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. 1982;333:481–509. doi: 10.1113/jphysiol.1982.sp014465

Some determinants of optic terminal localization and retinotopic polarity within fibre populations in the tectum of goldfish.

T J Horder, K A Martin
PMCID: PMC1197260  PMID: 7182475

Abstract

1. The reorganization of the retinotectal projection which results after partial ablation of tectal tissue was examined in goldfish using electrophysiological methods. 2. Regardless of the size of a unilateral ablation of caudal tectum, an orderly and virtually complete, 'compressed', visual projection re-formed on the remaining tectum after crushing the optic nerve and allowing it to regenerate. 3. If the optic nerve was left intact after ablations of caudal tectum, compressed projections were only found when the ablations were small. Large caudal ablations involving half or more of the dorsal tectum resulted in the cut fibres transposing onto the remaining tectum and forming an overlaid, 'duplicate', projection on the remaining intact projection. 4. In approximately one third of cases the duplicate projection lay in a reversed polarity along the rostrocaudal axis of the tectum. In the remaining cases the polarity of the duplicate projection was normal. 5. Transposed projections of reversed rostrocaudal polarity could be consistently obtained by ablating temporal retina and caudal tectum, leaving an intact strip of fibres terminals along the caudal edge of the tectal remnant. 6. Compression and duplication occurred in the same way if fish were maintained in constant light. 7. After ablations of lateral tectum, leaving the optic nerve intact, compression and some disorderly duplications were found. 8. Reversed projections could be induced across the mediolateral axis of dorsal tectum by denervating the medial tectum and ablating a strip of lateral tectum. 9. Projections of normal polarity were found after the optic nerve was allowed to regenerate into tecta which had previously supported reversed polarity projections.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. ATTARDI D. G., SPERRY R. W. Preferential selection of central pathways by regenerating optic fibers. Exp Neurol. 1963 Jan;7:46–64. doi: 10.1016/0014-4886(63)90093-1. [DOI] [PubMed] [Google Scholar]
  2. Bunt S. M., Horder T. J., Martin K. A. Evidence that optic fibres regenerating across the goldfish tectum may be assigned termination sites on a 'first come, first served' basis [proceedings]. J Physiol. 1978 Mar;276:45P–46P. [PubMed] [Google Scholar]
  3. Chung S. H., Cooke J. Polarity of structure and of ordered nerve connections in the developing amphibian brain. Nature. 1975 Nov 13;258(5531):126–132. doi: 10.1038/258126a0. [DOI] [PubMed] [Google Scholar]
  4. Cook J. E., Horder T. J. The multiple factors determining retinotopic order in the growth of optic fibres into the optic tectum. Philos Trans R Soc Lond B Biol Sci. 1977 Apr 26;278(961):261–276. doi: 10.1098/rstb.1977.0041. [DOI] [PubMed] [Google Scholar]
  5. Cook J. E. Interactions between optic fibres controlling the locations of their terminals in the goldfish optic tectum. J Embryol Exp Morphol. 1979 Aug;52:89–103. [PubMed] [Google Scholar]
  6. Cronly-Dillon J. R., Glaizner B. Specificity of regenerating optic fibres for left and right optic tecta in goldfish. Nature. 1974 Oct 11;251(5475):505–507. doi: 10.1038/251505b0. [DOI] [PubMed] [Google Scholar]
  7. Cunningham T. J., Speas G. Inversion of anomalous uncrossed projections along the mediolateral axis of the superior colliculus: implications for retinocollicular specificity. Brain Res. 1975 Apr 25;88(1):73–79. doi: 10.1016/0006-8993(75)90950-6. [DOI] [PubMed] [Google Scholar]
  8. Frost D. O., So K. F., Schneider G. E. Postnatal development of retinal projections in Syrian hamsters: a study using autoradiographic and anterograde degeneration techniques. Neuroscience. 1979;4(11):1649–1677. doi: 10.1016/0306-4522(79)90026-5. [DOI] [PubMed] [Google Scholar]
  9. Gaze R. M., Sharma S. C. Axial differences in the reinnervation of the goldfish optic tectum by regenerating optic nerve fibres. Exp Brain Res. 1970;10(2):171–181. [PubMed] [Google Scholar]
  10. Gaze R. M., Straznicky C. Regeneration of optic nerve fibres from a compound eye to both tecta in Xenopus: evidence relating to the state of specification of the eye and the tectum. J Embryol Exp Morphol. 1980 Dec;60:125–140. [PubMed] [Google Scholar]
  11. George S. A., Marks W. B. Optic nerve terminal arborizations in the frog: shape and orientation inferred from electrophysiological measurements. Exp Neurol. 1974 Mar;42(3):467–482. doi: 10.1016/0014-4886(74)90071-5. [DOI] [PubMed] [Google Scholar]
  12. Hope R. A., Hammond B. J., Gaze R. M. The arrow model: retinotectal specificity and map formation in the goldfish visual system. Proc R Soc Lond B Biol Sci. 1976 Nov 12;194(1117):447–466. doi: 10.1098/rspb.1976.0088. [DOI] [PubMed] [Google Scholar]
  13. Horder T. J. Changes of fibre pathways in the goldfish optic tract following regeneration. Brain Res. 1974 May 31;72(1):41–52. doi: 10.1016/0006-8993(74)90648-9. [DOI] [PubMed] [Google Scholar]
  14. Horder T. J., Martin K. A. Morphogenetics as an alternative to chemospecificity in the formation of nerve connections. A review of literature, before 1978, concerning the control of growth of regenerating optic nerve fibres to specific locations in the optic tectum and a new interpretation based on contact guidance. Symp Soc Exp Biol. 1978;32:275–358. [PubMed] [Google Scholar]
  15. Horder T. J., Martin K. A. Translocation of optic fibres in the tectum may be determined by their stability relative to surrounding fibre terminals [proceedings]. J Physiol. 1977 Oct;271(2):23P–24P. [PubMed] [Google Scholar]
  16. Horder T. J., Martin K. A. Variability among laboratories in the occurrence of functional modification in the intertectal visual projection of Xenopus laevis [proceedings]. J Physiol. 1977 Oct;272(1):90P–91P. [PubMed] [Google Scholar]
  17. JACOBSON M., GAZE R. M. TYPES OF VISUAL RESPONSE FROM SINGLE UNITS IN THE OPTIC TECTUM AND OPTIC NERVE OF THE GOLDFISH. Q J Exp Physiol Cogn Med Sci. 1964 Apr;49:199–209. doi: 10.1113/expphysiol.1964.sp001720. [DOI] [PubMed] [Google Scholar]
  18. Jacobson M., Gaze R. M. Selection of appropriate tectal connections by regenerating optic nerve fibers in adult goldfish. Exp Neurol. 1965 Dec;13(4):418–430. doi: 10.1016/0014-4886(65)90128-7. [DOI] [PubMed] [Google Scholar]
  19. Jacobson M., Levine R. L. Plasticity in the adult frog brain: filling the visual scotoma after excision or translocation of parts of the optic tectum. Brain Res. 1975 May 2;88(2):339–345. doi: 10.1016/0006-8993(75)90396-0. [DOI] [PubMed] [Google Scholar]
  20. Land P. W., Lund R. D. Development of the rat's uncrossed retinotectal pathway and its relation to plasticity studies. Science. 1979 Aug 17;205(4407):698–700. doi: 10.1126/science.462177. [DOI] [PubMed] [Google Scholar]
  21. Law M. I., Constantine-Paton M. Right and left eye bands in frogs with unilateral tectal ablations. Proc Natl Acad Sci U S A. 1980 Apr;77(4):2314–2318. doi: 10.1073/pnas.77.4.2314. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Levine R. L., Jacobson M. Discontinuous mapping of retina onto tectum innervated by both eyes. Brain Res. 1975 Nov 7;98(1):172–176. doi: 10.1016/0006-8993(75)90517-x. [DOI] [PubMed] [Google Scholar]
  23. Lo R. Y., Levine R. L. Time course and pattern of optic fiber regeneration following tectal lobe removal in the goldfish. J Comp Neurol. 1980 May 15;191(2):295–314. doi: 10.1002/cne.901910210. [DOI] [PubMed] [Google Scholar]
  24. MATURANA H. R., LETTVIN J. Y., MCCULLOCH W. S., PITTS W. H. Anatomy and physiology of vision in the frog (Rana pipiens). J Gen Physiol. 1960 Jul;43(6):129–175. doi: 10.1085/jgp.43.6.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Marotte L. R., Mark R. F., Wye-Dvorak J. Retinotectal reorganization in goldfish-III. Effect of thyroxine. Neuroscience. 1981;6(8):1591–1600. doi: 10.1016/0306-4522(81)90226-8. [DOI] [PubMed] [Google Scholar]
  26. Marotte L. R., Wye-Dvorak J., Mark R. F. Ultrastructure of reorganising visual projections in half tecta of carp kept in constant light. Neuroscience. 1977;2(5):767–780. doi: 10.1016/0306-4522(77)90030-6. [DOI] [PubMed] [Google Scholar]
  27. Martin K. A. Combination of fibre-fibre competition and regional tectal differences accounting for the results of tectal graft experiments in goldfish [proceedings]. J Physiol. 1978 Mar;276:44P–45P. [PubMed] [Google Scholar]
  28. Merrill E. G., Ainsworth A. Glass-coated platinum-plated tungsten microelectrodes. Med Biol Eng. 1972 Sep;10(5):662–672. doi: 10.1007/BF02476084. [DOI] [PubMed] [Google Scholar]
  29. Meyer R. L. "Extra" optic fibers exclude normal fibers from tectal regions in goldfish. J Comp Neurol. 1979 Feb 15;183(4):883–901. doi: 10.1002/cne.901830411. [DOI] [PubMed] [Google Scholar]
  30. Meyer R. L. Evidence from thymidine labeling for continuing growth of retina and tectum in juvenile goldfish. Exp Neurol. 1978 Mar;59(1):99–111. doi: 10.1016/0014-4886(78)90204-2. [DOI] [PubMed] [Google Scholar]
  31. Meyer R. L. Eye-in-water electrophysiological mapping of goldfish with and without tectal lesions. Exp Neurol. 1977 Jul;56(1):23–41. doi: 10.1016/0014-4886(77)90136-4. [DOI] [PubMed] [Google Scholar]
  32. Meyer R. L. Retinotectal projection in goldfish to an inappropriate region with a reversal in polarity. Science. 1979 Aug 24;205(4408):819–820. doi: 10.1126/science.462191. [DOI] [PubMed] [Google Scholar]
  33. Meyer R. L., Scott M. Y. Failure of continuous light to inhibit compression of retinotectal projection in goldfish. Brain Res. 1977 Jun 3;128(1):153–157. doi: 10.1016/0006-8993(77)90243-8. [DOI] [PubMed] [Google Scholar]
  34. Scalia F., Fite K. A retinotopic analysis of the central connections of the optic nerve in the frog. J Comp Neurol. 1974 Dec 15;158(4):455–477. doi: 10.1002/cne.901580406. [DOI] [PubMed] [Google Scholar]
  35. Schimidt J. T., Cicerone C. M., Easter S. S. Expansion of the half retinal projection to the tectum in goldfish: an electrophysiological and anatomical study. J Comp Neurol. 1978 Jan 15;177(2):257–277. doi: 10.1002/cne.901770206. [DOI] [PubMed] [Google Scholar]
  36. Schmidt J. T. Retinal fibers alter tectal positional markers during the expansion of the retinal projection in goldfish. J Comp Neurol. 1978 Jan 15;177(2):279–295. doi: 10.1002/cne.901770207. [DOI] [PubMed] [Google Scholar]
  37. Scott M. Y. Behavioral tests of compression of retinotectal projection after partial tectal ablation in goldfish. Exp Neurol. 1977 Mar;54(3):579–590. doi: 10.1016/0014-4886(77)90258-8. [DOI] [PubMed] [Google Scholar]
  38. Sharma S. C. Anomalous retinal projection after removal of contralateral optic tectum in adult goldfish. Exp Neurol. 1973 Dec;41(3):661–669. doi: 10.1016/0014-4886(73)90058-7. [DOI] [PubMed] [Google Scholar]
  39. Sharma S. C. Reformation of retinotectal projections after various tectal ablations in adult goldfish. Exp Neurol. 1972 Jan;34(1):171–182. doi: 10.1016/0014-4886(72)90197-5. [DOI] [PubMed] [Google Scholar]
  40. Sharma S. C. Retinal projection in a non-visual area after bilateral tectal ablation in goldfish. Nature. 1981 May 7;291(5810):66–67. doi: 10.1038/291066a0. [DOI] [PubMed] [Google Scholar]
  41. Sharma S. C., Tung Y. L. Interactions between nasal and temporal hemiretinal fibers in adult goldfish tectum. Neuroscience. 1979;4(1):113–119. doi: 10.1016/0306-4522(79)90221-5. [DOI] [PubMed] [Google Scholar]
  42. Springer A. D., Cohen S. M. Optic fiber segregation in goldfish with two eyes innervating one tectal lobe. Brain Res. 1981 Nov 23;225(1):23–36. doi: 10.1016/0006-8993(81)90315-2. [DOI] [PubMed] [Google Scholar]
  43. Straznicky C., Glastonbury J. Anomalous ipsilateral optic fibre projection in Xenopus induced by larval tectal ablation. J Embryol Exp Morphol. 1979 Apr;50:111–122. [PubMed] [Google Scholar]
  44. Thompson I. D. Changes in the uncrossed retinotectal projection after removal of the other eye at birth. Nature. 1979 May 3;279(5708):63–66. doi: 10.1038/279063a0. [DOI] [PubMed] [Google Scholar]
  45. Willshaw D. J., von der Malsburg C. How patterned neural connections can be set up by self-organization. Proc R Soc Lond B Biol Sci. 1976 Nov 12;194(1117):431–445. doi: 10.1098/rspb.1976.0087. [DOI] [PubMed] [Google Scholar]
  46. Wye-Dvorak J., Marotte L. R., Mark R. F. Retinotectal reorganization in goldfish--I. Effects of season, lighting conditions and size of fish. Neuroscience. 1979;4(6):789–802. doi: 10.1016/0306-4522(79)90007-1. [DOI] [PubMed] [Google Scholar]
  47. Yoon M. G. Effects of post-operative visual environments on reorganization of retinotectal projection in goldfish. J Physiol. 1975 Apr;246(3):673–694. doi: 10.1113/jphysiol.1975.sp010910. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Yoon M. G. Progress of topographic regulation of the visual projection in the halved optic tectum of adult goldfish. J Physiol. 1976 Jun;257(3):621–643. doi: 10.1113/jphysiol.1976.sp011388. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Yoon M. G. Transposition of the visual projection from the nasal hemiretina onto the foreign rostral zone of the optic tectum in goldfish. Exp Neurol. 1972 Dec;37(3):451–462. doi: 10.1016/0014-4886(72)90088-x. [DOI] [PubMed] [Google Scholar]
  50. Yoon M. Reorganization of retinotectal projection following surgical operations on the optic tectum in goldfish. Exp Neurol. 1971 Nov;33(2):395–411. doi: 10.1016/0014-4886(71)90031-8. [DOI] [PubMed] [Google Scholar]
  51. Yoon M. Reversibility of the reorganization of retinotectal projection in goldfish. Exp Neurol. 1972 Jun;35(3):565–577. doi: 10.1016/0014-4886(72)90128-8. [DOI] [PubMed] [Google Scholar]

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