The Problem of Specificity in the Formation of Nerve Connections

For thirty years or so the word’ specificity’ has been much used but under-defined in relation to the developing nervous system, and this has led to considerable confusion. Thus we may talk of specificity of nerve connections and of neuronal specificity; and these two usages have quite different meanings. By’ specificity of nerve connections’ we mean that nerve fibres make predictably particular and selective connections. The phrase, ‘neuronal specificity’, however, has other connotations. It is used to denote the hypothesis, put forward by Sperry (1943; 1944; 1945; 1951; 1963; 1965) to account for the formation of specific or particular nerve connections. I intend to discuss this hypothesis, and consider various of its ramifications, later; here it is merely necessary to point out that, whereas the mechanism proposed in the hypothesis of neuronal specificity is one way to establish specific nerve connections, it is by no means the only way. Specific nerve connections could well be established by a variety of other mechanisms, some of which will also be discussed below. In this chapter I will outline the possibilities as I see them at present, and attempt to assess these in terms of probability.

[1]  R. Sperry Visuomotor coordination in the newt (triturus viridescens) after regeneration of the optic nerve , 1943 .

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

[3]  Roger W. Sperry,et al.  RESTORATION OF VISION AFTER CROSSING OF OPTIC NERVES AND AFTER CONTRALATERAL TRANSPLANTATION OF EYE , 1945 .

[4]  S. S. Stevens,et al.  Handbook of experimental psychology , 1951 .

[5]  J. Faber,et al.  Normal Table of Xenopus Laevis (Daudin) , 1958 .

[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. 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.

[9]  R. M. Gaze The formation of nerve connections , 1970 .

[10]  R. M. Gaze,et al.  The retinotectal projections after uncrossing the optic chiasma in Xenopus with one compound eye. , 1971, Journal of embryology and experimental morphology.

[11]  Lewis Wolpert,et al.  Chapter 6 Positional Information and Pattern Formation , 1971 .

[12]  Horder Tj Retention, by fish optic nerve fibres regenerating to new terminal sites in the tectum, of 'chemospecific' affinity for their original sites. , 1971 .

[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]  S. Sharma,et al.  Reformation of retinotectal projections after various tectal ablations in adult goldfish. , 1972, Experimental neurology.

[16]  R. M. Gaze,et al.  The Visual System and “Neuronal Specificity” , 1972, Nature.

[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. M. Gaze,et al.  Development of the retinotectal projection in Xenopus. , 1972, Nature: New biology.

[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. Lázár The development of the optic tectum in Xenopus laevis: a Golgi study. , 1973, Journal of anatomy.

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

[22]  R. Sperry,et al.  Tests for neuroplasticity in the anuran retinotectal system. , 1973, Experimental neurology.

[23]  E R Macagno,et al.  Structure and development of neuronal connections in isogenic organisms: cellular interactions in the development of the optic lamina of Daphnia. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[24]  K. Fite,et al.  A retinotopic analysis of the central connections of the optic nerve in the frog , 1974, The Journal of comparative neurology.

[25]  Horder Tj Proceedings: Electron microscopic evidence in goldfish that different optic nerve fibres regenerate selectively through specific routes into the tectum. , 1974 .

[26]  T. Bliss,et al.  Functional synaptic relations during the development of the retino-tectal projection in amphibians , 1974, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[27]  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.

[28]  R. Hunt,et al.  Chapter 7 Neuronal Specificity Revisited , 1974 .

[29]  J. Cronly-Dillon,et al.  Intercellular gap junctions in pigment epithelium cells during retinal specification in Xenopus laevis , 1974, Nature.

[30]  W. Cowan,et al.  The specification of the retino‐tectal projection in the chick , 1974, The Journal of comparative neurology.

[31]  J. Cook,et al.  Proceedings: Interactions between optic fibres in their regeneration to specific sites in the goldfish tectum. , 1974, The Journal of physiology.

[32]  J. Cronly-Dillon,et al.  Specificity of regenerating optic fibres for left and right optic tecta in goldfish , 1974, Nature.

[33]  W. Cowan,et al.  Studies on the development of the chick optic tectum. IV. An autoradiographic study of the development of retino-tectal connections , 1975, Brain Research.

[34]  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.

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

[36]  S. C. Sharma,et al.  Visual projection in surgically created ‘compound’ tectum in adult goldfish , 1975, Brain Research.

[37]  R. Hunt,et al.  Neuronal locus specificity: trans-repolarization of Xenopus embryonic retina after the time of axial specification. , 1975, Science.

[38]  R. M. Gaze,et al.  The formation of continuously ordered mappings. , 1976, Progress in brain research.

[39]  T. Scott,et al.  An investigation into the hypothesis of shifting neuronal relationships during development. , 1976, Journal of anatomy.

[40]  M. Jacobson Histogenesis of retina in the clawed frog with implications for the pattern of development of retinotectal connections , 1976, Brain Research.

[41]  M. Murray Regeneration of retinal axons into the goldfish optic tectum , 1976, The Journal of comparative neurology.

[42]  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.

[43]  K. Rock,et al.  A gradient of adhesive specificity in developing avian retina. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[44]  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.

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

[46]  J. Freeman Possible regulatory function of acetylcholine receptor in maintenance of retinotectal synapses , 1977, Nature.

[47]  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.

[48]  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.

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