Journal of Neurocytology

, Volume 30, Issue 3, pp 219–230 | Cite as

Metabolic changes in the nucleus of the optic tract after monocular enucleation as revealed by cytochrome oxidase histochemistry

  • C. D. Vargas
  • A. O. Sousa
  • C. M. Santos
  • A. PereiraJr.
  • R. F. Bernardes
  • C. E. Rocha-Miranda
  • E. Volchan
Article

Abstract

The histochemistry for the mitochondrial enzyme cytochrome oxidase (CO) was used to evaluate the levels of metabolic activity in neurons of the nucleus of the optic tract (NOT) and dorsal terminal nucleus (DTN) in the opossum (Didelphis aurita). The observations were performed in four groups: normal juveniles (4 months old), monocularly enucleated juveniles analysed when adults, normal adults (8 to 18 months old) and monocularly enucleated adults. CO labeled cells were observed to have a similar distribution along the NOT-DTN anteroposterior axis in both juvenile and adult normal animals. Monocular enucleation performed in adults produced a significant reduction of the reactive neuropil but not of the number of CO labeled cells in the deafferented NOT-DTN: the number of labeled neurons per section in the deafferented side matched those of the ipsilateral complex. In juveniles, however, this procedure caused a systematic reduction of the number of CO labeled cells in the contralateral NOT-DTN in comparison to the spared complex. The lack of reduction in the number of neurons found on the deafferented side of the NOT-DTN of monocularly enucleated adult opossums compared with the ipsilateral side might result from the presence of compensatory inputs to maintain their metabolic equivalence. However, when the monocular enucleation was performed in juvenile opossums, a statistically significant asymmetry of CO neurons in the NOT-DTN was observed. In other words, the compensatory mechanisms proposed for the adults were either absent or insufficient to achieve symmetry in juveniles, suggesting a more heavily reliance in the retinal input.

Keywords

Label Cell Cytochrome Oxidase Optic Tract Ipsilateral Side Label Neuron 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Ballas, I. & Hofffmann, K. P. (1985) A correlation between receptive field properties and morphological structures in the pretectum of the cat. Journal of Comparative Neurology 238, 417–438.Google Scholar
  2. Cavalcante, L. A. & Rocha-Miranda, C. E. (1978) Development of the dorsal thalamus and superior colliculus in the opossum, with special reference to optic projection areas. In Opossum Neurobiology (edited by Rocha-Miranda, C. E. & Lent, R.), pp. 193–206. Rio de Janeiro: Academia Brasileira de Ciências.Google Scholar
  3. Cavalcante, L. A. (1985) Postnatal neurogenesis and the formation of neural connections in the visual system of a marsupial. In Working Group on Developmental Neurobiology of Mammals (edited by Chagas, C. & Linden, R.) pp. 1–29. Pontificiae Academia Scientifica Scripta Varia, Vatican.Google Scholar
  4. Cavalcante, L. A., Barradas, P. C. & Martinez, A. M. B. (1991) Patterns of myelination in the opossum superior colliculus with additional reference to the optic tract. Anatomy and Embryology 183, 273–285.Google Scholar
  5. Cazin, L., Precht, W. & Lannou, J. (1980) Optokinetic responses of vestibular nucleus neurons in the cat. Pflugers Archives 384, 31–38.Google Scholar
  6. Carroll, E. W. & Wong-Riley, M. T. T. (1984) Quantitative light and electron microscopic analysis of cytochrome oxidase rich zones in the striate cortex of the squirrel monkey. Journal of Comparative Neurology 222, 1–17.Google Scholar
  7. Chugani, H. T. (1999) Metabolic imaging; a window on brain development and plasticity. The Neuroscientist 5, 29–40.Google Scholar
  8. Cohen, B., Schiff, D. & Buttner, J. (1990) Contribution of the nucleus of the optic tract to optokinetic afternystagmus in the monkey: Clinical implications. In Vision and the Brain (edited by Cohen, B. & Bodiswollner, I.) pp. 233–255. New York: Raven Press.Google Scholar
  9. Collewijn, H. (1975a) Oculomotor areas in the rabbit's midbrain and pretectum. Journal of Neurobiology 6, 3–22.Google Scholar
  10. Collewijn, H. (1975b) Direction selective units in the rabbits nucleus of the optic tract. Brain Research 100, 489–508.Google Scholar
  11. Collewijn, H. & Holstege, G. (1984) Effects of neonatal and late unilateral enucleation on optkinetic responses and optic nerve projections in the rabbit. Experimental Brain Research 57, 138–150.Google Scholar
  12. Deyoe, E. A., Trusk, T. C. & Wong-Riley, M. T. T. (1995) Activity correlates of cytochrome oxidase defined compartments in granular and supragranular layers of primary visual cortex of macaque monkey. Visual Neuroscience 12, 629–639.Google Scholar
  13. Giolli, R. A., Clarke, R. J., Torigoe, Y., Blanks, R. H. I &. Fallon, J. H. (1990) The projection of GABAergic neurons of the medial terminal accessory optic nucleus to the pretectum in the rat. Brazilian Journal of Medical and Biological Research 23, 1349–1352.Google Scholar
  14. Giolli, R. A., Clarke, R. J., Torigoe, Y., Blanks, R. H. I & Fallon, J. H. (1992) GABAergic and non-GABAergic projections of optic nuclei including the visual tegmental relay zone to the nucleus of the optic tract and dorsal terminal accessory optic nucleus in rat. Journal of Comparative Neurology 319, 349–358.Google Scholar
  15. Hevner, R. F. & Wong Riley, M. T. T. (1990) Regulation of cytochrome oxidase protein levels by functional activity in the Macaque visual system. Journal of Neuroscience 10, 1331–1340.Google Scholar
  16. Hoffmann, K. P. & Schoppmann, A. (1975) Retinal input to direction-selective cells in the nucleus tractus opticus in the cat. Brain Research 99, 359–366.Google Scholar
  17. Hoffmann, K. P. & Schoppmann, A. (1981) A quantitative analysis of the direction-specific response of neurons in the cat's nucleus of the optic tract. Experimental Brain Research 42, 146–157.Google Scholar
  18. Horton, J. C. & Hubel, D. H. (1981) Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey. Nature 292, 762–764Google Scholar
  19. Horton, J. C. (1984) Cytochrome oxidase patches: A new cytoarchitetonic feature of monkey visual cortex. Philosophical Transactions of the Royal Society B (London) 304, 199–253.Google Scholar
  20. Horton, J. C. & Hocking, D. R. (1998) Effect of early monocular enucleation upon ocular dominance columns and cytochrome oxidase activity in monkey and human visual cortex. Visual Neuroscience 15, 289–303.Google Scholar
  21. Jacobs, B., Chugani, H. T., Allada, V., Chen, S., Phelps, M. E., Pollack, D.B. & Raleigh, M. J. (1995) Developmental changes in brain metabolism in sedated rhesus macaques and vervet monkeys revealed by positron emisson tomography. Cerebral Cortex 3, 222–233.Google Scholar
  22. Kato, I., Harada, K., Hasegawa, T. & Igarashi, T. (1988) Role of the nucleus of the optic tract of monkeys in optokinetic nystagmus and optokinetic afternystagmus. Brain Research 474, 16–26.Google Scholar
  23. Kageyama, G. H. & Wong Riley, M. (1982) Histochemical localization of cytochrome oxidase in the hippocampus: Correlation with specific neuronal types and afferent pathways. Neuroscience 7, 2337–2361.Google Scholar
  24. Kageyama, G. H. & Wong Riley, M. (1984) The histochemical localization of cytochrome oxidase in the retina and lateral geniculate nucleus of the ferret, cat and monkey, with particular reference to retinal mosaics and ON/OFF center visual channels. Journal of Neuroscience 4, 2445–2459.Google Scholar
  25. Kageyama, G. H. & Wong Riley, M. (1985) An analysis of the cellular localization of cytochrome oxidase in the lateral geniculate nucleus of the adult cat. Journal of Comparative Neurology 242, 338–357.Google Scholar
  26. Kageyama, G. H. & Wong Riley, M. (1986a) The localization of cytochrome oxidase in the LGN and striate cortex of postnatal kittens. Journal of Comparative Neurology 243, 182–184.Google Scholar
  27. Kageyama, G. H. & Wong-Riley, M. (1986b) Differential effect of visual deprivation on cytochrome oxidase levels in major cell classes of the cat LGN. Journal of Comparative Neurology 246, 212–237.Google Scholar
  28. Kennedy, H., Bullier, J. & Dehay, C. (1985) Cytochrome oxidase activity in the striate cortex and lateral geniculate nucleus of the newborn and adult monkey. Experimental Brain Research 61, 204–209.Google Scholar
  29. Kling, A. (1965) Behavioral and somatic development following lesions of the amygdala in the cat. Journal of Psychiatric Research 3, 263–273.Google Scholar
  30. Land, P. (1987) Dependence of cytochrome oxidase activity in the rat lateral geniculate nucleus on retinal innervation. Journal of Comparative Neurology 262, 78–89.Google Scholar
  31. Luo, X. G., Kong, X. Y. & Wong-Riley, M. T. T. (1991) Effect of monocular enucleation or impulse blockade on gamma-aminobutyric acid and cytochrome oxidase levels in neurons of the adult cat lateral geniculate nucleus. Visual Neuroscience 6, 55–68.Google Scholar
  32. Mendez-Otero, R., Cavalcante, L. A., Rocha-Miranda, C. E., Bernardes, R. F. & Barradas, P. C. R. (1985) Growth and restriction of the ipsilateral retinocollicular projection in the opossum. Developmental Brain Research 18, 199–210.Google Scholar
  33. Nasi, J. P., Volchan, E., Tecles, M. T., Bernardes, R. F. & Rocha-Miranda, C. E. (1997) The horizontal optokinetic reflex of the opossum (Didelphis marsupialis aurita). Physiological and anatomical studies in normal and early monoenucleated specimens. Vision Research 37, 1207–1216.Google Scholar
  34. Nie, F. & Wong Riley, M. T. T. (1995) Double labeling of GABA and Cytochrome oxidase in the macaque visual cortex: Quantitative EM analysis. Journal of Comparative Neurology 356, 115–131.Google Scholar
  35. Nie, F. & Wong-Riley, M. T. T. (1996a) Differential glutamatergic innervation in cytochrome oxidase-rich and-poor regions of the macaque striate cortex: Quantitative EM analysis of neurons and neuropil. Journal of Comparative Neurology 369, 571–590.Google Scholar
  36. Nie, F. & Wong-Riley, M. T. T. (1996b) Metabolic and neurochemical plasticity of gamma-aminobutyric acid immuno reactive neurons in the adult macaque striate cortex following monocular impulse blockade: Quantitative electron microscopic analysis. Journal of Comparative Neurology 370, 350–366.Google Scholar
  37. Oswaldo-Cruz, E. & Rocha-Miranda, C. E. (1968) The brain of the opossum (Didelphis marsupialis). A cytochitectonic atlas in stereotaxic coordinates (edited by Oswaldo-Cruz, E. & Rocha-Miranda. C. E.) pp. 1–99. Rio de Janeiro: Instituto de Biofísica da U.F.R.J.Google Scholar
  38. Payne, B. R. & Lomber, S. G. (1996) Age dependent modification of cytochrome oxidase activity in the cat dorsal lateral geniculate nucleus following removal of primary visual cortex. Visual Neuroscience 13, 805–816.Google Scholar
  39. Pereira, Jr. A., Volchan, E., Bernardes, R. F. & Rocha-Miranda, C. E. (1994) Binocularity in the nucleus of the optic tract of the opossum. Experimental Brain Research 102, 327–338.Google Scholar
  40. Pereira, Jr. A., Volchan, E., ' Vargas, C. D., Penetra, L. & Rocha-Miranda, C. E. (2000) Cortical and subcortical influences on the nucleus of the optic tract of the opossum. Neuroscience 95, 953–963.Google Scholar
  41. Purves, D. & Lamantia, A. (1993) Development of blobs in the visual cortex of Macaques. Journal of Comparative Neurology 334, 169–175.Google Scholar
  42. Reber, A., Lannou, J. & Hess, B. J. M. (1989) Development of optokinetic neuronal responses in the pretectum and horizontal optokinetic nystagmus in unilaterally enucleated rats. Archives Italiennes de Biologie 127, 225–242.Google Scholar
  43. Precht, W., Montarolo, P. G. & Strata. P. (1980) The role of crossed and uncrossed retinal fibers in mediating the horizontal optokinetic nystagmus in the cat. Neuroscience Letters 17, 39–42.Google Scholar
  44. Robertson, R. T. (1983) Efferents of the pretectal complex: Separate populations of neurons project to lateral thalamus and to inferior olive. Brain Research 258, 91–95.Google Scholar
  45. Rosa, M. G. P., Gattass, R. & Soares, J. G. M. (1991) A quantitative analysis of cytochrome oxidaserich patches in the primary visual cortex of cebus monkeys: Topographic distribution and effects of late monocular enucleation. Experimental Brain Research 84, 195–209.Google Scholar
  46. Schiff, D., Cohen, B. & Raphan, T. (1988) Nystagmus induced by stimulation of the optic tract in the monkey. Experimental Brain Research 70, 1–14.Google Scholar
  47. Schiff, D., Cohen, B., Buttner-Ennever, J. & Matsuo V. (1990) Effects of lesions of the nucleus of the optic tract on optokinetic nystagmus and afternystagmus in the monkey. Experimental Brain Research 79, 225–239.Google Scholar
  48. Schiff, D. & Schmidt, M. (1990) Anatomical and histochemical characterization of nucleus of the optic tract (NOT) efferent populations in the rat. European Journal of Neuroscience Supplement 3, 243.Google Scholar
  49. Silverman, M. S., Grosof, D. H., de Valois, R. L. & Elfar, S. D. (1989) Spacial frequency organization in primate striate cortex. Proceedings of the National Academy of Sciences (USA) 86, 711–715.Google Scholar
  50. Simpson, J. I., Giolli, R. A. & Blanks, R. H. I. (1988) The pretectal nuclear complex and the accessory optic system. In Neuroanatomy of the Oculomotor System (edited by Buttner-Ennever, J. A.) pp. 335–364. Amsterdam: Elsevier.Google Scholar
  51. Tai, T. C., Tompa, J., Nobrega, J. N. & Adamson, S. L. (1995) Changes in cytochromeoxidase activity in the fetal, newborn and adult ovine brainstem. Developmental Brain Research 86, 7–15.Google Scholar
  52. Trusk, T. C., Kaboord, W. S. & Wong-Riley, M. T. T. (1990) Effects of monocular enucleation, tetrodotoxin and lid suture on cytochrome-oxidase reactivity in supragranular puffs of adult macaque striate cortex. Visual Neuroscience 4, 195–204.Google Scholar
  53. Vargas, C. D., Volchan, E., HokoÇ, J. N., Pereira, A., Bernardes, R. F. & Rochamiranda, C. E. (1997) On the functional anatomy of the nucleus of the optic tract-dorsal terminal nucleus commissural connection in the opossum (Didelphis marsupialis aurita). Neuroscience 76, 313–321.Google Scholar
  54. Vargas, C. D., Volchan, E., Nasi, J. P., Bernardes, R. F. & Rocha-Miranda, C. E. (1996) The nucleus of the optic tract (NOT) and the dorsal terminal nucleus (DTN) of opossums (Didelphis marsupialis aurita). Brain, Behavior and Evolution 48, 1–15.Google Scholar
  55. Vargas, C. D., Sousa, A. O., Bittencourt, F. L. R., Santos, C. M., Pereira, Jr. A., Bernardes, R. F., Rocha-Miranda, C. E. & Volchan, E. (1998) Cytochrome oxidase and NADPH-Diaphorase on the afferent relay branch of the optokinetic reflex in the opossum. Journal of Comparative Neurolology 398, 206–224.Google Scholar
  56. Volchan, E., Rocha-Miranda, C. E., PicanÇo-Diniz, C. W., Zinsmeisser, B., Bernardes, R. F. & Franca, J. G. (1989) Visual response properties of the pretectal nucleus of the optic tract in the opossum. Experimental Brain Research 78, 380–386.Google Scholar
  57. Wong-Riley, M. (1979) Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Research 171, 11–28.Google Scholar
  58. Wong-Riley, M. T. T. (1989) Cytochrome oxidase: An endogenous metabolic marker of neuronal activity. Trends in Neurosciences 12, 94–102.Google Scholar
  59. Wong-Riley, M. & Carroll, E. W. (1984) Effect of impulse blockade on cytochrome oxidase activity in monkey visual system. Nature 307, 262–264.Google Scholar
  60. Wong-Riley, M. T. T., Merzenich, M. M. & Leake, P. A. (1978) Changes in endogenous enzymatic reactivity to DAB induced by neuronal inactivity. Brain Research 141, 185–192.Google Scholar
  61. Wong-Riley, M. T. T. & Norton, T. T. (1988) Histochemical localization of cytochrome oxidase activity in the visual system of the tree shrew: Normal patterns and the effect of retinal impulse blockade. Journal of Comparative Neurology 272, 562–578.Google Scholar
  62. Wong-Riley, M. & Riley, D. A. (1983) The effect of impulse blockage on cytochrome oxidase activity in the cat visual system. Brain Research 261, 185–193.Google Scholar
  63. Wong Riley, M. T. T., Tripathi, S. C., Trusk, T. C. & Hope, D. A. (1989) Effect of retinal impulse blockage on cytochrome oxidase-rich zones in the macaque striate cortex: 1. Quantitative electronmicroscopic (EM) analysis of neurons. Visual Neuroscience 2, 483–497.Google Scholar
  64. Wong Riley, M. T. T., Hevner, R. F., Cutlan, R., Earnest, M., Egan, R., Frost, J. & Nguyen, T. (1993) Cytochrome oxidase in the human visual cortex: Distribution in the developing and the adult brain.Visual Neuroscience 10, 41–58.Google Scholar
  65. Wong Riley, M. T. T., Trusk, T. C., Kaboord, W. & Huang, Z. (1994) Effect of retinal impulse blockage on cytochrome oxidase-poor interpuffs in the macaque striate cortex: Quantitative EM analysis of neurons. Journal of Neurocytology 23, 533–553.Google Scholar
  66. Wood, C. C., Spear, P. D. & Braun, J. J. (1973) Direction-specific deficits in horizontal optokinetic nystagmus following removal of visual cortex in the cat. Brain Research 60, 231–237.Google Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • C. D. Vargas
    • 1
  • A. O. Sousa
    • 1
  • C. M. Santos
    • 1
  • A. PereiraJr.
    • 1
  • R. F. Bernardes
    • 1
  • C. E. Rocha-Miranda
    • 1
  • E. Volchan
    • 1
  1. 1.Laboratory of Neurobiology II, Institute of Biophysics Carlos Chagas FilhoFederal University of Rio de JaneiroRio de Janeiro, R.J.Brazil

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