Skip to main content
Log in

A sharp retinal image increases the topographic precision of the goldfish retinotectal projection during optic nerve regeneration in stroboscopic light

  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Summary

Locally-correlated neural activity appears to play a key role in refining topographically mapped projections. The retinotectal projection of the goldfish normally regains a high degree of spatial precision after regeneration of a cut optic nerve, but it fails to do so if retinal ganglion cell activity is blocked by tetrodotoxin, or if local correlations in activity are masked by the synchronizing effect of stroboscopic light. A sharp retinal image is not normally needed for a sharp map because local correlation occurs even in darkness or diffuse light, but the possibility that a sharp image might restore local correlation and sharpen the map in stroboscopic light, though taken into account in earlier experiments, has not previously been tested. The precision of the retinotectal map was therefore studied, by retrograde transport of WGA-HRP from a standard tectal injection site and quantitative analysis of the labelled ganglion cell distribution, after regeneration of a cut optic nerve for 83–84 days in either continuous stroboscopic light or normal diurnal light. The lens of the eye was either ablated to blur the retinal image or sham-operated. Two different strobe flash patterns used in previous experiments were also compared. With the lens ablated, stroboscopic light impaired map refinement significantly, confirming previous results. A rapid, irregular flash pattern averaging about 5 Hz was rather more effective than a regular 1 Hz pattern. With the lens intact, however, neither pattern had any detectable effect. The significant gain in precision resulting from a sharp retinal image in these circumstances suggests that common mechanisms could underlie both the internal refinement of the retinotectal map and such directly experience-sensitive processes as the experimental realignment of binocular maps in the frog Xenopus, and of auditory and visual maps in the barn owl.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Arnett DW (1978) Statistical dependence between neighbouring retinal ganglion cells in goldfish. Exp Brain Res 32: 49–53

    Google Scholar 

  • Arnett DW, Spraker TE (1981) Cross-correlation analysis of the maintained discharge of rabbit retinal ganglion cells. J Physiol (Lond) 317: 29–47

    Google Scholar 

  • Charman WN, Tucker J (1973) The optical system of the goldfish eye. Vision Res 13: 1–8

    Google Scholar 

  • Chung SH (1974) In search of the rules for nerve connections. Cell 3: 201–205

    Google Scholar 

  • Cook JE (1979) Interactions between optic fibres controlling the locations of their terminals in the goldfish optic tectum. J Embryol Exp Morphol 52: 89–103

    Google Scholar 

  • Cook JE (1984) A simple pseudorandom interval generator. J Physiol (Lond) 357: 6P

  • Cook JE (1986) A sharp retinal image increases the precision of the regenerated goldfish retinotectal projection under stroboscopic conditions. J Physiol (Lond) 372: 84P

  • Cook JE (1987) Full spatial refinement of the regenerated goldfish retinotectal projection can occur in darkness, though not in diffuse stroboscopic light. Neurosci Lett 29 Suppl: S31

    Google Scholar 

  • Cook JE, Rankin ECC (1984) An effect of stroboscopic light on the retinotopography of regenerated optic terminals in goldfish. J Physiol (Lond) 357: 23P

  • Cook JE, Rankin ECC (1986) Impaired refinement of the regenerated goldfish retinotectal projection in stroboscopic light: a quantitative WGA-HRP study. Exp Brain Res 63: 421–430

    Google Scholar 

  • Cook JE, Rankin ECC, Stevens HP (1983) A pattern of optic axons in the normal goldfish tectum consistent with the caudal migration of optic terminals during development. Exp Brain Res 52: 147–151

    Google Scholar 

  • Cowan WM, Hunt RK (1985) The development of the retinotectal projection: an overview. In: Edelman GM, Gall WE, Cowan WM (eds) Molecular basis of neural development. Wiley, New York, pp 389–428

    Google Scholar 

  • Dubin MW, Stark LA, Archer SM (1986) A role for actionpotential activity in the development of neuronal connections in the kitten retinogeniculate pathway. J Neurosci 6: 1021–1036

    Google Scholar 

  • Easter SS Jr, Stuermer CAO (1984) An evaluation of the hypothesis of shifting terminals in goldfish optic tectum. J Neurosci 4: 1052–1063

    Google Scholar 

  • Gaze RM, Sharma SC (1970) Axial differences in the reinnervation of the goldfish optic tectum by regenerating optic nerve fibres. Exp Brain Res 10: 171–181

    Google Scholar 

  • Ginsburg KS, Johnsen JA, Levine MW (1984) Common noise in the firing of neighbouring ganglion cells in goldfish retina. J Physiol (Lond) 351: 433–450

    Google Scholar 

  • Harris WA (1980) The effects of eliminating impulse activity on the development of the retinotectal projection in salamanders. J Comp Neurol 194: 303–317

    Google Scholar 

  • Horder TJ, Martin KAC (1982) Some determinants of optic terminal localization and retinotopic polarity within fibre populations in the tectum of goldfish. J Physiol (Lond) 333: 481–509

    Google Scholar 

  • Johnsen JA, Levine MW (1983) Correlation of activity in neighbouring goldfish ganglion cells: relationship between latency and lag. J Physiol (Lond) 345: 439–449

    Google Scholar 

  • Keating MJ, Grant S, Dawes EA, Nanchahal K (1986) Visual deprivation and the maturation of the retinotectal projection in Xenopus laevis. J Embryol Exp Morphol 91: 101–115

    Google Scholar 

  • Knudsen EI (1985) Experience alters the spatial tuning of auditory units in the optic tectum during a sensitive period in the barn owl. J Neurosci 5: 3094–3109

    Google Scholar 

  • Lewis D, Teyler TJ (1986) Long-term potentiation in the goldfish optic tectum. Brain Res 375: 246–250

    Google Scholar 

  • Mastronarde DN (1983) Correlated firing of cat retinal ganglion cells. I. Spontaneously active inputs to X-and Y-cells. J Neurophysiol 49: 303–324

    Google Scholar 

  • Meredith MA, Stein BE (1986) Spatial factors determine the activity of multisensory neurons in cat superior colliculus. Brain Res 365: 350–354

    Google Scholar 

  • Meyer RL (1983) Tetrodotoxin inhibits the formation of refined retinotopography in goldfish. Dev Brain Res 6: 293–298

    Google Scholar 

  • Rankin ECC, Cook JE (1986) Topographic refinement of the regenerating retinotectal projection of the goldfish in standard laboratory conditions: a quantitative WGA-HRP study. Exp Brain Res 63: 409–420

    Google Scholar 

  • Rodieck RW (1967) Maintained activity of cat retinal ganglion cells. J Neurophysiol 30: 1043–1071

    Google Scholar 

  • Sanes DH, Constantine-Paton M (1985) The sharpening of frequency tuning curves requires patterned activity during development in the mouse, Mus musculus. J Neurosci 5: 1152–1166

    Google Scholar 

  • Schmidt JT (1985) Formation of retinotopic connections: selective stabilization by an activity-dependent mechanism. Cell Mol Neurobiol 5: 65–84

    Google Scholar 

  • Schmidt JT, Edwards DL (1983) Activity sharpens the map during the regeneration of the retinotectal projection in goldfish. Brain Res 269: 29–39

    Google Scholar 

  • Schmidt JT, Eisele LE (1985) Stroboscopic illumination and dark rearing block the sharpening of the regenerated retinotectal map in goldfish. Neuroscience 14: 535–546

    Google Scholar 

  • Schmidt JT, Tieman SB (1985) Eye-specific segregation of optic afferents in mammals, fish and frogs: the role of activity. Cell Mol Neurobiol 5: 5–34

    Google Scholar 

  • Siegel S (1956) Nonparametric statistics for the behavioral sciences. McGraw-Hill, Tokyo, pp 184–194

    Google Scholar 

  • Stiles M, Tzanakou E, Michalak R, Unnikrishnan KP, Goyal P, Harth E (1985) Periodic and nonperiodic burst responses of frog (Rana pipiens) retinal ganglion cells. Exp Neurol 88: 176–197

    Google Scholar 

  • Udin S (1985) The role of visual experience in the formation of binocular projections in frogs. Cell Mol Neurobiol 5: 85–102

    Google Scholar 

  • Whitelaw VA, Cowan JD (1981) Specificity and plasticity of retinotectal connections: a computational model. J Neurosci 1: 1369–1387

    Google Scholar 

  • Willshaw DJ, Malsburg C von der (1976) How patterned neural connections can be set up by self-organization. Proc R Soc (Lond) B 194: 431–445

    Google Scholar 

  • Wye-Dvorak J, Marotte LR, Mark RF (1979) Retinotectal reorganization in goldfish. I. Effects of season, lighting conditions and size of fish. Neuroscience 4: 789–802

    Google Scholar 

  • Yoon MG (1975) Effects of postoperative visual environments on reorganization of retinotectal projection in goldfish. J Physiol (Lond) 246: 673–694

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cook, J.E. A sharp retinal image increases the topographic precision of the goldfish retinotectal projection during optic nerve regeneration in stroboscopic light. Exp Brain Res 68, 319–328 (1987). https://doi.org/10.1007/BF00248798

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00248798

Key words

Navigation