Neurochemical correlates of cortical plasticity after unilateral elevated intraocular pressure in a primate model of glaucoma.

PURPOSE To examine the time course of changes in the expression patterns of several synaptic plasticity markers in the primary visual cortex after unilateral elevated intraocular pressure (IOP) in a primate model of glaucoma. METHODS A monkey model of experimental glaucoma was combined with immunohistochemical and histochemical methods to assess changes in expression patterns and metabolic activity of cortical neurons in V1. RESULTS Experimental unilateral glaucoma altered the spatial and temporal distribution of several neurochemicals associated with cortical plasticity in V1 of the primate. Within-animal comparisons of immunohistochemical studies revealed that GABAa receptor protein and GAP-43 were significantly lower in glaucomatous versus normal eye bands after 2, 4, and 7 months of elevated IOP. SYN immunoreactivity was also lower in the glaucomatous versus the normal eye bands but only at 4 months of elevated IOP. CAMKIIalpha immunoreactivity levels were higher in the glaucomatous versus the normal eye bands. Between-animal comparisons revealed that the levels of GAP-43 and SYN were upregulated, whereas levels of GABAa receptor protein were downregulated, in glaucomatous eyes when compared with levels in the visual cortex of normal animals. CONCLUSIONS Unilateral elevation of IOP affects both the metabolic activity of cortical neurons and the expressed levels of GAP-43, SYN, GABAa receptor protein, and CAMKIIalpha, as measured immunohistochemically in the primary visual cortex of adult monkeys. Because these neurochemicals are thought to be necessary for synaptic plasticity, their redistribution may support functional recovery of cortical neurons after damage to retinal ganglion cells induced by elevated IOP.

[1]  J. Horton,et al.  Cytochrome oxidase patches: a new cytoarchitectonic feature of monkey visual cortex. , 1984, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[2]  C. Gall,et al.  Differential effects of monocular deprivation on glutamic acid decarboxylase and type II calcium-calmodulin-dependent protein kinase gene expression in the adult monkey visual cortex [published erratum appears in J Neurosci 1991 May;11(5):following Table of Contents] , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  H. Mohler,et al.  GABAA receptor subunit immunoreactivity in primate visual cortex: distribution in macaques and humans and regulation by visual input in adulthood , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  L. Benowitz,et al.  Increased transport of 44,000- to 49,000-dalton acidic proteins during regeneration of the goldfish optic nerve: a two-dimensional gel analysis , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  P. Kaufman,et al.  Intraocular pressure measurement in cynomolgus monkeys. Tono-Pen versus manometry. , 1996, Investigative ophthalmology & visual science.

[6]  M. Wong-Riley.  Cytochrome oxidase: an endogenous metabolic marker for neuronal activity , 1989, Trends in Neurosciences.

[7]  D. Gaasterland,et al.  Experimental glaucoma in the rhesus monkey. , 1974, Investigative ophthalmology.

[8]  J. Kaas,et al.  Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina. , 1990, Science.

[9]  C. Gall,et al.  Decreased expression of the alpha subunit of Ca2+/ calmodulin-dependent protein kinase type II mRNA in the adult rat CNS following recurrent limbic seizures. , 1995, Brain research. Molecular brain research.

[10]  E. Jones,et al.  Differential and Time-Dependent Changes in Gene Expression for Type II Calcium/Calmodulin-Dependent Protein Kinase, 67 kDa Glutamic Acid Decarboxylase, and Glutamate Receptor Subunits in Tetanus Toxin-Induced Focal Epilepsy , 1997, The Journal of Neuroscience.

[11]  C. Pantev,et al.  Cortical reorganization in patients with high frequency cochlear hearing loss , 2001, Hearing Research.

[12]  H. Quigley,et al.  Chronic experimental glaucoma in primates. II. Effect of extended intraocular pressure elevation on optic nerve head and axonal transport. , 1980, Investigative ophthalmology & visual science.

[13]  C. Gilbert,et al.  Topographic reorganization in the striate cortex of the adult cat and monkey is cortically mediated , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  Abel Lajtha,et al.  Handbook of Neurochemistry , 2013, Springer US.

[15]  E. G. Jones,et al.  Distribution and plasticity of immunocytochemically localized GABAA receptors in adult monkey visual cortex , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  A. Hendrickson,et al.  Enucleation demonstrates ocular dominance columns in Old World macaque but not in New World squirrel monkey visual cortex , 1985, Brain Research.

[17]  Fred H. Gage,et al.  Reactive synaptogenesis assessed by synaptophysin immunoreactivity is associated with GAP-43 in the dentate gyrus of the adult rat , 1991, Experimental Neurology.

[18]  C. Gall,et al.  Contrasting patterns in the localization of glutamic acid decarboxylase and Ca2+ /calmodulin protein kinase gene expression in the rat centrat nervous system , 1992, Neuroscience.

[19]  A. Safran,et al.  From cortical plasticity to unawareness of visual field defects. , 1999, Journal of neuro-ophthalmology : the official journal of the North American Neuro-Ophthalmology Society.

[20]  P. Kaufman,et al.  "Minified" Goldmann applanating prism for tonometry in monkeys and humans. , 1980, Archives of ophthalmology.

[21]  E. Nedivi,et al.  A protein associated with axon growth, GAP-43, is widely distributed and developmentally regulated in rat CNS , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  J. Freeman,et al.  Changes in axonally transported proteins during axon regeneration in toad retinal ganglion cells , 1981, The Journal of cell biology.

[23]  A. Bignami.  Central nervous system plasticity and repair , 1985 .

[24]  M K Bennett,et al.  Biochemical and immunochemical evidence that the "major postsynaptic density protein" is a subunit of a calmodulin-dependent protein kinase. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[25]  S. Hendry,et al.  Differential gene expression for glutamic acid decarboxylase and type II calcium-calmodulin-dependent protein kinase in basal ganglia, thalamus, and hypothalamus of the monkey , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  W. Green,et al.  Blood vessels of the glaucomatous optic disc in experimental primate and human eyes. , 1984, Investigative ophthalmology & visual science.

[27]  T. Wiesel,et al.  Receptive field dynamics in adult primary visual cortex , 1992, Nature.

[28]  J. Skene,et al.  Axonally transported proteins associated with axon growth in rabbit central and peripheral nervous systems , 1981, The Journal of cell biology.

[29]  S. Hendry,et al.  Activity-dependent regulation of GABA expression in the visual cortex of adult monkeys , 1988, Neuron.

[30]  Paul De Koninck,et al.  Interaction with the NMDA receptor locks CaMKII in an active conformation , 2001, Nature.

[31]  P. Kaufman,et al.  Loss of neurons in magnocellular and parvocellular layers of the lateral geniculate nucleus in glaucoma. , 2000, Archives of ophthalmology.

[32]  J. Boyd,et al.  Laminar and columnar patterns of geniculocortical projections in the cat: Relationship to cytochrome oxidase , 1996, The Journal of comparative neurology.

[33]  E. G. Jones,et al.  Reduction in number of immunostained GABAergic neurones in deprived-eye dominance columns of monkey area 17 , 1986, Nature.

[34]  T. Staehelin,et al.  Monoclonal antibodies reveal structural homogeneity of gamma-aminobutyric acid/benzodiazepine receptors in different brain areas. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[35]  E. G. Jones,et al.  Localization of alpha type II calcium calmodulin-dependent protein kinase at glutamatergic but not gamma-aminobutyric acid (GABAergic) synapses in thalamus and cerebral cortex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[36]  P. Kaufman,et al.  Experimental glaucoma and cell size, density, and number in the primate lateral geniculate nucleus. , 2000, Investigative ophthalmology & visual science.

[37]  D. Schreyer,et al.  Fate of GAP-43 in ascending spinal axons of DRG neurons after peripheral nerve injury: delayed accumulation and correlation with regenerative potential , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  M. Reynolds,et al.  GAP-43 expression in primary sensory neurons following central axotomy , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  R S Harwerth,et al.  Experimental glaucoma in primates: changes in cytochrome oxidase blobs in V1 cortex. , 2001, Investigative ophthalmology & visual science.

[40]  M. Fishman,et al.  A membrane-targeting signal in the amino terminus of the neuronal protein GAP-43 , 1989, Nature.

[41]  P. Hoffman.  Expression of GAP-43, a rapidly transported growth-associated protein, and class II beta tubulin, a slowly transported cytoskeletal protein, are coordinated in regenerating neurons , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  D. Hubel,et al.  Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey , 1981, Nature.

[43]  M. Wong-Riley,et al.  Effect of impulse blockage on cytochrome oxidase activity in monkey visual system , 1984, Nature.

[44]  G. Orban,et al.  Long-term effects of retinal lesions on growth-associated protein 43 (GAP-43) expression in the visual system of adult cats , 1996, Neuroscience Letters.

[45]  P. Schoch,et al.  Purified benzodiazepine receptor retains modulation by GABA. , 1983, European journal of pharmacology.

[46]  J. Horton,et al.  Intrinsic Variability of Ocular Dominance Column Periodicity in Normal Macaque Monkeys , 1996, The Journal of Neuroscience.

[47]  C. Gilbert,et al.  Axonal sprouting accompanies functional reorganization in adult cat striate cortex , 1994, Nature.

[48]  P. Greengard,et al.  Evidence that the major postsynaptic density protein is a component of a Ca2+/calmodulin-dependent protein kinase. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[49]  J. Bronstein,et al.  Long-lasting decreases of type II calmodulin kinase expression in kindled rat brains , 1992, Brain Research.

[50]  M. Wong-Riley,et al.  Effects of monocular enucleation, tetrodotoxin, and lid suture on cytochrome-oxidase reactivity in supragranular puffs of adult macaque striate cortex , 1990, Visual Neuroscience.

[51]  T. Voigt,et al.  Synaptophysin immunohistochemistry reveals inside‐out pattern of early synaptogenesis in ferret cerebral cortex , 1993, The Journal of comparative neurology.

[52]  R S Harwerth,et al.  Glaucoma in primates: cytochrome oxidase reactivity in parvo- and magnocellular pathways. , 2000, Investigative ophthalmology & visual science.

[53]  M. Fishman,et al.  Cloning of complementary DNA for GAP-43, a neuronal growth-related protein. , 1987, Science.

[54]  M. Wong-Riley,et al.  Effect of retinal impulse blockage on cytochrome oxidase-rich zones in the macaque striate cortex: I. Quantitative electron-microscopic (EM) analysis of neurons , 1989, Visual Neuroscience.

[55]  I. Martin,et al.  GABA RECEPTORS , 2002 .

[56]  D. J. Felleman,et al.  Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation , 1983, Neuroscience.

[57]  M. Fishman,et al.  Cloning of human GAP 43: Growth association and ischemic resurgence , 1988, Neuron.

[58]  A. Lozano,et al.  Expression of the growth-associated protein GAP-43 in adult rat retinal ganglion cells following axon injury , 1991, Neuron.

[59]  S. Enna.  The GABA receptors , 1997 .

[60]  A. A. Skavenski,et al.  Recovery of visual responses in foveal V1 neurons following bilateral foveal lesions in adult monkey , 2004, Experimental Brain Research.

[61]  S. Finklestein,et al.  Anatomical distribution of the growth-associated protein GAP-43/B-50 in the adult rat brain , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[62]  G. Dunkelberger,et al.  Chronic glaucoma selectively damages large optic nerve fibers. , 1987, Investigative ophthalmology & visual science.

[63]  G. Orban,et al.  Alterations in GAP‐43 and Synapsin Immunoreactivity Provide Evidence for Synaptic Reorganization in Adult Cat Dorsal Lateral Geniculate Nucleus following Retinal Lesions , 1994, The European journal of neuroscience.