Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-23T06:56:16.511Z Has data issue: false hasContentIssue false

Effect of retinal impulse blockage on cytochrome oxidase-rich zones in the macaque striate cortex: II. Quantitative electron-microscopic (EM) analysis of neuropil

Published online by Cambridge University Press:  02 June 2009

Margaret T. T. Wong-Riley
Affiliation:
Department of Anatomy and Cellular Biology, Medical College of Wisconsin, Milwaukee, Wisconsin
Thomas C. Trusk
Affiliation:
Department of Anatomy and Cellular Biology, Medical College of Wisconsin, Milwaukee, Wisconsin
Satish C. Tripathi
Affiliation:
Department of Anatomy and Cellular Biology, Medical College of Wisconsin, Milwaukee, Wisconsin
Daniel A. Hoppe
Affiliation:
Department of Anatomy and Cellular Biology, Medical College of Wisconsin, Milwaukee, Wisconsin

Abstract

Unilateral retinal impulse blockage with tetrodotoxin (TTX) induces reversible shrinkage and decreased cytochrome oxidase (CO) activity in alternate rows of supragranular, CO-rich puffs in the adult macaque striate cortex (Wong-Riley & Carroll, 1984b: Carroll & Wong-Riley, 1987). The present study extended the findings to the electron-microscopic (EM) level to determine if various neuropil profiles in control puffs exhibit heterogeneous levels of CO activity, and whether specific processes were more susceptible to intravitreal TTX than others.

Within the neuropil of control puffs, 60% of the total mitochondrial population resided in dendrites, and the majority of dendritic mitochondria were highly reactive for CO. Axon terminals forming symmetrical synapses also contained darkly reactive mitochondria, whereas those forming asymmetrical synapses possessed very few and mainly lightly reactive mitochondria. Unmyelinated axon trunks, myelinated axons, and glia all exhibited low levels of CO activity. Synaptic count revealed a 3:1 ratio of asymmetrical to symmetrical synapses.

Intravitreal TTX for 2–4 weeks adversely affects dendrites and symmetrical terminals much more so than other neuropil processes. There was a general decrease in darkly and moderately reactive mitochondria and an increase in lightly reactive mitochondria throughout the puffs, especially in dendrites. This indicates that afferent blockade is more detrimental to processes of higher metabolic activity. Changes also differed between central and peripheral regions of puffs, and indications of axonal and synaptic reorganization were more evident in the latter. Thus, stabilization of neuronal structure and synapses appears to be activity-dependent even in the adult. A working model of these metabolic and morphological responses to chronic TTX is proposed.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1989

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Baisden, R.H., Polley, E.H., Goodman, D.C. & Wolf, E.D. (1980). Absence of sprouting by retinogeniculate axons after chronic focal lesions in the adult cat retina. Neuroscience Letters 17, 3338.CrossRefGoogle ScholarPubMed
Beaulieu, C. & Colonnier, M. (1987). Effect of the richness of the environment on the cat visual cortex. Journal of Comparative Neurology 266, 478494.CrossRefGoogle ScholarPubMed
Blakemore, C., Garey, L.J. & Vital-Durand, F. (1978). The physiological effects of monocular deprivation and their reversal in the monkey's visual cortex. Journal of Physiology 283, 223262.CrossRefGoogle ScholarPubMed
Blasdel, G.G. & Lund, J.S. (1983). Termination of afferent axons in macaque striate cortex. Journal of Neuroscience 3, 13891413.CrossRefGoogle ScholarPubMed
Brown, M.C., Holland, R.L. & Ironton, R. (1980). Nodal and terminal sprouting from motor nerves in fast and slow muscles of the mouse. Journal of Physiology 306, 493510.CrossRefGoogle ScholarPubMed
Brown, M.C. & Ironton, R. (1978). Sprouting and regression of neuromuscular synapses in partially denervated mammalian muscles. Journal of Physiology 278, 325348.CrossRefGoogle ScholarPubMed
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, 117.CrossRefGoogle ScholarPubMed
Carroll, E.W. & Wong-Riley, M. (1987). Recovery of cytochrome oxidase activity in the adult macaque visual system after termination of impulse blockage due to tetrodotoxin. Society for Neuroscience Abstracts 13, 1046.Google Scholar
Cotman, C.W. (1978). Neuronal Plasticity. New York: Raven Press.Google Scholar
Cotman, C.W. (1985). Synaptic Plasticity. New York: Guilford.Google Scholar
Creutzfeldt, O.D. (1975). Neurophysiological correlates of different functional states of the brain. In Brain Work. Alfred Benzon Symposium, VIII, ed. Ingvar, D.H. & Lassen, N.A., pp. 2146. New York: Academic Press.Google Scholar
Dietrich, W.D., Durham, D.B., Lowry, O.H. & Woolsey, T.A. (1981). Quantitative histochemical effects of whisker damage on single identified cortical barrels in the adult mouse. Journal of Neuroscience 1, 929935.CrossRefGoogle ScholarPubMed
Dubin, M.W., Stark, L.A. & Archer, S.M. (1986). A role for actionpotential activity in the development of neuronal connections in the kitten retinogeniculate pathway. Journal of Neuroscience 6, 10211036.CrossRefGoogle ScholarPubMed
Fitzpatrick, D., Itoh, K. & Diamond, I.T. (1983). The laminar organization of the lateral geniculate body and the striate cortex in the squirrel monkey (Saimiri sciureus). Journal of Neuroscience 3, 673702.CrossRefGoogle ScholarPubMed
Franck, J.I. (1980). Functional reorganization of cat somatic sensorymotor cortex (SM I) after selective dorsal root rhizotomies. Brain Research 186, 458462.CrossRefGoogle Scholar
Goldberger, M. (1977). Locomotor recovery after unilateral hindlimb deafferentation in cats. Brain Research 123, 5974.CrossRefGoogle ScholarPubMed
Gurney, M.E. (1984). Suppression of sprouting at the neuromuscular junction by immune sera. Nature 307, 546548.CrossRefGoogle ScholarPubMed
Hendrickson, A.E., Movshon, J.A., Eggers, H.M., Gizzi, M.S., Boothe, R.G. & Kiorpes, L. (1987). Effects of early unilateral blur on the macaque's visual system. II. Anatomical observations. Journal of Neuroscience 7, 13271339.CrossRefGoogle ScholarPubMed
Hendry, S.H.C. & Jones, E.G. (1986). Reduction in number of immunostained GABAergic neurones in deprived-eye dominance columns of monkey area 17. Nature 320, 750753.CrossRefGoogle ScholarPubMed
Hendry, S.H.C., Jones, E.G. & Burstein, N. (1987). Activity-dependent regulation of tachykinin-like immunoreactivity in visual cortical neurons: increased and decreased immunostaining in the cytochrome oxidase patches of monocularly aphakic monkeys. Society for Neuroscience Abstracts 13, 358.Google Scholar
Hendry, S.H.C. & Kennedy, M.B. (1986). Immunoreactivity for a calmodulin-dependent protein kinase is selectively increased in macaque striate cortex after monocular deprivation. Proceedings of the National Academy of Science of the U.S.A. 83, 15361540.CrossRefGoogle ScholarPubMed
Hiltgen, G. & Wong-Riley, M. (1986). Quantitative EM analysis of the effect of retinal impulse blockage on cytochrome oxidase activity in lamina IVC of macaque striate cortex. Society for Neuroscience Abstracts 12, 130.Google Scholar
Horton, J.C. (1984). Cytochrome oxidase patches: a new cytoarchitectonic feature of monkey visual cortex. Philosophical Transactions of the Royal Society B (London) 304, 199253.Google ScholarPubMed
Hubel, D.H., Wiesel, T.N. & Levay, S. (1977). Plasticity of ocular dominance columns in monkey striate cortex. Philosophical Transactions of the Royal Society B (London) 278, 377409.Google ScholarPubMed
Itaya, S.K., Itaya, P.W. & Van Hoesen, G.W. (1984). Intracortical termination of the retino-geniculo-striate pathway studied with transsynaptic tracer (wheat germ agglutinin-horseradish peroxidase) and cytochrome oxidase staining in the macaque monkey. Brain Research 304, 303310.CrossRefGoogle ScholarPubMed
Kageyama, G.H. & Wong-Riley, M.T.T. (1982). Histochemical localization of cytochrome oxidase in the hippocampus: correlation with specific neuronal types and afferent pathways. Neuroscience 7, 23372361.CrossRefGoogle ScholarPubMed
Kageyama, G.H. & Wong-Riley, M.T.T. (1985). An analysis of the cellular localization of cytochrome oxidase in the lateral geniculate nucleus of the adult cat. Journal of Comparative Neurology 242, 338357.CrossRefGoogle ScholarPubMed
Kiorpes, L., Boothe, R.G., Hendrickson, A.E., Movshon, J.A., Eggers, H.M. & Gizzi, M.S. (1987). Effects of early unilateral blur on the macaque's visual system. I. Behavior observations. Journal of Neuroscience 7, 13181326.CrossRefGoogle Scholar
LeVay, S., Wiesel, T.N. & Hubel, D.H. (1980). The development of ocular dominance columns in normal and visually deprived monkeys. Journal of Comparative Neurology 191, 151.CrossRefGoogle ScholarPubMed
Liu, C.N. & Chambers, W.W. (1958). Intraspinal sprouting of dorsal root axons. Archives of Neurology and Psychiatry 79, 4661.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1982). Thalamic inputs to cytochrome oxidase-rich regions in monkey visual cortex. Proceedings of the National Academy of Sciences of the U.S.A. 79, 60986101.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1983). Specificity of cortico-cortical connections in monkey visual system. Nature 304, 531534.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1984). Specificity of intrinsic connections in primate primary visual cortex. Journal of Neuroscience 4, 28302835.CrossRefGoogle ScholarPubMed
Lowry, O.H., Roberts, N.R., Leiner, K.Y., Wu, M.-L., Farr, A.L. & Albers, R.W. (1954). The quantitative histochemistry of brain. III. Ammon's horn. Journal of Biological Chemistry 207, 3949.CrossRefGoogle ScholarPubMed
Lund, R.D. (1978). Development and Plasticity of the Brain. New York: Oxford Press.Google Scholar
Lund, R.D. & Lund, J.S. (1971). Synaptic adjustment after deafferentation of the superior colliculus of the rat. Science 171, 804807.CrossRefGoogle ScholarPubMed
Merrill, E.G. & Wall, P.D. (1978). Plasticity of connection in the adult nervous system. In Neuronal Plasticity, ed. Cotman, C.W., pp. 97111. New York: Raven Press.Google Scholar
Merzenich, M.M., Kaas, J.H., Wall, J., Nelson, R.J., Sur, M. & Felleman, D. (1983). Topographical reorganization of somatosensory cortical areas 3B and 1 in adult monkeys following restricted deafferentation. Neuroscience 8, 3355.CrossRefGoogle ScholarPubMed
Mjaatvedt, A.T. & Wong-Riley, M.T.T. (1988). The relationship between synaptogenesis and cytochrome oxidase activity in Purkinje cells of the developing rat cerebellum. Journal of Comparative Neurology 277, 155182.CrossRefGoogle ScholarPubMed
Movshon, J.A., Eggers, H.M., Gizzi, M.S., Hendrickson, A.E., Kiorpes, L. & Boothe, R.G. (1987). Effects of early unilateral blur on the macaque's visual system. III. Physiological observations. Journal of Neuroscience 7, 13401351.CrossRefGoogle ScholarPubMed
O'Leary, D.D.M., Fawcett, J.W. & Cowan, W.M. (1986). Topographic targeting errors in the retinocollicular projection and their elimination by selective ganglion cell death. Journal of Neuroscience 6, 36923705.CrossRefGoogle ScholarPubMed
Pons, T.P., Garraghty, P.E. & Mishkin, M. (1988). Lesion-induced plasticity in the second somatosensory cortex of adult macaques. Proceedings of the National Academy of Sciences of the U.S.A. 85, 52795281.CrossRefGoogle ScholarPubMed
Raisman, G. (1969). Neuronal plasticity in the septal nuclei of the adult rat. Brain Research 14, 2548.CrossRefGoogle ScholarPubMed
Riccio, R.V. & Matthews, M.A. (1985 a). Effects of intraocular tetrodotoxin on dendritic spines in the developing rat visual cortex: a Golgi analysis. Developmental Brain Research 19, 173182.CrossRefGoogle Scholar
Riccio, R.V. & Matthews, M.A. (1985b). The postnatal development of the rat primary visual cortex during optic nerve impulse blockade by intraocular tetrodotoxin: a quantitative electron-microscopic analysis. Developmental Brain Research 20, 5568.CrossRefGoogle Scholar
Riley, D.A. & Fahlman, C.S. (1985). Colchicine-induced differential sprouting of the endplates on fast and slow muscle fibers in rat extensor digitorum longus, soleus, and tibialis anterior muscles. Brain Research 329, 8395.CrossRefGoogle ScholarPubMed
Robbins, N. (1980). Plasticity at the mature neuromuscular junction. Trends in Neurosciences 3, 120122.CrossRefGoogle Scholar
Rodin, B.E., Sampogna, S.L. & Kruger, L. (1983). An examination of intraspinal sprouting in dorsal root axons with the tracer horseradish peroxidase. Journal of Comparative Neurology 215, 187198.CrossRefGoogle ScholarPubMed
Rotshenker, S. (1979). Synapse formation in intact innervated cutaneous-pectoris muscles of the frog following denervation of the opposite muscle. Journal of Physiology 292, 535547.CrossRefGoogle ScholarPubMed
Rotshenker, S. & Tal, M. (1985). The transneuronal induction of sprouting and synapse formation in intact mouse muscles. Journal of Physiology 360, 387396.CrossRefGoogle ScholarPubMed
Sherman, S.M. & Spear, P.D. (1982). Organization of the visual pathways in normal and visually deprived cats. Physiological Review 62, 738855.CrossRefGoogle ScholarPubMed
Singer, W., Tretter, F. & Yinon, U. (1982). Evidence for long-term functional plasticity in the visual cortex of adult cats. Journal of Physiology 324, 239248.CrossRefGoogle ScholarPubMed
Stelzner, D.J. & Keating, E.G. (1977). Lack of intralaminar sprouting of retinal axons in monkey LGN. Brain Research 126, 201210.CrossRefGoogle ScholarPubMed
Stryker, M.P. & Harris, W.A. (1986). Binocular impulse blockade prevents the formation of ocular dominance columns in cat visual cortex. Journal of Neuroscience 6, 21172133.CrossRefGoogle ScholarPubMed
Trusk, T.C. & Wong-Riley, M.T.T. (1987). Effect of monocular lid suture, enucleation, and retinal impulse blockage on the volume of cytochrome oxidase-rich puffs in the adult macaque striate cortex. Society for Neuroscience Abstracts 13, 1046.Google Scholar
Von Noorden, G.K. & Crawford, M.L.J. (1978). Morphological and physiological changes in the monkey visual system after short-time lid closure. Investigative Ophthalmology 17, 762768.Google Scholar
Weber, J.T., Huerta, M.F., Kaas, J.H. & Harting, J.K. (1983). The projections of the lateral geniculate nucleus of the squirrel monkey: studies of the interlaminar zones and the S layers. Journal of Comparative Neurology 213, 135145.CrossRefGoogle ScholarPubMed
Weddell, G., Guttmann, L. & Guttmann, E. (1941). The local extension of nerve fibers into denervated areas of skin. Journal of Neurological Psychiatry 4, 206225.CrossRefGoogle ScholarPubMed
Wong-Riley, M. (1979). Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Research 171, 1128.CrossRefGoogle ScholarPubMed
Wong-Riley, M. (1989). Cytochrome oxidase: an endogenous metabolic marker of neuronal activity. Trends in Neurosciences 12, 94101.CrossRefGoogle ScholarPubMed
Wong-Riley, M.T.T. & Carroll, E.W. (1984 a). Quantitative lightand electron-microscopic analysis of cytochrome oxidase-rich zones in VII prestriate cortex of the squirrel monkey. Journal of Comparative Neurology 111, 1837.CrossRefGoogle Scholar
Wong-Riley, M. & Carroll, E.W. (1984 b). The effect of impulse blockage on cytochrome oxidase activity in the monkey visual system. Nature 307, 262264.CrossRefGoogle ScholarPubMed
Wong-Riley, M.T.T. & Kageyama, G. (1986). Localization of cytochrome oxidase in the spinal cord and dorsal root ganglia, with quantitative analysis of ventral horn cells in monkeys. Journal of Comparative Neurology 245, 4161.CrossRefGoogle ScholarPubMed
Wong-Riley, M.T., Merzenich, M.M. & Leake, P.A. (1978). Changes in endogenous enzymatic reactivity to DAB induced by neuronal inactivity. Brain Research 141, 185192.CrossRefGoogle ScholarPubMed
Wong-Riley, M. & Riley, D.A. (1983). The effect of impulse blockage on cytochrome oxidase activity in the cat visual system. Brain Research 261, 185193.CrossRefGoogle ScholarPubMed
Wong-Riley, M., Tripathi, S. & Hoppe, D. (1986). Quantitative EM analysis of the effect of retinal impulse blockage on cytochrome oxidase-rich zones in the macaque striate cortex. Society for Neuroscience Abstracts 12, 130.Google Scholar
Wong-Riley, M.T.T., Tripathi, S.C., Trusk, T.C. & Hoppe, D.A. (1989). Effect of retinal impulse blockage on cytochrome oxidaserich zones in the macaque striate cortex. I. Quantitative electronmicroscopic (EM) analysis of neurons. Visual Neuroscience 2, 483.CrossRefGoogle ScholarPubMed
Wong-Riley, M.T.T. & Welt, C. (1980). Histochemical changes in cytochrome oxidase of cortical barrels following vibrissal removal in neonatal and adult mice. Proceedings of the National Academy of Sciences of the U.S.A. 77, 23332337.CrossRefGoogle Scholar