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PMID: 17507550 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Genetic single-cell mosaic analysis implicates ephrinB2 reverse signaling in projections from the posterior tectum to the hindbrain in zebrafish.

Sato T, Hamaoka T, Aizawa H, Hosoya T, Okamoto H

Abstract

The optic tectum is a visual center in vertebrates. It receives topographically ordered visual inputs from the retina in the superficial layers and then sends motor outputs from the deeper layers to the premotor reticulospinal system in the hindbrain. Although the topographic patterns of the retinotectal projection are well known, it is not yet well understood how tectal efferents in the tectobulbar tract project to the hindbrain. The retinotectal and the tectobulbar projections were visualized in a zebrafish stable transgenic line Tg(brn3a-hsp70:GFP). Using a single-neuron labeling system in combination with the cre/loxP and Gal4/UAS systems, we showed that the tectal neurons that projected to rhombomeres 2 and 6 were distributed with distinctive patterns along the anterior-posterior axis. Furthermore, we found that ephrinB2a was critically involved in increasing the probability of neurons projecting to rhombomere 2 through a reverse signaling mechanism. These results may provide a neuroanatomical and molecular basis for the motor command map in the tectum.

MeSH Terms
Animals Animals, Genetically Modified Ephrin-B2/genetics,physiology Mosaicism/embryology Neurons/cytology,physiology Rhombencephalon/cytology,embryology,physiology Signal Transduction/genetics Superior Colliculi/cytology,embryology,physiology Visual Pathways/cytology,embryology,physiopathology Zebrafish Zebrafish Proteins/biosynthesis,genetics
Chemicals
Ephrin-B2 Zebrafish Proteins
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Sato Tomomi
Laboratory for Developmental Gene Regulation, Brain Science Institute, RIKEN, Wako, Saitama 351-0198, Japan.
Hamaoka Takanori
Aizawa Hidenori
Hosoya Toshihiko
Okamoto Hitoshi
References (43)
43 references, click to expand
  1. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis.
    Neuron. 1999 Mar;22(3):451-61 PMID: 10197526
  2. Laser ablations reveal functional relationships of segmental hindbrain neurons in zebrafish.
    Neuron. 1999 Jun;23(2):325-35 PMID: 10399938
  3. Tectotectal connectivity in goldfish.
    J Comp Neurol. 1999 Aug 30;411(3):455-71 PMID: 10413779
  4. Laser-induced gene expression in specific cells of transgenic zebrafish.
    Development. 2000 May;127(9):1953-60 PMID: 10751183
  5. Eph signalling functions downstream of Val to regulate cell sorting and boundary formation in the caudal hindbrain.
    Development. 2001 Feb;128(4):571-80 PMID: 11171340
  6. Tracing transgene expression in living zebrafish embryos.
    Dev Biol. 2001 May 15;233(2):329-46 PMID: 11336499
  7. Morphogenesis of prechordal plate and notochord requires intact Eph/ephrin B signaling.
    Dev Biol. 2001 Jun 15;234(2):470-82 PMID: 11397014
  8. Eye and head movements evoked by electrical stimulation of monkey superior colliculus.
    Exp Brain Res. 1975 Jul 11;23(1):103-12 PMID: 1149845
  9. Evidence for a widespread brain stem escape network in larval zebrafish.
    J Neurophysiol. 2002 Jan;87(1):608-14 PMID: 11784774
  10. Constructing the hindbrain: insights from the zebrafish.
    Dev Dyn. 2002 May;224(1):1-17 PMID: 11984869
  11. Topographic mapping in dorsoventral axis of the Xenopus retinotectal system depends on signaling through ephrin-B ligands.
    Neuron. 2002 Aug 1;35(3):461-73 PMID: 12165469
  12. Connectivity of the goldfish optic tectum with the mesencephalic and rhombencephalic reticular formation.
    Exp Brain Res. 2003 Jul;151(1):123-35 PMID: 12748838
  13. In vivo imaging of synapse formation on a growing dendritic arbor.
    Nat Neurosci. 2004 Mar;7(3):254-60 PMID: 14758365
  14. EphrinB2a in the zebrafish retinotectal system.
    J Neurobiol. 2004 Apr;59(1):57-65 PMID: 15007827
  15. Common sensory inputs and differential excitability of segmentally homologous reticulospinal neurons in the hindbrain.
    J Neurosci. 2004 Mar 31;24(13):3199-209 PMID: 15056699
  16. Ephrin-B2 reverse signaling is required for axon pathfinding and cardiac valve formation but not early vascular development.
    Dev Biol. 2004 Jul 15;271(2):263-71 PMID: 15223333
  17. Ephrin signaling in vivo: look both ways.
    Dev Dyn. 2005 Jan;232(1):1-10 PMID: 15580616
  18. Mechanisms of retinotopic map development: Ephs, ephrins, and spontaneous correlated retinal activity.
    Prog Brain Res. 2005;147:43-65 PMID: 15581697
  19. Transgene manipulation in zebrafish by using recombinases.
    Methods Cell Biol. 2004;77:363-79 PMID: 15602922
  20. Laterotopic representation of left-right information onto the dorso-ventral axis of a zebrafish midbrain target nucleus.
    Curr Biol. 2005 Feb 8;15(3):238-43 PMID: 15694307
  21. Functional imaging reveals rapid development of visual response properties in the zebrafish tectum.
    Neuron. 2005 Mar 24;45(6):941-51 PMID: 15797554
  22. Mosaic analysis with double markers in mice.
    Cell. 2005 May 6;121(3):479-92 PMID: 15882628
  23. alx, a zebrafish homolog of Chx10, marks ipsilateral descending excitatory interneurons that participate in the regulation of spinal locomotor circuits.
    J Neurosci. 2006 May 24;26(21):5684-97 PMID: 16723525
  24. Role of the Mauthner cell in sensorimotor integration by the brain stem escape network.
    Brain Behav Evol. 1991;37(5):272-85 PMID: 1933251
  25. Event or emergency? Two response systems in the mammalian superior colliculus.
    Trends Neurosci. 1989 Apr;12(4):137-47 PMID: 2470171
  26. Expression of a large family of POU-domain regulatory genes in mammalian brain development.
    Nature. 1989 Jul 6;340(6228):35-41 PMID: 2739723
  27. Characterisation of five novel zebrafish Eph-related receptor tyrosine kinases suggests roles in patterning the neural plate.
    Dev Genes Evol. 1997 May;206(8):515-531 PMID: 27747378
  28. Retinotopic organization of the developing retinotectal projection in the zebrafish embryo.
    J Neurosci. 1988 Dec;8(12):4513-30 PMID: 2848935
  29. Segmental homologies among reticulospinal neurons in the hindbrain of the zebrafish larva.
    J Comp Neurol. 1986 Sep 8;251(2):147-59 PMID: 3782495
  30. Motor responses to localized electrical stimulation of the tectum in the freshwater perch (Perca fluviatilis).
    Neuroscience. 1986 Dec;19(4):1381-91 PMID: 3822126
  31. Functional anatomy of the tectum mesencephali of the goldfish. An explorative analysis of the functional implications of the laminar structural organization of the tectum.
    Brain Res. 1983 Dec;287(3):247-97 PMID: 6362772
  32. Visual-motor function of the primate superior colliculus.
    Annu Rev Neurosci. 1980;3:189-226 PMID: 6774653
  33. The Brn-3 family of POU-domain factors: primary structure, binding specificity, and expression in subsets of retinal ganglion cells and somatosensory neurons.
    J Neurosci. 1995 Jul;15(7 Pt 1):4762-85 PMID: 7623109
  34. Stages of embryonic development of the zebrafish.
    Dev Dyn. 1995 Jul;203(3):253-310 PMID: 8589427
  35. The development of vision in the zebrafish (Danio rerio).
    Dev Biol. 1996 Dec 15;180(2):646-63 PMID: 8954734
  36. valentino: a zebrafish gene required for normal hindbrain segmentation.
    Development. 1996 Dec;122(12):3981-90 PMID: 9012518
  37. Tectal codification of eye movements in goldfish studied by electrical microstimulation. f.
    Neuroscience. 1997 May;78(1):271-88 PMID: 9135107
  38. Novel Eph-family receptor tyrosine kinase is widely expressed in the developing zebrafish nervous system.
    Dev Dyn. 1997 Jun;209(2):166-81 PMID: 9186052
  39. The development of eye movements in the zebrafish (Danio rerio).
    Dev Psychobiol. 1997 Dec;31(4):267-76 PMID: 9413674
  40. The ephrins and Eph receptors in neural development.
    Annu Rev Neurosci. 1998;21:309-45 PMID: 9530499
  41. Tail and eye movements evoked by electrical microstimulation of the optic tectum in goldfish.
    Exp Brain Res. 1998 Jun;120(3):291-305 PMID: 9628416
  42. Eph signaling is required for segmentation and differentiation of the somites.
    Genes Dev. 1998 Oct 1;12(19):3096-109 PMID: 9765210
  43. Morphology, axonal projection pattern, and response types of tectal neurons in plethodontid salamanders. II: intracellular recording and labeling experiments.
    J Comp Neurol. 1999 Feb 22;404(4):489-504 PMID: 9987993
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2007-05-16
Pages
5271-9
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6672335
Subset
IM
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