Control of Axon Branch Dynamics by Correlated Activity in Vivo

To determine how patterned visual activity regulates the development of axonal projections, we collected in vivo time-lapse images of retinal axons from albino Xenopus tadpoles in which binocular innervation of the optic tectum was induced. Axons added branch tips with nearly equal probability in all territories, but eliminated them preferentially from territory dominated by the opposite eye. This selective branch elimination was abolished by blockade of N-methyl-d-aspartate receptors. These results describe a correlation-based mechanism by which visual experience directly governs axon branch dynamics that contribute to the development of topographic maps.

[1]  M P Stryker,et al.  Plasticity of geniculocortical afferents following brief or prolonged monocular occlusion in the cat , 1996, The Journal of comparative neurology.

[2]  H. Cline.  Activity-dependent plasticity in the visual systems of frogs and fish , 1991, Trends in Neurosciences.

[3]  M. Law,et al.  Eye-specific termination bands in tecta of three-eyed frogs. , 1978, Science.

[4]  C. Straznicky,et al.  Anomalous ipsilateral optic fibre projection in Xenopus induced by larval tectal ablation. , 1979, Journal of embryology and experimental morphology.

[5]  T. Reh,et al.  Retinal ganglion cell terminals change their projection sites during larval development of Rana pipiens , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  M. Constantine-Paton,et al.  N-methyl-D-aspartate receptor antagonists disrupt the formation of a mammalian neural map. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[7]  Hollis T. Cline,et al.  NMDA receptor activity stabilizes presynaptic retinotectal axons and postsynaptic optic tectal cell dendrites in vivo. , 1999 .

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

[9]  T. McLaughlin,et al.  Topographic-Specific Axon Branching Controlled by Ephrin-As Is the Critical Event in Retinotectal Map Development , 2001, The Journal of Neuroscience.

[10]  J G Flanagan,et al.  The ephrins and Eph receptors in neural development. , 1998, Annual review of neuroscience.

[11]  J. Lichtman,et al.  In Vivo Time-Lapse Imaging of Synaptic Takeover Associated with Naturally Occurring Synapse Elimination , 2003, Neuron.

[12]  M P Stryker,et al.  Control of thalamocortical afferent rearrangement by postsynaptic activity in developing visual cortex. , 1994, Science.

[13]  R L Meyer,et al.  Tetrodotoxin blocks the formation of ocular dominance columns in goldfish. , 1982, Science.

[14]  M. Constantine-Paton,et al.  Patterned activity, synaptic convergence, and the NMDA receptor in developing visual pathways. , 1990, Annual review of neuroscience.

[15]  S. Cohen-Cory,et al.  BDNF Modulates, But Does Not Mediate, Activity-Dependent Branching and Remodeling of Optic Axon Arbors In Vivo , 1999, The Journal of Neuroscience.

[16]  R. Sperry.  CHEMOAFFINITY IN THE ORDERLY GROWTH OF NERVE FIBER PATTERNS AND CONNECTIONS. , 1963, Proceedings of the National Academy of Sciences of the United States of America.

[17]  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.

[18]  Jeff W. Lichtman,et al.  Long-term synapse loss induced by focal blockade of postsynaptlc receptors , 1994, Nature.

[19]  宁北芳,et al.  疟原虫var基因转换速率变化导致抗原变异[英]／Paul H, Robert P, Christodoulou Z, et al//Proc Natl Acad Sci U S A , 2005 .

[20]  Hollis T. Cline,et al.  NMDA receptor antagonists disrupt the retinotectal topographic map , 1989, Neuron.

[21]  E. Debski,et al.  N-methyl-D-aspartate receptor antagonist desegregates eye-specific stripes. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[22]  S. Schmid,et al.  Analysis of the Activity-Deprived Zebrafish Mutantmacho Reveals an Essential Requirement of Neuronal Activity for the Development of a Fine-Grained Visuotopic Map , 2001, The Journal of Neuroscience.

[23]  D. Hubel,et al.  Ferrier lecture - Functional architecture of macaque monkey visual cortex , 1977, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[24]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[25]  M. Constantine-Paton,et al.  Eye-specific segregation requires neural activity in three-eyed Rana pipiens , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  C. Rittenhouse,et al.  Monocular deprivation induces homosynaptic long-term depression in visual cortex , 1999, Nature.

[27]  R. Meyer,et al.  The effect of TTX‐activity blockade and total darkness on the formation of retinotopy in the goldfish retinotectal projection , 1991, The Journal of comparative neurology.

[28]  G. Stent.  A physiological mechanism for Hebb's postulate of learning. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[29]  R. M. Gaze,et al.  The relationship between retinal and tectal growth in larval Xenopus: implications for the development of the retino-tectal projection. , 1979, Journal of embryology and experimental morphology.

[30]  R. Meyer,et al.  Regenerating optic fibers correct large‐scale errors by random growth: Evidence from in vivo imaging , 2001, The Journal of comparative neurology.

[31]  J. Lichtman,et al.  Synapse Elimination and Indelible Memory , 2000, Neuron.

[32]  J. Schmidt,et al.  MK801 increases retinotectal arbor size in developing zebrafish without affecting kinetics of branch elimination and addition. , 2000, Journal of neurobiology.

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

[34]  J. Schmidt,et al.  Activity and the formation of ocular dominance patches in dually innervated tectum of goldfish , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.