Specificity and plasticity of retinotectal connections: a computational model

A computational model is presented which simulates the development and regeneration of orderly connections between retinal fibers and tectal cells in frogs and goldfish. The model distinguishes two aspects of retinotectal connectivity: (1) the contact adhesion between retinal fibers and tectal cells as mediated by fixed chemospecific markers and (2) the formation of modifiable synapses between them. Chemospecificity is assumed to be an intrinsic property of both the retina and tectum and is modeled as a graded distribution of a binding determinant or marker. Synapse formation depends upon the timing of neural activity as well as on the intinsic chemospecificity of retinotectal contacts. In addition to the normal development and regeneration of the retinotectal map, the model simulates the compressed, expanded, translocated, and rotated maps that have been found in surgically manipulated contexts. There examples of plasticity in the retinotectal map can be simulated without assuming any changes in the marker distributions. Moreover, the model demonstrates that a very shallow gradient of a single marker suffices to organize retinotectal connections in a variety of contexts.

[1]  Roger W. Sperry,et al.  The effect of crossing nerves to antagonistic muscles in the hind limb of the rat , 1941 .

[2]  Roger W. Sperry,et al.  OPTIC NERVE REGENERATION WITH RETURN OF VISION IN ANURANS , 1944 .

[3]  Reimplantation of Eyes in Fishes (Bathygobius soporator) with Recovery of Vision.∗ , 1949, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[4]  S. Kaplan The Physiology of Thought , 1950 .

[5]  A. M. Uttley,et al.  Conditional Probability Machines and Conditioned Reflexes , 1956 .

[6]  R. M. Gaze,et al.  The retino‐tectal projection in Xenopus with compound eyes , 1963, The Journal of physiology.

[7]  R. Sperry,et al.  Preferential selection of central pathways by regenerating optic fibers. , 1963, Experimental neurology.

[8]  R. M. Gaze,et al.  On the formation of connexions by compound eyes in Xenopus , 1965, The Journal of physiology.

[9]  G. Brindley The classification of modifiable synapses and their use in models for conditioning , 1967, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[10]  G. Székely,et al.  Golgi studies on the optic center of the frog. , 1967, Journal fur Hirnforschung.

[11]  L. Wolpert Positional information and the spatial pattern of cellular differentiation. , 1969, Journal of theoretical biology.

[12]  R. M. Gaze,et al.  The retinotopic organization of visual responses from tectal reimplants in adult goldfish. , 1971, Archives italiennes de biologie.

[13]  R. M. Gaze,et al.  The growth of the retina in Xenopus laevis: an autoradiographic study. , 1971, Journal of embryology and experimental morphology.

[14]  M. Yoon Reorganization of retinotectal projection following surgical operations on the optic tectum in goldfish. , 1971, Experimental neurology.

[15]  T J Horder Retention, by fish optic nerve fibres regenerating to new terminal sites in the tectum, of 'chemospecific' affinity for their original sites. , 1971, The Journal of physiology.

[16]  M. Yoon Reversibility of the reorganization of retinotectal projection in goldfish. , 1972, Experimental neurology.

[17]  M. Yoon Transposition of the visual projection from the nasal hemiretina onto the foreign rostral zone of the optic tectum in goldfish. , 1972, Experimental neurology.

[18]  R. Hunt,et al.  Development and stability of postional information in Xenopus retinal ganglion cells. , 1972, Proceedings of the National Academy of Sciences of the United States of America.

[19]  R. M. Gaze,et al.  The development of the tectum in Xenopus laevis: an autoradiographic study. , 1972, Journal of embryology and experimental morphology.

[20]  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.

[21]  R. Hunt,et al.  Specification of positional information in retinal ganglion cells of Xenopus: assays for analysis of the unspecified state. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[22]  R. Marchase,et al.  Adhesive recognition and retinotectal specificity. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[23]  M. Yoon Retention of the original topographic polarity by the 180° rotated tectal reimplant in young adult goldfish , 1973 .

[24]  R. Hunt,et al.  Development of neuronal locus specificity in Xenopus retinal ganglion cells after surgical eye transection after fusion of whole eyes. , 1974, Developmental biology.

[25]  R. M. Gaze,et al.  The evolution of the retinotectal map during development in Xenopus , 1974, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[26]  W. B. Marks,et al.  Optic nerve terminal arborizations in the frog: shape and orientation inferred from electrophysiological measurements. , 1974, Experimental neurology.

[27]  D. Willshaw,et al.  On a role for competition in the formation of patterned neural connexions , 1975, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[28]  M. Jacobson,et al.  Stability of implanted duplicate tectal positional markers serving as targets for optic axons in adult frogs , 1975, Brain Research.

[29]  M. Jacobson,et al.  Plasticity in the adult frog brain: filling the visual scotoma after excision or translocation of parts of the optic tectum , 1975, Brain Research.

[30]  R. Marchase,et al.  A molecular approach to retinotectal specificity. , 1975, Ciba Foundation symposium.

[31]  M. Yoon Readjustment of retinotectal projection following reimplantation of a rotated or inverted tectal tissue in adult goldfish. , 1975, The Journal of physiology.

[32]  Shin-Ho Chung,et al.  Polarity of structure and of ordered nerve connections in the developing amphibian brain , 1975, Nature.

[33]  A. Barbera,et al.  Adhesive recognition between developing retinal cells and the optic tecta of the chick embryo. , 1975, Developmental biology.

[34]  J. Lilien,et al.  Retinal-tectal connections in the embryonic chick: evidence for regionally specific cell surface components which mimic the pattern of innervation. , 1976, Developmental biology.

[35]  R. M. Gaze,et al.  The arrow model: retinotectal specificity and map formation in the goldfish visual system , 1976, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[36]  M. Yoon Topographic polarity of the optic tectum studied by reimplantation of the tectal tissue in adult goldfish. , 1976, Cold Spring Harbor symposia on quantitative biology.

[37]  C. Malsburg,et al.  How patterned neural connections can be set up by self-organization , 1976, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[38]  M. Yoon Progress of topographic regulation of the visual projection in the halved optic tectum of adult goldfish. , 1976, The Journal of physiology.

[39]  J. Changeux,et al.  Selective stabilisation of developing synapses as a mechanism for the specification of neuronal networks , 1976, Nature.

[40]  T. Horder,et al.  A proposal regarding the significance of simple mechanical events, such as the development of the choroid fissure, in the organization of central visual projections [proceedings]. , 1977, The Journal of physiology.

[41]  Cell-cell recognition in the embryonal nervous system. , 1977, Society of General Physiologists series.

[42]  M. Romeskie,et al.  Immediate ‘compression’ of the goldfish retinal projection to a tectum devoid of degenerating debris , 1977, Brain Research.

[43]  J. Cook,et al.  The multiple factors determining retinotopic order in the growth of optic fibres into the optic tectum. , 1977, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[44]  C. Malsburg,et al.  How to label nerve cells so that they can interconnect in an ordered fashion. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[45]  Combination of fibre-fibre competition and regional tectal differences accounting for the results of tectal graft experiments in goldfish [proceedings]. , 1978 .

[46]  G. I. Bell Models for the specific adhesion of cells to cells. , 1978, Science.

[47]  K. Straznicky The acquisition of tectal positional specification in Xenopus , 1978, Neuroscience Letters.

[48]  J. Schmidt,et al.  Retinal fibers alter tectal positional markers during the expansion of the half retinal projection in goldfish , 1978, The Journal of comparative neurology.

[49]  R. Meyer Deflection of selected optic fibers into a denervated tectum in goldfish , 1978, Brain Research.

[50]  Evidence that optic fibres regenerating across the goldfish tectum may be assigned termination sites on a 'first come, first served' basis [proceedings]. , 1978, The Journal of physiology.

[51]  S. Easter,et al.  Expansion of the half retinal projection to the tectum in goldfish: An electrophysiological and Anatomical study , 1978, The Journal of comparative neurology.

[52]  R. M. Gaze,et al.  The orientation of the visuotectal map in Xenopus: developmental aspects. , 1979, Journal of embryology and experimental morphology.

[53]  David H. Hubel,et al.  Non-retinotopic arrangement of fibres in cat optic nerve , 1979, Nature.

[54]  D J Willshaw,et al.  A marker induction mechanism for the establishment of ordered neural mappings: its application to the retinotectal problem. , 1979, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[55]  Edds Mv,et al.  Specificity and plasticity of retinotectal connections. , 1979, Neurosciences Research Program bulletin.

[56]  R L Meyer,et al.  Retinotectal projection in goldfish to an inappropriate region with a reversal in polarity. , 1979, Science.

[57]  R M Gaze,et al.  Specificity and plasticity of retinotectal connections. , 1979, Neurosciences Research Program bulletin.

[58]  J. Scholes Nerve fibre topography in the retinal projection to the tectum , 1979, Nature.

[59]  R. Hunt,et al.  Retinotectal specificity: models and experiments in search of a mapping function. , 1980, Annual review of neuroscience.

[60]  R. M. Gaze,et al.  Axial differences in the reinnervation of the goldfish optic tectum by regenerating optic nerve fibres , 2004, Experimental Brain Research.