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Experience-dependent changes in NMDAR1 expression in the visual cortex of an animal model for amblyopia

Published online by Cambridge University Press:  01 July 2004

KATHRYN M. MURPHY ,
KEVIN R. DUFFY  and
DAVID G. JONES
KATHRYN M. MURPHY
Affiliation:
Department of Psychology, McMaster University, Hamilton ON, Canada Medical Physics and Applied Radiation Sciences Unit, McMaster University, Hamilton ON, Canada
KEVIN R. DUFFY
Affiliation:
Department of Psychology, McMaster University, Hamilton ON, Canada Department of Psychology, Dalhousie University, Halifax NS, Canada
DAVID G. JONES
Affiliation:
Department of Psychology, McMaster University, Hamilton ON, Canada Department of Electrical and Computer Engineering, McMaster University, Hamilton ON, Canada
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Abstract

When normal binocular visual experience is disrupted during postnatal development, it affects the maturation of cortical circuits and often results in the development of poor visual acuity known as amblyopia. Two main factors contribute to the development of amblyopia: visual deprivation and reduced binocular competition. We investigated the affect of these two amblyogenic factors on the expression of the NMDAR1 subunit in the visual cortex because activation of the NMDA receptor is a key mechanism of developmental neural plasticity. We found that disruption of binocular correlations by monocular deprivation promoted a topographic loss of NMDAR1 expression within the cortical representations of the central visual field and the vertical and horizontal meridians. In contrast, binocular deprivation, which primarily affects visual deprivation, promoted an increase in NMDAR1 expression throughout the visual cortex. These different changes in NMDAR1 expression can be described as topographic and homeostatic plasticity of NMDA expression, respectively. In addition, the changes in NMDA expression in the visual cortex provide a greater understanding of the neural mechanisms that underlie the development of amblyopia and the potential for visual recovery.

Keywords

Visual deprivationMonocular deprivationBinocular deprivationAmblyopiaNMDAExperience-dependent plasticity
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 4 , July 2004 , pp. 653 - 670
Copyright
2004 Cambridge University Press

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References

REFERENCES

Adams, D.L. & Horton, J.C. (2003). The representation of retinal blood vessels in primate striate cortex. Journal of Neuroscience 23, 5984–5997.Google Scholar
Antonini, A. & Stryker, M.P. (1993). Rapid remodeling of axonal arbors in the visual cortex. Science 260, 1819–1821.Google Scholar
Aoki, C., Fujisawa, S., Mahadomrongkul, V., Shah, P.J., Nader, K., & Erisir, A. (2003). NMDA receptor blockade in intact adult cortex increases trafficking of NR2A subunits into spines, postsynaptic densities, and axon terminals. Brain Research 963, 139–149.Google Scholar
Bear, M.F. (1995). Mechanism for a sliding synaptic modification threshold. Neuron 15, 1–4.Google Scholar
Bear, M.F., Kleinschmidt, A., Gu, Q., & Singer, W. (1990). Disruption of experience-dependent synaptic modifications in striate cortex by infusion of an NMDA-receptor antagonist. Journal of Neuroscience 10, 909–925.Google Scholar
Beaver, C.J., Ji, Q., & Daw, N.W. (2001). Layer differences in the effect of monocular vision in light- and dark-reared kittens. Visual Neuroscience 18, 811–820.Google Scholar
Birch, E.E., Stager, D., Leffler, J., & Weakley, D. (1998). Early treatment of congenital unilateral cataract minimizes unequal competition. Investigative ophthalmology and Visual Science 39, 1560–1566.Google Scholar
Bode-Greuel, K.M. & Singer, W. (1989). The development of N-methyl-D-aspartate receptors in cat visual cortex. Developmental Brain Research 46, 197–204.Google Scholar
Borbely, A.A., Achermann, P., Trachsel, L., & Tobler, I. (1989). Sleep initiation and initial sleep intensity: Interactions of homeostatic and circadian mechanisms. Journal of Biological Rhythms 4, 149–160.Google Scholar
Burrone, J., O'Byrne, M., & Murthy, V.N. (2002). Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons. Nature 420, 414–418.Google Scholar
Carroll, R.C. & Zukin, R.S. (2002). NMDA-receptor trafficking and targeting: Implications for synaptic transmission and plasticity. Trends in Neuroscience 25, 571–577.Google Scholar
Catalano, S.M., Chang, C.K., & Shatz, C.J. (1997). Activity-dependent regulation of NMDAR1 immunoreactivity in the developing visual cortex. Journal of Neuroscience 17, 8376–8390.Google Scholar
Chen, L., Cooper, N.G., & Mower, G.D. (2000). Developmental changes in the expression of NMDA receptor subunits (NR1, NR2A, NR2B) in the cat visual cortex and the effects of dark rearing. Molecular Brain Research 78, 196–200.Google Scholar
Constantine-Paton, M., Cline, H.T., & Debski, E. (1990). Patterned activity synaptic convergence, and the NMDA receptor in developing visual pathways. Annual Review of Neuroscience 13, 129–154.Google Scholar
Crouch, E.R., Crouch, E.R., Jr., & Pressman, S.H. (2002). Prospective analysis of pediatric pseudophakia: Myopic shift and postoperative outcomes. Journal of AAPOS 6, 277–282.Google Scholar
Daw, N.W. (1994). Mechanisms of plasticity in the visual cortex. Investigative Ophthalmology and Visual Science 35, 4168–4179.Google Scholar
Daw, N.W., Fox, K., Sato, H., & Czepita, D. (1992). Critical period for monocular deprivation in the cat visual cortex. Journal of Neurophysiology 67, 197–202.Google Scholar
DeYoe, E.A., Trusk, T.C., & Wong-Riley, M.T. (1995). Activity correlates of cytochrome oxidase-defined compartments in granular and supragranular layers of primary visual cortex of the macaque monkey. Visual Neuroscience 12, 629–639.Google Scholar
Duffy, K.R., Jones, D.G., & Murphy, K.M. (2001). Experience-dependent visuotopic and homeostatic plasticity of NMDA expression in the developing visual cortex. Society for Neuroscience 619, 5.Google Scholar
Duffy, K.R., Murphy, K.M., & Jones, D.J. (1998). Analysis of postnatal growth of visual cortex. Visual Neuroscience 15, 831–839.Google Scholar
Fava, M.A., Duffy, K.R., & Murphy, K.M. (1999). Experience-dependent development of NMDAR1 subunit expression in the lateral geniculate nucleus. Visual Neuroscience 16, 781–789.Google Scholar
Fonta, C., Chappert, C., & Imbert, M. (2000). Effect of monocular deprivation on NMDAR1 immunostaining in ocular dominance columns of the marmoset Callithrix jacchus. Visual Neuroscience 3, 345–352.Google Scholar
Fox, K. & Daw, N.W. (1993). Do NMDA receptors have a critical function in visual cortical plasticity? Trends in Neurosciences 16, 116–122.Google Scholar
Fujisawa, S. & Aoki, C. (2003). In vivo blockade of N-methyl-D-aspartate receptors induces rapid trafficking of NR2B subunits away from synapses and out of spines and terminals in adult cortex. Neuroscience 121, 51–63.Google Scholar
Gordon, B., Daw, N., & Parkinson, D. (1991). The effect of age on binding of MK-801 in the cat visual cortex. Developmental Brain Research 62, 61–67.Google Scholar
Gordon, B., Kinch, G., Kato, N., Keele, C., Lissman, T., & Fu, L.N. (1997). Development of MK-801, kainate, AMPA, and muscimol binding sites and the effect of dark rearing in rat visual cortex. Journal of Comparative Neurology 383, 73–81.Google Scholar
Gordon, B., Pardo, D., & Conant K. (1996). Laminar distribution of MK-801, kainate, AMPA, and muscimol sites in cat visual cortex: A developmental study. Journal of Comparative Neurology 365, 466–478.Google Scholar
Helmholtz, H. von. (1925). Helmholtz's Treatise on Physiological Optics. Vol. 3, edited by JPC Southhall, Thoemmes Press.
Hevner, R.F. & Wong-Riley, M.T. (1990). Regulation of cytochrome oxidase protein levels by functional activity in the macaque monkey visual system. Journal of Neuroscience 10, 1331–1340.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, 199–253.Google Scholar
Horton, J.C. & Hocking, D.R. (1997). Timing of the critical period for plasticity of ocular dominance columns in macaque striate cortex. Journal of Neuroscience 17, 3684–3709.Google Scholar
Horton, J.C. & Stryker, M.P. (1993). Amblyopia induced by anisometropia without shrinkage of ocular dominance columns in human striate cortex. Proceedings of the National Academy of Sciences of the U.S.A. 90, 5494–5498.Google Scholar
Katz, L.C. & Shatz, C.J. (1996). Synaptic activity and the construction of cortical circuits. Science 274, 1133–1138.Google Scholar
Kiorpes, L., Kiper, D.C., O'Keefe, L.P., Cavanaugh, J.R., & Movshon, J.A. (1998). Neural correlates of amblyopia in the visual cortex of macaque monkeys with experimental strabismus and anisometropia. Journal of Neuroscience 18, 6411–6424.Google Scholar
Kirkwood, A., Hey-Kyoung, L., & Bear, M.F. (1995). Co-regulation of long-term potentiation and experience-dependent synaptic plasticity in visual cortex by age and experience. Nature 375, 328–331.Google Scholar
Kleinschmidt, A., Bear, M.F., & Singer, W. (1987). Blockade of “NMDA” receptors disrupts experience-dependent plasticity of kitten striate cortex. Science 238, 355–358.Google Scholar
Krug, K., Akerman, C.J., & Thompson, I.D. (2001). Responses of neurons in neonatal cortex and thalamus to patterned visual stimulation through the naturally closed lids. Journal of Neurophysiology 85, 1436–1443.Google Scholar
Liu, Q. & Wong-Riley, M.T. (2002). Postnatal expression of neurotransmitters, receptors, and cytochrome oxidase in the rat pre-Botzinger complex. Journal of Applied Physiology 92, 923–934.Google Scholar
Luskin, M.B. & Shatz, C.J. (1985). Neurogenesis of the cat's primary visual cortex. Journal of Comparative Neurology 242, 611–631.Google Scholar
Maurer, D. & Lewis, T.L. (1993). Early visual development: Normal and abnormal. In Committee on Vision. Commission on Behavioural and Social Sciences and Education. National Research Council, ed. Simons, K., pp. 454–484. New York: Oxford University Press.
Maurer, D., Lewis, T.L., Brent, H.P., & Levin, A.V. (1999). Rapid improvement in the acuity of infants after visual input. Science 286, 108–110.Google Scholar
Murphy, K.M. & Mitchell, D.E. (1987). Reduced visual acuity in both eyes of monocularly deprived kittens following a short or long period of reverse occlusion. Journal of Neuroscience 7, 1526–1536.Google Scholar
Murphy, K.M., Jones, D.G., & Van Sluyters, R.C. (1995). Cytochrome-oxidase blobs in cat primary visual cortex. Journal of Neuroscience 15, 4196–4208.Google Scholar
Murphy, K.M., Trepel, C., & Pegado, V.D. (1996). Non-uniform distribution of the NMDAR1 receptor subunit in area 17 at the peak of the critical period. Molecular Vision [Online], 2, 9.Google Scholar
Murphy, K.M., Jones, D.G., Fenstemaker, S.B., Pegado, V.D., Kiorpes, L., & Movshon, J.A. (1998). Spacing of cytochrome oxidase blobs in visual cortex of normal and strabismic monkeys. Cerebral Cortex 8, 237–244.Google Scholar
Murphy, K.M., Duffy, K.R., Jones, D.G., & Mitchell, D.E. (2001). Development of cytochrome-oxidase blobs in the visual cortex of normal and visually deprived cats. Cerebral Cortex 11, 122–135.Google Scholar
Ohzawa, I. & Freeman, R.D. (1988). Binocularly deprived cats: Binocular tests of cortical cells show regular patterns of interaction. Journal of Neuroscience 8, 2507–2516.Google Scholar
Olson, C.R. & Freeman, R.D. (1980). Profile of the sensitive period for monocular deprivation in kittens. Experimental Brain Research 39, 17–21.Google Scholar
Pardhan, S. & Whitaker, A. (2000). Binocular summation in the fovea and peripheral field of anisometropic amblyopes. Current Eye Research 20, 35–44.Google Scholar
Quinlan, E.M., Olstein, D.H., & Bear, M.F. (1999a). Bidirectional, experience-dependent regulation of N-methyl-D-aspartate receptor subunit composition in the rat visual cortex during postnatal development. Proceedings of the National Academy of Sciences of the U.S.A. 96, 12867–12880.Google Scholar
Quinlan, E.M., Philpot, B.D., Huganir, R.L., & Bear, M.F. (1999b). Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo. Nature Neuroscience 2, 352–357.Google Scholar
Rao, A. & Craig, A.M. (1997). Activity regulates the synaptic localization of the NMDA receptor in hippocampal neurons. Neuron 19, 801–812.Google Scholar
Reynolds, I.J. & Bear, M.F. (1991). Effects of age and visual experience on [3H] MK801 binding to NMDA receptors in the kitten visual cortex. Experimental Brain Research 85, 611–615.Google Scholar
Rittenhouse, C.D., Shouval, H.Z., Pasadiso, M.A., & Bear, M.F. (1999). Monocular deprivation induces homosynaptic long-term depression in visual cortex. Nature 397, 347–350.Google Scholar
Roberts, E.B., Meredith, M.A., & Ramoa, A.S. (1998). Suppression of NMDA receptor function using antisense DNA blocks ocular dominance plasticity while preserving visual responses. Journal of Neurophysiology 80, 1021–1032.Google Scholar
Shatz, C.J. & Stryker, M.P. (1978). Ocular dominance in layer IV of the cat's visual cortex and the effects of monocular deprivation. Journal of Physiology 281, 267–283.Google Scholar
Singer, W. & Artola, A. (1991). The role of NMDA receptors in use-dependent synaptic plasticity of the visual cortex. In Excitatory Amino Acids Synaptic Function, ed. Wheal, H.V. & Thomson, A.M., pp. 333–353. London: Academic Press.
Spear, P.D., Tong, L., & Langsetmo, A. (1978). Striate cortex neurons of binocularly deprived kittens respond to visual stimuli through the closed eyelids. Brain Research 155, 141–146.Google Scholar
Trachtenberg, J.T., Trepel, C., & Stryker, M.P. (2000). Rapid extragranular plasticity in the absence of thalamocortical plasticity in the developing primary visual cortex. Science 287, 2029–2032.Google Scholar
Trepel, C., Duffy, K.R., Pegado, V.D., & Murphy, K.M. (1998). Patchy distribution of NMDAR1 subunit immunoreactivty in developing visual cortex. Journal of Neuroscience 18, 3404–3415.Google Scholar
Trusk, T.C., Kaboord, W.S., & Wong-Riley, M.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, 185–204.Google Scholar
Turrigiano, G.G. (1999). Homeostatic plasticity in neuronal networks: The more things change, the more they stay the same. Trends in Neurosciences 22, 221–227.Google Scholar
Turrigiano, G.G. & Nelson, S.B. (2000). Hebb and homeostasis in neuronal plasticity. Current Opinion in Neurobiology 10, 358–364.Google Scholar
Turrigiano, G.G. & Nelson, S.B. (2004). Homeostatic plasticity in the developing nervous system. Nature Reviews Neuroscience 5, 97–107.Google Scholar
Tusa, R.J., Palmer, L.A., & Rosenquist, A.C. (1978). The retinotopic organization of area 17 (striate cortex) in the cat. Journal of Comparative Neurology 177, 213–236.Google Scholar
Tytla, M.E., Lewis, T.L., Maurer, D., & Brent, H.P. (1993). Stereopsis after congenital cataract. Investigative Ophthalmology and Visual Science 34, 1767–1773.Google Scholar
Tytla, M.E., Maurer, D., Lewis, T.L., & Brent, H.P. (1988). Contrast sensitivity in children treated for congenital cataract. Clinical Vision Sciences 2, 251–264.Google Scholar
Wiesel, T.N. & Hubel, D.H. (1965). Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. Journal of Neurophysiology 28, 1029–1040.Google Scholar
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
Wong-Riley, M.T. (1989). Cytochrome oxidase: An endogenous metabolic marker for neuronal activity. Trends in Neuroscience 12, 94–101.Google Scholar
Yin, Z.Q., Crewther, S.G., Yang, M., & Crewther, D.P. (1996). Distribution and localization of NMDA receptor subunit 1 in the visual cortex of strabismic and anisometropic amblyopic cats. Neuroreport. 7, 2997–3003.Google Scholar
Yin, Z.Q., Deng, Z.M., Crewther, S.G., & Crewther, D.P. (2001). Altered expression of alternatively spliced isoforms of the mRNA NMDAR1 receptor in the visual cortex of strabismic cats. Molecular Vision 7, 271–276.Google Scholar
Zhang, C. & Wong-Riley, M. (1999). Expression and regulation of NMDA receptor subunit R1 and neuronal nitric oxide synthase in cortical neuronal cultures: Correlation with cytochrome oxidase. Journal of Neurocytology 28, 525–539.Google Scholar
Zubcov, A.A., Stahl, E., Rossillion, B., Nutzenberger, A., Kohnen, T., Ohrloff, C., & Stark, N. (1999). Stereopsis after primary in-the-bag posterior chamber implantation in children. Journal of AAPOS 3, 227–233.Google Scholar