Growth cone and dendrite dynamics in zebrafish embryos: early events in synaptogenesis imaged in vivo

We used time-lapse fluorescence microscopy to observe the growth of Mauthner cell axons and their postsynaptic targets, the primary motor neurons, in spinal cords of developing zebrafish embryos. Upon reaching successive motor neurons, the Mauthner growth cone paused briefly before continuing along its path. Varicosities formed at regular intervals and were preferentially associated with the target regions of the primary motor neurons. In addition, the postsynaptic motor neurons showed highly dynamic filopodia, which transiently interacted with both the growth cone and the axon. Both Mauthner cell and motor neurons were highly active, each showing motility sufficient to initiate synaptogenesis.

[1]  H. Cline,et al.  Stabilization of dendritic arbor structure in vivo by CaMKII. , 1998, Science.

[2]  B. Mendelson.  Development of reticulospinal neurons of the zebrafish. I. Time of origin , 1986, The Journal of comparative neurology.

[3]  J. Fetcho,et al.  Identification of motoneurons and interneurons in the spinal network for escapes initiated by the mauthner cell in goldfish , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  Scott E. Fraser,et al.  Dynamic changes in optic fiber terminal arbors lead to retinotopic map formation: An in vivo confocal microscopic study , 1990, Neuron.

[5]  M. G. Honig,et al.  Fluorescent carbocyanine dyes allow living neurons of identified origin to be studied in long-term cultures , 1986, The Journal of cell biology.

[6]  K. Svoboda,et al.  Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. , 1999, Science.

[7]  J. Ngai,et al.  Pathfinding of Olfactory Neuron Axons to Stereotyped Glomerular Targets Revealed by Dynamic Imaging in Living Zebrafish Embryos , 1998, Neuron.

[8]  M. Westerfield,et al.  Function of identified motoneurones and co‐ordination of primary and secondary motor systems during zebra fish swimming. , 1988, The Journal of physiology.

[9]  W. Shoji,et al.  Zebrafish semaphorin Z1a collapses specific growth cones and alters their pathway in vivo. , 1998, Development.

[10]  Stephen J. Smith,et al.  Evidence for a Role of Dendritic Filopodia in Synaptogenesis and Spine Formation , 1996, Neuron.

[11]  R J Kaethner,et al.  Dynamics of terminal arbor formation and target approach of retinotectal axons in living zebrafish embryos: a time-lapse study of single axons , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  N. Patel,et al.  Fasciclin IV: Sequence, expression, and function during growth cone guidance in the grasshopper embryo , 1992, Neuron.

[13]  F. Murakami,et al.  Preferential Termination of Corticorubral Axons on Spine-Like Dendritic Protrusions in Developing Cat , 1997, The Journal of Neuroscience.

[14]  C. Kimmel,et al.  Stages of embryonic development of the zebrafish , 1995, Developmental dynamics : an official publication of the American Association of Anatomists.

[15]  W. K. Metcalfe,et al.  Segmental homologies among reticulospinal neurons in the hindbrain of the zebrafish larva , 1986, The Journal of comparative neurology.

[16]  F. Murakami,et al.  Developing corticorubral axons of the cat form synapses on filopodial dendritic protrusions , 1992, Neuroscience Letters.

[17]  J. Fiala,et al.  Synaptogenesis Via Dendritic Filopodia in Developing Hippocampal Area CA1 , 1998, The Journal of Neuroscience.

[18]  W. K. Metcalfe,et al.  Brain neurons which project to the spinal cord in young larvae of the zebrafish , 1982, The Journal of comparative neurology.

[19]  M. Westerfield,et al.  Pathway selection by growth cones of identified motoneurones in live zebra fish embryos , 1986, Nature.

[20]  C. Holt,et al.  Retinal axons with and without their somata, growing to and arborizing in the tectum of Xenopus embryos: a time-lapse video study of single fibres in vivo. , 1987, Development.

[21]  P. Drapeau,et al.  Time course of the development of motor behaviors in the zebrafish embryo. , 1998, Journal of neurobiology.

[22]  M. Westerfield,et al.  Development and axonal outgrowth of identified motoneurons in the zebrafish , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  M. Celio,et al.  Ultrastructure of the Mauthner axon collateral and its synapses in the goldfish spinal cord , 1979, Journal of neurocytology.

[24]  D. Raible,et al.  Collapsin: A protein in brain that induces the collapse and paralysis of neuronal growth cones , 1993, Cell.

[25]  Scott E. Fraser,et al.  Rapid remodeling of retinal arbors in the tectum with and without blockade of synaptic transmission , 1994, Neuron.

[26]  Stephen J. Smith,et al.  The Dynamics of Dendritic Structure in Developing Hippocampal Slices , 1996, The Journal of Neuroscience.

[27]  H. Cline,et al.  In vivo observations of timecourse and distribution of morphological dynamics in Xenopus retinotectal axon arbors. , 1996, Journal of neurobiology.

[28]  P Z Myers,et al.  Spinal motoneurons of the larval zebrafish , 1985, The Journal of comparative neurology.

[29]  C. Sandri,et al.  Topography and ultrastructure of commissural interneurons that may establish reciprocal inhibitory connections of the Mauthner axons in the spinal cord of the tench,Tinca tinca L. , 1990, Journal of neurocytology.

[30]  J. Diamond,et al.  Startle-response in Teleost Fish: an Elementary Circuit for Neural Discrimination , 1968, Nature.

[31]  M. Westerfield,et al.  Identified motoneurons and their innervation of axial muscles in the zebrafish , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  B. Mendelson.  Development of reticulospinal neurons of the zebrafish. II. Early axonal outgrowth and cell body position , 1986, The Journal of comparative neurology.