E., Campbell, D.S.,Parant, J.M., Yost, H.J., Kanki, J.P., and Chien, C.B. (2007). The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev Dyn 236, 3088-3099.
44. Laplante, M., Kikuta, H., Konig, M., and Becker, T.S. (2006). Enhancer detection in the zebrafish using pseudotyped murine retroviruses. Methods 39, 189-198.
45. Li, L., Tasic, B., Micheva, K.D., Ivanov, V.M., Spletter, M.L., Smith, S.J., and Luo, L.(2010). Visualizing the distribution of synapses from individual neurons in the mouse brain. PLoS One 5.
46. Lister, J.A., Robertson, C.P., Lepage, T., Johnson, S.L., and Raible, D.W. (1999). Nacre encodes a zebrafish microphthalmia-related protein that regulates neural-crest- derived pigment cell fate. Development 126, 3757-3767.
47. 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.
48. Longair, M.H., Baker, D.A., and Armstrong, J.D. (2011). Simple Neurite Tracer: open source software for reconstruction, visualization and analysis of neuronal processes. Bioinformatics 27, 2453-2454.
49. Luo, L., Callaway, E.M., and Svoboda, K. (2008). Genetic dissection of neural circuits. Neuron 57, 634-660.
50. Mcclenahan, P., Troup, M., and Scott, E.K. (2012). Fin-tail coordination during escape and predatory behavior in larval zebrafish. PLoS One 7, e32295.
51. Mcfarland, K.A., Topczewska, J.M., Weidinger, G., Dorsky, R.I., and Appel, B. (2008). Hh and Wnt signaling regulate formation of olig2+ neurons in the zebrafish cerebellum. Dev Biol 318, 162-171.
52. Meek, J., Nieuwenhuys, R., and Elsavier, D. (1986a) Afferent and efferent connections of cerebellar lobe C1 of the mormyrid fish Gnathonemuspetersi: An HRP study. J Comp Neurol 245, 319-341
53. Meek, J., Nieuwenhuys, R., and Elsevier, D. (1986b). Afferent and efferent connections of cerebellar lobe C3 of the mormyrid fish Gnathonemus petersi: an HRP study. J Comp Neurol 245, 342-358.
54. Meyer, M.P., and Smith, S.J. (2006). Evidence from in vivo imaging that synaptogenesis guides the growth and branching of axonal arbors by two distinct mechanisms. J Neurosci 26, 3604-3614.
55. Miall, R.C., Weir, D.J., Wolpert, D.M., and Stein, J.F. (1993). Is the cerebellum a smith predictor? J Mot Behav 25, 203-216.
56. Miles, F.A., and Lisberger, S.G. (1981). Plasticity in the vestibulo-ocular reflex: a new hypothesis. Annu Rev Neurosci 4, 273-299.
57. Miyamura, Y., and Nakayasu, H. (2001). Zonal distribution of Purkinje cells in the zebrafish cerebellum: analysis by means of a specific monoclonal antibody. Cell Tissue Res 305, 299-305.
58. Mueller, T. (2012). What is the thalamus in zebrafish? Frontiers in Neuroscience 6, 64.
59. Murakami, T., and Morita, Y. (1987). Morphology and distribution of the projection neurons in the cerebellum in a teleost, Sebastiscus marmoratus. J Comp Neurol 256, 607-623.
60. Nederstigt, L.J., and Schellart, N.A. (1986). Acousticolateral processing in the torus semicircularis of the trout Salmo gairdneri. Pflugers Arch 406, 151-157.
61. Nevin, L.M., Robles, E., Baier, H., and Scott, E.K. (2010). Focusing on optic tectum circuitry through the lens of genetics. BMC Biol 8, 126.
62. Niell, C.M., Meyer, M.P., and Smith, S.J. (2004). In vivo imaging of synapse formation on a growing dendritic arbor. Nature Neuroscience 7, 254-260.
63. Northcutt, R.G. (2006). Connections of the lateral and medial divisions of the goldfish telencephalic pallium. J Comp Neurol 494, 903-943.
64. Northcutt, R.G. (2008). Forebrain evolution in bony fishes. Brain Res Bull 75, 191-205.
65. Palmer, A.R., and King, A.J. (1982). The representation of auditory space in the mammalian superior colliculus. Nature 299, 248-249.
66. Person, R.J., Andrezik, J.A., Dormer, K.J., and Foreman, R.D. (1986). Fastigial nucleus projections in the midbrain and thalamus in dogs. Neuroscience 18, 105-120.
67. Rupp, B., and Northcutt, R.G. (1998). The diencephalon and pretectum of the white sturgeon (Acipenser transmontanus): a cytoarchitectonic study. Brain Behav Evol 51, 239-262.
68. Sajovic, P., and Levinthal, C. (1982). Visual cells of zebrafish optic tectum: Mapping with small spots. Neuroscience 7, 2407-2426.
69. Sato, T., Hamaoka, T., Aizawa, H., Hosoya, T., and Okamoto, H. (2007). Genetic single-cell mosaic analysis implicates ephrinB2 reverse signaling in projections from the posterior tectum to the hindbrain in zebrafish. JNeurosci 27, 5271-5279.
70. Scheer, N., and Campos-Ortega, J.A. (1999). Use of the Gal4-UAS technique for targeted gene expression in the zebrafish. Mech Dev 80, 153-158.
71. Scott, E.K. (2009). The Gal4/UAS toolbox in zebrafish: new approaches for defining behavioral circuits. J Neurochem 110, 441-456.
72. Scott, E.K., and Baier, H. (2009). The cellular architecture of the larval zebrafish tectum, as revealed by gal4 enhancer trap lines. Front Neural Circuits 3, 13.
73. Scott, E.K., Mason, L., Arrenberg, A.B., Ziv, L., Gosse, N.J., Xiao, T., Chi, N.C., Asakawa, K., Kawakami, K., and Baier, H. (2007). Targeting neural circuitry in zebrafish using GAL4 enhancer trapping. NatMeth 4, 323-326.
74. Sedgwick, E.M., and Williams, T.D. (1967). Responses of single units in the inferior olive to stimulation of the limb nerves, peripheral skin receptors, cerebellum, caudate nucleus and motor cortex. J Physiol 189, 261-279.
75. Simmich, J., Staykov, E., and Scott, E. (2012). Zebrafish as an appealing model for optogenetic studies. Prog Brain Res 196, 145-162.
76. Simpson, H.D., Kita, E.M., Scott, E.K., and Goodhill, G.J. (2012). A quantitative analysis of branching, growth cone turning and directed growth in zebrafish retinotectal axon guidance. J Comp Neurol.
77. Sparks, D.L., and Hartwich-Young, R. (1989). The deep layers of the superior colliculus. Rev Oculomot Res 3, 213-255.
78. Stuermer, C.A. (1988). Retinotopic organization of the developing retinotectal projection in the zebrafish embryo. J Neurosci 8, 4513-4530.
79. Sultan, F., Augath, M., Hamodeh, S., Murayama, Y., Oeltermann, A., Rauch, A., and Thier, P. (2012). Unravelling cerebellar pathways with high temporal precision targeting motor and extensive sensory and parietal networks. Nat Commun 3, 924.
80. Szabo, T. (1983). Cerebellar pathways in the brain of the mormyrid teleost fish. Acta Morphol Hung 31, 219-234.
81. Thach, W.T. (1968). Discharge of Purkinje and cerebellar nuclear neurons during rapidly alternating arm movements in the monkey. J Neurophysiol 31, 785-797.
82. Thierry-Mieg, D., and Thierry-Mieg, J. (2006). AceView: a comprehensive cDNA-supported gene and transcripts annotation. Genome Biol 7 Suppl 1, S12 11-14.
83. Tseng, Y.W., Diedrichsen, J., Krakauer, J.W., Shadmehr, R., and Bastian, A.J. (2007). Sensory prediction errors drive cerebellum-dependent adaptation of reaching. J Neurophysiol 98, 54-62.
84. Volkmann, K., Rieger, S., Babaryka, A., and Koster, R.W. (2008). The zebrafish cerebellar rhombic lip is spatially patterned in producing granule cell populations of different functional compartments. Dev Biol 313, 167-180.
85. Westerfield, M. (2000). The zebrafish book. A guide for the laboratory use of zebrafish (Danio rerio). 4th ed. University of Oregon Press, Eugene.
86. Wullimann, M.F., and Mueller, T. (2004). Teleostean and mammalian forebrains contrasted: Evidence from genes to behavior. J Comp Neurol 475, 143-162.
87. Wullimann, M.F., and Northcutt, R.G. (1988). Connections of the corpus cerebelli in the green sunfish and the common goldfish: a comparison of perciform and cypriniform teleosts.Brain Behav Evol 32, 293-316.
88. Wyart, C., Del Bene, F., Warp, E., Scott, E.K., Trauner, D., Baier, H., and Isacoff, E.Y.(2009). Optogenetic dissection of a behavioural module in the vertebrate spinal cord. Nature 461, 407-410.
89. Xiao, T., Roeser, T., Staub, W., and Baier, H. (2005). A GFP-based genetic screen reveals mutations that disrupt the architecture of the zebrafish retinotectal projection. Development 132, 2955-2967.
90. Yamamoto, N., and Ito, H. (2005). Fiber connections of the anterior preglomerular nucleus in cyprinids with notes on telencephalic connections of the preglomerular complex. J Comp Neurol 491, 212-233.
91. Zapala, M.A., Hovatta, I., Ellison, J.A., Wodicka, L., Del Rio, J.A., Tennant, R., Tynan, W., Broide, R.S., Helton, R., Stoveken, B.S., Winrow, C., Lockhart, D.J., Reilly, J.F., Young, W.G., Bloom, F.E., Lockhart, D.J., and Barlow, C. (2005). Adult mouse brain gene expression patterns bear an embryologic imprint. Proc Natl Acad Sci U S A 102, 10357-10362.
92. Zhang, Y., Magnus, G., and Han V.Z. (2008). Local Circuitry in the Anterior Lateral Caudal Lobe of the Mormyrid Cerebellum: a Study of Intracellular Recording and Labelling. J. Comp Neurol 509, 1-22.