Developmental relocation of presynaptic terminals along distinct types of dendritic filopodia.

Dendritic filopodia are long thin protrusions occurring predominantly on developing neurons. Data from different systems suggest a range of crucial functions for filopodia in central circuit formation, including steering of dendritic growth, branch formation, synaptogenesis, and spinogenesis. Are the same filopodia competent to mediate all these processes, do filopodia acquire different functions through development, or do different filopodial types with distinct functions exist? In this study, 3-dimensional reconstructions from confocal image stacks demonstrate the existence of two morphologically and functionally distinct types of filopodia located on the dendritic tips versus the dendritic shafts of the same developing motoneuron. During dendritic growth, both filopodial types undergo a process of stage-specific morphogenesis. Using novel quantification strategies of 3-dimensional co-localization analysis for immunocytochemically labeled presynaptic specializations along postsynaptic filopodia, we find that presynaptic terminals accumulate along filopodia towards the dendrites at both stable dendritic shafts and on growing dendritic tips. On tips, this is likely to reflect synaptotrophic growth of the dendrite. At stable shafts, however, presynaptic sites become relocated along filopodia towards dendritic branches. This indicates the interactive growth of both pre- and postsynaptic partner towards one another during synaptogenesis, using filopodia as guides.

[1]  James S. Buckner,et al.  LIFE CYCLE OF LABORATORY-REARED TOBACCO HORNWORMS, MANDUCA SEXTA, A STUDY OF DEVELOPMENT AND BEHAVIOR, USING TIME-LAPSE CINEMATOGRAPHY , 1980 .

[2]  N. Spitzer,et al.  Regulation of growth cone behavior by calcium: new dynamics to earlier perspectives. , 2000, Journal of neurobiology.

[3]  L. Tolbert,et al.  Immunolocalization of synaptotagmin for the study of synapses in the developing antennal lobe of Manduca sexta , 2001, The Journal of comparative neurology.

[4]  R. Yuste,et al.  Activity-Regulated Dynamic Behavior of Early Dendritic Protrusions: Evidence for Different Types of Dendritic Filopodia , 2003, The Journal of Neuroscience.

[5]  F. Wouterlood,et al.  Two-laser dual-immunofluorescence confocal laser scanning microscopy using Cy2- and Cy5-conjugated secondary antibodies: unequivocal detection of co-localization of neuronal markers. , 1998, Brain research. Brain research protocols.

[6]  Stanley B. Kater,et al.  Filopodia on neuronal growth cones: multi-functional structures with sensory and motor capabilities , 1996 .

[7]  M. Poo,et al.  Filopodial Calcium Transients Promote Substrate-Dependent Growth Cone Turning , 2001, Science.

[8]  Gerd Bicker STOP and GO with NO: Nitric oxide as a regulator of cell motility in simple brains , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[9]  H. Cline,et al.  Dendritic Dynamics In Vivo Change during Neuronal Maturation , 1999, The Journal of Neuroscience.

[10]  Rafael Yuste,et al.  Genesis of dendritic spines: insights from ultrastructural and imaging studies , 2004, Nature Reviews Neuroscience.

[11]  L. Gilbert,et al.  Ecdysteroid titer during larval--pupal--adult development of the tobacco hornworm, Manduca sexta. , 1981, General and comparative endocrinology.

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

[13]  R. Yuste,et al.  Imaging the motility of dendritic protrusions and axon terminals: roles in axon sampling and synaptic competition , 2004, Molecular and Cellular Neuroscience.

[14]  R. A. Bell,et al.  Techniques for Rearing Laboratory Colonies of Tobacco Hornworms and Pink Bollworms , 1976 .

[15]  Michael Scholz,et al.  New methods for the computer-assisted 3-D reconstruction of neurons from confocal image stacks , 2004, NeuroImage.

[16]  Martin P Meyer,et al.  In vivo imaging of synapse formation on a growing dendritic arbor , 2004, Nature Neuroscience.

[17]  S. B. Kater,et al.  The unique and shared properties of neuronal growth cones that enable navigation and specific pathfinding , 1994, Journal of Physiology-Paris.

[18]  A. Watson,et al.  Synaptic structure, distribution, and circuitry in the central nervous system of the locust and related insects , 2002, Microscopy research and technique.

[19]  J. Hildebrand,et al.  Development of synapses in the antennal lobes of the moth Manduca sexta during metamorphosis , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  Darren W. Williams,et al.  Mechanisms of Dendritic Elaboration of Sensory Neurons in Drosophila: Insights from In Vivo Time Lapse , 2004, The Journal of Neuroscience.

[21]  C Duch,et al.  Remodeling of Membrane Properties and Dendritic Architecture Accompanies the Postembryonic Conversion of a Slow into a Fast Motoneuron , 2000, The Journal of Neuroscience.

[22]  J F Evers,et al.  Progress in functional neuroanatomy: precise automatic geometric reconstruction of neuronal morphology from confocal image stacks. , 2005, Journal of neurophysiology.

[23]  S. Kater,et al.  Regulation of neuronal growth cone filopodia by intracellular calcium , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  R. Levine,et al.  Steroid hormone enhancement of neurite outgrowth in identified insect motor neurons involves specific effects on growth cone form and function. , 1999, Journal of neurobiology.

[25]  James E. Vaughn,et al.  Review: Fine structure of synaptogenesis in the vertebrate central nervous system , 1989 .

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

[27]  Carsten Duch,et al.  Activity Affects Dendritic Shape and Synapse Elimination during Steroid Controlled Dendritic Retraction in Manduca sexta , 2004, The Journal of Neuroscience.

[28]  Tobias Bonhoeffer,et al.  Local calcium transients regulate the spontaneous motility of dendritic filopodia , 2005, Nature Neuroscience.

[29]  Carsten Duch,et al.  Behavioral transformations during metamorphosis: remodeling of neural and motor systems , 2000, Brain Research Bulletin.

[30]  Frederic Libersat,et al.  Morphometric analysis of dendritic remodeling in an identified motoneuron during postembryonic development , 2002, The Journal of comparative neurology.

[31]  Mu-ming Poo,et al.  Adaptation in the chemotactic guidance of nerve growth cones , 2002, Nature.

[32]  R. Levine,et al.  Changes in calcium signaling during postembryonic dendritic growth in Manduca sexta. , 2002, Journal of neurophysiology.