Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1980 Apr;77(4):2314–2318. doi: 10.1073/pnas.77.4.2314

Right and left eye bands in frogs with unilateral tectal ablations.

M I Law, M Constantine-Paton
PMCID: PMC348705  PMID: 6929551

Abstract

Surgical ablation of a single tectal lobe in Rana pipiens can cause regenerating retinal ganglion cell axons to cross to the remaining tectum. These synaptically deprived fibers can obtain termination space in a retinotopic and highly stereotyped manner. Each of the two eyes can share the undisturbed tectum by terminating in mutually exclusive, eye-specific stripes that alternate across the medial-lateral extent of the tectal lobe. Invading axons from the ipsilateral eye must actively displace established synapses from the contralateral eye in order to form these exclusive termination zones because the normal projection to the intact tectum is not severed in these experiments. In animals in which a large proportion of anomalous fibers do not reach the undisturbed tectum, only a few ipsilateral eye bands are observed. Nevertheless, these bands have the same width, periodicity, and orientation as those observed in fully banded preparations. When ipsilateral eye terminal density is extremely low, banding is absent. The completely striped termination pattern of unitectal animals is identical to the pattern previously reported in the dually innervated tecta of three-eyed R. pipiens. We theorize that this pattern results from a compromise between two synaptogenic forces that are active in regeneration as well as in development.

Full text

PDF
2316

Images in this article

2315Image
on p.2315

Selected References

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

  1. Adams J. C. Technical considerations on the use of horseradish peroxidase as a neuronal marker. Neuroscience. 1977;2(1):141–145. doi: 10.1016/0306-4522(77)90074-4. [DOI] [PubMed] [Google Scholar]
  2. Colman D. R., Scalia F., Cabrales E. Light and electron microscopic observations on the anterograde transport of horseradish peroxidase in the optic pathway in the mouse and rat. Brain Res. 1976 Jan 30;102(1):156–163. doi: 10.1016/0006-8993(76)90582-5. [DOI] [PubMed] [Google Scholar]
  3. Constantine-Paton M., Capranica R. R. Axonal guidance of developing optic nerves in the frog. I. Anatomy of the projection from transplanted eye primordia. J Comp Neurol. 1976 Nov 1;170(1):17–31. doi: 10.1002/cne.901700103. [DOI] [PubMed] [Google Scholar]
  4. Constantine-Paton M., Law M. I. Eye-specific termination bands in tecta of three-eyed frogs. Science. 1978 Nov 10;202(4368):639–641. doi: 10.1126/science.309179. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Devor M. Fiber trajectories of olfactory bulb efferents in the hamster. J Comp Neurol. 1976 Mar 1;166(1):31–47. doi: 10.1002/cne.901660104. [DOI] [PubMed] [Google Scholar]
  7. Easter S. S., Jr, Schmidt J. T. Reversed visuomotor behavior mediated by induced ipsilateral retinal projections in goldfish. J Neurophysiol. 1977 Nov;40(6):1245–1254. doi: 10.1152/jn.1977.40.6.1245. [DOI] [PubMed] [Google Scholar]
  8. Goldman P. S., Nauta W. J. Autoradiographic demonstration of a projection from prefrontal association cortex to the superior colliculus in the rhesus monkey. Brain Res. 1976 Oct 29;116(1):145–149. doi: 10.1016/0006-8993(76)90256-0. [DOI] [PubMed] [Google Scholar]
  9. Graybiel A. M. A stereometric pattern of distribution of acetylthiocholinesterase in the deep layers of the superior colliculus. Nature. 1978 Apr 6;272(5653):539–541. doi: 10.1038/272539b0. [DOI] [PubMed] [Google Scholar]
  10. Graybiel A. M. Anatomical organization of retinotectal afferents in the cat: an autoradiographic study. Brain Res. 1975 Oct 10;96(1):1–23. doi: 10.1016/0006-8993(75)90566-1. [DOI] [PubMed] [Google Scholar]
  11. Graybiel A. M. Anatomical organization of retinotectal afferents in the cat: an autoradiographic study. Brain Res. 1975 Oct 10;96(1):1–23. doi: 10.1016/0006-8993(75)90566-1. [DOI] [PubMed] [Google Scholar]
  12. Hubel D. H., LeVay S., Wiesel T. N. Mode of termination of retinotectal fibers in macaque monkey: an autoradiographic study. Brain Res. 1975 Oct 10;96(1):25–40. doi: 10.1016/0006-8993(75)90567-3. [DOI] [PubMed] [Google Scholar]
  13. Hubel D. H., Wiesel T. N. Laminar and columnar distribution of geniculo-cortical fibers in the macaque monkey. J Comp Neurol. 1972 Dec;146(4):421–450. doi: 10.1002/cne.901460402. [DOI] [PubMed] [Google Scholar]
  14. Hubel D. H., Wiesel T. N. Receptive fields and functional architecture of monkey striate cortex. J Physiol. 1968 Mar;195(1):215–243. doi: 10.1113/jphysiol.1968.sp008455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ingle D. Two visual systems in the frog. Science. 1973 Sep 14;181(4104):1053–1055. doi: 10.1126/science.181.4104.1053. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Kicliter E., Misantone L. J., Stelzner D. J. Neuronal specificity and plasticity in frog visual system: anatomical correlates. Brain Res. 1974 Dec 27;82(2):293–297. doi: 10.1016/0006-8993(74)90608-8. [DOI] [PubMed] [Google Scholar]
  18. LeVay S., Hubel D. H., Wiesel T. N. The pattern of ocular dominance columns in macaque visual cortex revealed by a reduced silver stain. J Comp Neurol. 1975 Feb 15;159(4):559–576. doi: 10.1002/cne.901590408. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. 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]
  21. 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]
  22. Meyer R. L. Deflection of selected optic fibers into a denervated tectum in goldfish. Brain Res. 1978 Oct 27;155(2):213–227. doi: 10.1016/0006-8993(78)91018-1. [DOI] [PubMed] [Google Scholar]
  23. Miller B. F., Lund R. D. The pattern of retinotectal connections in albino rats can be modified by fetal surgery. Brain Res. 1975 Jun 20;91(1):119–125. doi: 10.1016/0006-8993(75)90470-9. [DOI] [PubMed] [Google Scholar]
  24. Misantone L. J., Stelzner D. J. Behavioral manifestations of competition of retinal endings for sites in doubly innervated frog optic tectum. Exp Neurol. 1974 Nov;45(2):364–376. doi: 10.1016/0014-4886(74)90125-3. [DOI] [PubMed] [Google Scholar]
  25. Pollack J. G., Hickey T. L. The distribution of retino-collicular axon terminals in rhesus monkey. J Comp Neurol. 1979 Jun 15;185(4):587–602. doi: 10.1002/cne.901850402. [DOI] [PubMed] [Google Scholar]
  26. Pollack J. G., Hickey T. L. The distribution of retino-collicular axon terminals in rhesus monkey. J Comp Neurol. 1979 Jun 15;185(4):587–602. doi: 10.1002/cne.901850402. [DOI] [PubMed] [Google Scholar]
  27. Prestige M. C., Willshaw D. J. On a role for competition in the formation of patterned neural connexions. Proc R Soc Lond B Biol Sci. 1975 Jun 20;190(1098):77–98. doi: 10.1098/rspb.1975.0080. [DOI] [PubMed] [Google Scholar]
  28. Rakic P. Prenatal development of the visual system in rhesus monkey. Philos Trans R Soc Lond B Biol Sci. 1977 Apr 26;278(961):245–260. doi: 10.1098/rstb.1977.0040. [DOI] [PubMed] [Google Scholar]
  29. SPERRY R. W. CHEMOAFFINITY IN THE ORDERLY GROWTH OF NERVE FIBER PATTERNS AND CONNECTIONS. Proc Natl Acad Sci U S A. 1963 Oct;50:703–710. doi: 10.1073/pnas.50.4.703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Scalia F., Colman D. R. Aspects of the central projection of the optic nerve in the frog as revealed by anterograde migration of horseradish peroxidase. Brain Res. 1974 Oct 25;79(3):496–504. doi: 10.1016/0006-8993(74)90447-8. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Schneider G. E. Early lesions of superior colliculus: factors affecting the formation of abnormal retinal projections. Brain Behav Evol. 1973;8(1):73–109. doi: 10.1159/000124348. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. Straznicky C., Gaze R. M., Horder T. J. Selection of appropriate medial branch of the optic tract by fibres of ventral retinal origin during development and in regeneration: an autoradiographic study in Xenopus. J Embryol Exp Morphol. 1979 Apr;50:253–267. [PubMed] [Google Scholar]
  35. 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]
  36. Udin S. B. Rearrangements of the retinotectal projection in Rana pipiens after unilateral caudal half-tectum ablation. J Comp Neurol. 1977 Jun 1;173(3):561–582. doi: 10.1002/cne.901730310. [DOI] [PubMed] [Google Scholar]
  37. Wiesel T. N., Hubel D. H., Lam D. M. Autoradiographic demonstration of ocular-dominance columns in the monkey striate cortex by means of transneuronal transport. Brain Res. 1974 Oct 18;79(2):273–279. doi: 10.1016/0006-8993(74)90416-8. [DOI] [PubMed] [Google Scholar]
  38. Willshaw D. J., von der Malsburg C. A marker induction mechanism for the establishment of ordered neural mappings: its application to the retinotectal problem. Philos Trans R Soc Lond B Biol Sci. 1979 Nov 1;287(1021):203–243. doi: 10.1098/rstb.1979.0056. [DOI] [PubMed] [Google Scholar]
  39. Wise S. P., Jones E. G. Cells of origin and terminal distribution of descending projections of the rat somatic sensory cortex. J Comp Neurol. 1977 Sep 15;175(2):129–157. doi: 10.1002/cne.901750202. [DOI] [PubMed] [Google Scholar]
  40. von der Malsburg C. Development of ocularity domains and growth behaviour of axon terminals. Biol Cybern. 1979 Feb 2;32(1):49–62. doi: 10.1007/BF00337452. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES