Stroboscopic illumination and dark rearing block the sharpening of the regenerated retinotectal map in goldfish

Blocking activity with intraocular tetrodotoxin prevents the sharpening of the retinotectal map formed during regeneration of the optic nerve. If (under normal conditions) the initially diffuse map sharpens because of correlated activity in neighboring but not distant ganglion cells, then sharpening should also be prevented merely by disrupting the spatiotemporal correlation in the pattern of activity. To test this idea, fish were exposed during regeneration to stroboscopic illumination in a featureless environment, or were maintained in complete darkness. The regenerating cells remained visually responsive after axotomy, and the xenon strobe effectively drove each ganglion cell at a constant latency. The maps formed in the strobe-reared fish were normally oriented, but the multiunit receptive fields were greatly enlarged, averaging 32 degrees. In control regenerates, multiunit receptive fields averaged only 11-12 degrees, nearly the same as for single units. Dark rearing, which allows only spontaneous activity, also resulted in enlarged multiunit receptive fields, averaging more than 28 degrees. Both effects parallel those reported previously with tetrodotoxin block. The mature projection did not become diffuse as a result of the strobe rearing, and the sensitive period corresponded to the early stage of synaptogenesis (20-34 days). Periods of normal visual exposure after 35 days produced very little sharpening of the diffuse maps produced during either strobe or dark rearing. The results are attributed to an activity-dependent stabilization of developing synapses. The correlated firing of neighboring ganglion cells could allow postsynaptic summation of their responses, and the retention of those more effective, retinotopically placed synapses might then occur via a Hebbian mechanism.

[1]  S. Easter,et al.  A comparison of the normal and regenerated retinotectal pathways of goldfish , 1984, The Journal of comparative neurology.

[2]  J. Schmidt,et al.  Effect of α-bungarotoxin on retinotectal synaptic transmission in the goldfish and the toad , 1980, Neuroscience.

[3]  J. Schmidt,et al.  The re-establishment of synaptic transmission by regenerating optic axons in goldfish: Time course and effects of blocking activity by intraocular injection of tetrodotoxin , 1983, Brain Research.

[4]  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.

[5]  R L Meyer,et al.  Tetrodotoxin inhibits the formation of refined retinotopography in goldfish. , 1983, Brain research.

[6]  R. M. Gaze,et al.  Abnormal visual function in Xenopus following stroboscopic illumination. , 1973, Nature: New biology.

[7]  H Spekreijse,et al.  Spectral and spatial coding of ganglion cell responses in goldfish retina. , 1972, Journal of neurophysiology.

[8]  R. M. Gaze,et al.  Further studies on the restoration of the contralateral retinotectal projection following regeneration of the optoc nerve in the frog. , 1970, Brain research.

[9]  M. Gazzaniga,et al.  Optic nerve regeneration in goldfish under light deprivation , 1982, Brain Research Bulletin.

[10]  D. Purves,et al.  Elimination of synapses in the developing nervous system. , 1980, Science.

[11]  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.

[12]  D. Edwards,et al.  Intraocular tetrodotoxin in goldfish hinders optic nerve regeneration , 1983, Brain Research.

[13]  M. Murray,et al.  A quantitative study of the reinnervation of the goldfish optic tectum following optic nerve crush , 1982, The Journal of comparative neurology.

[14]  K. Watanabe,et al.  Branching of regenerating retinal axons and preferential selection of appropriate branches for specific neuronal connection in the newt. , 1982, Developmental biology.

[15]  M. Keating,et al.  Visual deprivation and intertectal neuronal connexions in Xenopus laevis , 1975, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[16]  R. O'brien,et al.  Observations on the elimination of polyneuronal innervation in developing mammalian skeletal muscle. , 1978, The Journal of physiology.

[17]  S M Archer,et al.  Abnormal development of kitten retino-geniculate connectivity in the absence of action potentials. , 1982, Science.

[18]  J. Schmidt,et al.  Activity sharpens the map during the regeneration of the retinotectal projection in goldfish , 1983, Brain Research.

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

[20]  R. Meyer Mapping the normal and regenerating retinotectal projection of goldfish with autoradiographic methods , 1980, The Journal of comparative neurology.

[21]  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.

[22]  L. Chalupa,et al.  Modification of visual response properties in the superior colliculus of the golden hamster following stroboscopic rearing , 1978, Journal of Physiology.

[23]  J. Schmidt,et al.  Regeneration of the retinotectal projection following compression onto a half tectum in goldfish. , 1983, Journal of embryology and experimental morphology.

[24]  A. Macy Growth-related changes in the receptive field properties of retinal ganglion cells in goldfish , 1981, Vision Research.

[25]  L. Beazley,et al.  An electrophysiological study of early retinotectal projection patterns during optic nerve regeneration inHyla moorei , 1982, Brain Research.

[26]  E. Meeter,et al.  Reduction of polyneuronal innervation of muscle cells in tissue culture after long-term indirect stimulation. , 1982, Brain research.

[27]  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.

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

[29]  J. Wye-Dvorak,et al.  Retinotectal reorganization in goldfish—II. Effects of partial tectal ablation and constant light on the retina , 1979, Neuroscience.

[30]  T. Creazzo,et al.  Effects of chronic paralysis with α-bungarotoxin on development of innervation , 1979, Experimental Neurology.

[31]  P. Grobstein,et al.  Recovery of the ipsilateral oculotectal projection following nerve crush in the frog: evidence that retinal afferents make synapses at abnormal tectal locations , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  J. Changeux,et al.  Consequences of blocking the nerve with a local anaesthetic on the evolution of multiinnervation at the regenerating neuromuscular junction of the rat , 1978, Brain Research.

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

[34]  Gerta Vrbová,et al.  The role of muscle activity in the differentiation of neuromuscular junctions in slow and fast chick muscles , 1978, Journal of neurocytology.

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

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

[37]  John T. Schmidt,et al.  Electrophysiologic evidence that retinotectal synaptic transmission in the goldfish is nicotinic cholinergic , 1980, Brain Research.

[38]  J. K. S. Jansen,et al.  The effect of prolonged, reversible block of nerve impulses on the elimination of polyneuronal innervation of new-born rat skeletal muscle fibers , 1979, Neuroscience.