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Light deprivation suppresses the light response of inner retina in both young and adult mouse

Published online by Cambridge University Press:  03 May 2004

SETAREH VISTAMEHR  and
NING TIAN
SETAREH VISTAMEHR
Affiliation:
Department of Ophthalmology and Visual Science, Yale University School of Medicine, New Haven
NING TIAN
Affiliation:
Department of Ophthalmology and Visual Science, Yale University School of Medicine, New Haven Department of Neurobiology, Yale University School of Medicine, New Haven
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Abstract

The retinal synaptic network continues its development after birth in mammals. Recent studies show that postnatal development of retinal circuitry depends on visual stimulation. We sought to determine whether there is a time period during which the retina shows evidence of increased plasticity. We examined the effects of light deprivation on the retinal light response of mouse retina using electroretinogram (ERG) measurements. Our results showed that dark rearing mice from birth to postnatal day (P) 30, 60, and 90 suppressed the amplitudes of oscillatory potentials (OPs) and the magnitudes of suppression were age independent. In addition, dark-rearing-produced suppression of OP amplitudes can be completely reversed in both young and adult mice by returning them to cyclic light/dark conditions for 1 to 2 weeks. However, the recovery time course was age dependent with younger animals needing a longer time to achieve a full recovery. Furthermore, dark rearing of P60 mice raised under cyclic light/dark conditions for 30 days resulted in a similar magnitude of suppression of OP amplitudes as in age-matched mice dark reared from birth. These findings demonstrate that both the normal developmental changes and the maintenance of mature inner retinal light response in adult animals require visual stimulation. These results indicate a degree of activity-dependent plasticity in mouse retina that has not been previously described.

Keywords

Light deprivationSynaptic plasticityCritical periodRetinal light responsesERG
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 1 , January 2004 , pp. 23 - 37
Copyright
2004 Cambridge University Press

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References

REFERENCES

Aleman, T.S., LaVail, M.M., Montemayor, R., Ying, G., Maguire, M.M., Laties, A.M., Jacobson, S.G., & Cideciyan, A.V. (2001). Augmented rod bipolar cell function in partial receptor loss: an ERG study in P23H rhodopsin transgenic and aging normal rats. Vision Research 41, 2779–2797.CrossRefGoogle Scholar
Babkoff, H. (1975). The effect of light deprivation on the B-wave input-output function. Annals of Ophthalmology 7, 1335–1338.Google Scholar
Babkoff, H. (1977). Light-deprivation and light-adaptation: A preliminary study. Annals of Ophthalmology 9, 1535–1539.Google Scholar
Baxter, B.I. & Riesen, A.H. (1961). Electroretinogram of the visually deprived cat. Science 134, 1626–1627.CrossRefGoogle Scholar
Berardi, N., Pizzorusso, T., & Maffei, L. (2000). Critical periods during sensory development. Current Opinion in Neurobiology 10, 138–145.CrossRefGoogle Scholar
Birch, D.G. & Anderson, J.L. (1992). Standardized full-field electroretinography. Normal values and their variation with age. Archives of Ophthalmology 110, 1571–1576.CrossRefGoogle Scholar
Birch, D.G. & Jacobs, G.H. (1979). The effects of prolonged dark exposure on visual thresholds in young and adult rats. Investigative Ophthalmology and Visual Science 18, 752–756.Google Scholar
Bisti, S., Gargini, C., & Chalupa, L.M. (1998). Blockade of glutamate-mediated activity in the developing retina perturbs the functional segregation of ON and OFF pathways. Journal of Neuroscience 18, 5019–5025.Google Scholar
Bodnarenko, S.R. & Chalupa, L.M. (1993). Stratification of ON and OFF ganglion cell dendrites depends on glutamate-mediated afferent activity in the developing retina. Nature 364, 144–146.CrossRefGoogle Scholar
Bodnarenko, S.R., Jeyarasasingam, G., & Chalupa, L.M. (1995). Development and regulation of dendritic stratification in retinal ganglion cells by glutamate-mediated afferent activity. Journal of Neuroscience 15, 7037–7045.Google Scholar
Braekevelt, C.R. & Hollenberg, M.J. (1970). The development of the retina of the albino rat. American Journal of Anatomy 127, 281–301.CrossRefGoogle Scholar
Breton, M.E., Quinn, G.E., & Schueller, A.W. (1995). Development of electroretinogram and rod phototransduction response in human infants. Investigative Ophthalmology and Visual Science 36, 1588–1602.Google Scholar
Bui, B.V. & Vingrys, A.J. (1999). Development of receptoral responses in pigmented and albino guinea-pigs (Cavia porcellus). Documenta Ophthalmologica 99, 151–170.CrossRefGoogle Scholar
Chen, S. & Diamond, J.S. (2002). Synaptically released glutamate activates extrasynaptic NMDA receptors on cells in the ganglion cell layer of rat retina. Journal of Neuroscience 22, 2165–2173.Google Scholar
Cohen, E.D. (2000). Light-evoked excitatory synaptic currents of X-type retinal ganglion cells. Journal of Neurophysiology 83, 3217–3229.CrossRefGoogle Scholar
Cynader, M. (1983). Prolonged sensitivity to monocular deprivation in dark-reared cats: Effects of age and visual exposure. Brain Research 284, 155–164.CrossRefGoogle Scholar
Cynader, M. & Mitchell, D.E. (1980). Prolonged sensitivity to monocular deprivation in dark-reared cats. Journal of Neurophysiology 43, 1026–1040.CrossRefGoogle Scholar
Daw, N.W. (1995). Visual Development. New York, New York: Plenum Press.CrossRef
Diamond, J.S. & Copenhagen, D.R. (1995). The relationship between light-evoked synaptic excitation and spiking behaviour of salamander retinal ganglion cells. Journal of Physiology 487(Pt. 3), 711–725.Google Scholar
DiLoreto, D., Jr., Ison, J.R., Bowen, G.P., Cox, C., & del Cerro, M. (1995). A functional analysis of the age-related degeneration in the Fischer 344 rat. Current Eye Research 14, 303–310.CrossRefGoogle Scholar
Dowling, J.E. & Sidman, R.L. (1962). Inherited retinal dystrophy in the rat. Journal of Cell Biology 14, 459–474.CrossRefGoogle Scholar
el-Azazi, M. & Wachtmeister, L. (1990). The postnatal development of the oscillatory potentials of the electroretinogram. I. Basic characteristics. Acta Ophthalmology (Copenhagen) 68, 401–409.Google Scholar
Fagiolini, M., Pizzorusso, T., Berardi, N., Domenici, L., & Maffei, L. (1994). Functional postnatal development of the rat primary visual cortex and the role of visual experience: Dark rearing and monocular deprivation. Vision Research 34, 709–720.CrossRefGoogle Scholar
Fisher, L.J. (1979). Development of retinal synaptic arrays in the inner plexiform layer of dark-reared mice. Journal of Embryology and Experimental Morphology 54, 219–227.Google Scholar
Fletcher, E.L., Hack, I., Brandstatter, J.H., & Wässle, H. (2000). Synaptic localization of NMDA receptor subunits in the rat retina. Journal of Comparative Neurology 420, 98–112.3.0.CO;2-U>CrossRefGoogle Scholar
Flores-Guevara, R., Renault, F., Ostre, C., & Richard, P. (1996). Maturation of the electroretinogram in children: Stability of the amplitude ratio a/b. Electroencephalography and Clinical Neurophysiology 100, 422–427.Google Scholar
Fox, K., Daw, N., Sato, H., & Czepita, D. (1991). Dark-rearing delays the loss of NMDA-receptor function in kitten visual cortex. Nature 350, 342–344.CrossRefGoogle Scholar
Fujikado, T., Hosohata, J., & Omoto, T. (1996). ERG of form deprivation myopia and drug induced ametropia in chicks. Current Eye Research 15, 79–86.CrossRefGoogle Scholar
Gilbert, C.D. (1998). Adult cortical dynamics. Physiological Reviews 78, 467–485.CrossRefGoogle Scholar
Gordon, J.A. & Stryker, M.P. (1996). Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse. Journal of Neuroscience 16, 3274–3286.Google Scholar
Gorfinkel, J. & Lachapelle, P. (1990). Maturation of the photopic b-wave and oscillatory potentials of the electroretinogram in the neonatal rabbit. Canadian Journal of Ophthalmology 25, 138–144.Google Scholar
Gorfinkel, J., Lachapelle, P., & Molotchnikoff, S. (1988). Maturation of the electroretinogram of the neonatal rabbit. Document Ophthalmology 69, 237–245.CrossRefGoogle Scholar
Goto, Y., Peachey, N.S., Ripps, H., & Naash, M.I. (1995). Functional abnormalities in transgenic mice expressing a mutant rhodopsin gene. Investigative Ophthalmology and Visual Science 36, 62–71.Google Scholar
Guire, E.S., Lickey, M.E., & Gordon, B. (1999). Critical period for the monocular deprivation effect in rats: Assessment with sweep visually evoked potentials. Journal of Neurophysiology 81, 121–128.CrossRefGoogle Scholar
Hahm, J.O., Langdon, R.B., & Sur, M. (1991). Disruption of retinogeniculate afferent segregation by antagonists to NMDA receptors. Nature 351, 526.Google Scholar
Hamasaki, D.I. & Maguire, G.W. (1985). Physiological development of the kitten's retina: An ERG study. Vision Research 25, 1537–1543.CrossRefGoogle Scholar
Harwerth, R.S., Smith, E.L., III, Duncan, G.C., Crawford, M.L., & von Noorden, G.K. (1986). Multiple sensitive periods in the development of the primate visual system. Science 232, 235–238.CrossRefGoogle Scholar
Heynen, A.J., Quinlan, E.M., Bae, D.C., & Bear, M.F. (2000). Bidirectional, activity-dependent regulation of glutamate receptors in the adult hippocampus in vivo. Neuron 28, 527–536.CrossRefGoogle Scholar
Horiguchi, M., Suzuki, S., Kondo, M., Tanikawa, A., & Miyake, Y. (1998). Effect of glutamate analogues and inhibitory neurotransmitters on the electroretinograms elicited by random sequence stimuli in rabbits. Investigative Ophthalmology and Visual Science 39, 2171–2176.Google Scholar
Issa, N.P., Trachtenberg, J.T., Chapman, B., Zahs, K.R., & Stryker, M.P. (1999). The critical period for ocular dominance plasticity in the Ferret's visual cortex. Journal of Neuroscience 19, 6965–6978.Google Scholar
Kapousta-Bruneau, N.V. (2000). Opposite effects of GABA(A) and GABA(C) receptor antagonists on the b-wave of ERG recorded from the isolated rat retina. Vision Research 40, 1653–1665.CrossRefGoogle Scholar
Katz, M.L. & Robison, W.G., Jr. (1986). Evidence of cell loss from the rat retina during senescence. Experimental Eye Research 42, 293–304.CrossRefGoogle Scholar
Knott, G.W., Quairiaux, C., Genoud, C., & Welker, E. (2002). Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice. Neuron 34, 265–273.CrossRefGoogle Scholar
Kolb, H. & Nelson, R. (1981). Amacrine cells of the cat retina. Vision Research 21, 1625–1633.CrossRefGoogle Scholar
Korol, S., Leuenberger, P.M., Englert, U., & Babel, J. (1975). In vivo effects of glycine on retinal ultrastructure and averaged electroretinogram. Brain Research 97, 235–251.CrossRefGoogle Scholar
Lai, Y.L., Jacoby, R.O., & Jonas, A.M. (1978). Age-related and light-associated retinal changes in Fischer rats. Investigative Ophthalmology and Visual Science 17, 634–638.Google Scholar
Li, Y., Erzurumlu, R.S., Chen, C., Jhaveri, S., & Tonegawa, S. (1994). Whisker-related neuronal patterns fail to develop in the trigeminal brainstem nuclei of NMDAR1 knockout mice. Cell 76, 427–437.CrossRefGoogle Scholar
Li, Q., Timmers, A.M., Hunter, K., Gonzalez-Pola, C., Lewin, A.S., Reitze, D.H., & Hauswirth, W.W. (2001). Noninvasive imaging by optical coherence tomography to monitor retinal degeneration in the mouse. Investigative Ophthalmology and Visual Science 42, 2981–2989.Google Scholar
Masland, R.H. (1977). Maturation of function in the developing rabbit retina. Journal of Comparative Neurology 175, 275–286.CrossRefGoogle Scholar
Massey, S.C. & Miller, R.F. (1990). N-methyl-D-aspartate receptors of ganglion cells in rabbit retina. Journal of Neurophysiology 63, 16–30.CrossRefGoogle Scholar
Masu, M., Iwakabe, H., Tagawa, Y., Miyoshi, T., Yamashita, M., Fukuda, Y., Sasaki, H., Hiroi, K., Nakamura, Y., Shigemoto, R., Takada, M., Nakamura, K., Nakao, K., Katsuki, M., & Nakanishi S. (1995). Specific deficit of the ON response in visual transmission by targeted disruption of the mGluR6 gene. Cell 80, 757–765.CrossRefGoogle Scholar
Matthews, G.P., Crane, W.G., & Sandberg, M.A. (1989). Effects of 2-amino-4-phosphonobutyric acid (APB) and glycine on the oscillatory potentials of the rat electroretinogram. Experimental Eye Research 49, 777–787.CrossRefGoogle Scholar
McCall, M.A., Lukasiewicz, P.D., Gregg, R.G., & Peachey, N.S. (2002). Elimination of the rho1 subunit abolishes GABA(C) receptor expression and alters visual processing in the mouse retina. Journal of Neuroscience 22, 4163–4174.Google Scholar
Mittman, S., Taylor, W.R., & Copenhagen, D.R. (1990). Concomitant activation of two types of glutamate receptor mediate sexcitation of salamander retinal ganglion cells. Journal of Physiology (London) 428, 175–197.CrossRefGoogle Scholar
Mower, G.D. (1991). The effect of dark rearing on the time course of the critical period in cat visual cortex. Developmental Brain Research 58, 151–158.CrossRefGoogle Scholar
Obin, M., Halbleib, M., Lipman, R., Carroll, K., Taylor, A., & Bronson, R. (2000). Calorie restriction increases light-dependent photoreceptor cell loss in the neural retina of fischer 344 rats. Neurobiology of Aging 21, 639–645.CrossRefGoogle Scholar
Philpot, B.D., Sekhar, A.K., Shouval, H.Z., & Bear, M.F. (2001). Visual experience and deprivation bidirectionally modify the composition and function of NMDA receptors in visual cortex. Neuron 29, 157–169.CrossRefGoogle Scholar
Pizzorusso, T., Medini, P., Berardi, N., Chierzi, S., Fawcett, J.W., & Maffei, L. (2002). Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298, 1248–1251.CrossRefGoogle Scholar
Pourcho, R.G., Qin, P., & Goebel, D.J. (2001). Cellular and subcellular distribution of NMDA receptor subunit NR2B in the retina. Journal of Comparative Neurology 433, 75–85.CrossRefGoogle Scholar
Quinlan, E.M., Olstein, D.H., & Bear, M.F. (1999). 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, 12876–12880.CrossRefGoogle Scholar
Rabacchi, S., Bailly, Y., Delhaye-Bouchaud, N., & Mariani, J. (1992). Involvement of the N-methyl D-aspartate (NMDA) receptor in synapse elimination during cerebellar development. Science 256, 1823–1825.CrossRefGoogle Scholar
Reuter, J.H. (1976). The development of the electroretinogram in normal and light-deprived rabbits. Pflugers Archive 363, 7–13.CrossRefGoogle Scholar
Rodriguez-Saez, E., Otero-Costas, J., Moreno-Montanes, J., & Relova, J.L. (1993). Electroretinographic changes during childhood and adolescence. European Journal of Ophthalmology 3, 6–12.CrossRefGoogle Scholar
Schlaggar, B.L., Fox, K., & O'Leary, D.D. (1993). Postsynaptic control of plasticity in developing somatosensory cortex. Nature 364, 623–626.CrossRefGoogle Scholar
Schnupp, J.W., King, A.J., Smith, A.L., & Thompson, I.D. (1995). NMDA-receptor antagonists disrupt the formation of the auditory space map in the mammalian superior colliculus. Journal of Neuroscience 15, 1516–1531.Google Scholar
Sernagor, E. & Grzywacz, N.M. (1996). Influence of spontaneous activity and visual experience on developing retinal receptive fields. Current Biology 6, 1503–1508.CrossRefGoogle Scholar
Severns, M.L., Johnson, M.A., & Bresnick, G.H. (1994). Methodologic dependence of electroretinogram oscillatory potential amplitudes. Documenta Ophthalmologica 86, 23–31.CrossRefGoogle Scholar
Simon, D.K., Prusky, G.T., O'Leary, D.D., & Constantine-Paton, M. (1992). N-methyl-D-aspartate receptor antagonists disrupt the formation of a mammalian neural map. Proceedings of the National Academy Sciences of the U.S.A. 89, 10593–10597.CrossRefGoogle Scholar
Sosula, L. & Glow, P.H. (1971). Increase in number of synapses in the inner plexiform layer of light deprived rat retinae: Quantitative electron microscopy. Journal of Comparative Neurology 141, 427–451.CrossRefGoogle Scholar
Stockton, R.A. & Slaughter, M.M. (1989). B-wave of the electroretinogram. A reflection of ON bipolar cell activity. Journal of General Physiology 93, 101–122.Google Scholar
Tian, N. & Copenhagen, D.R. (2001). Visual deprivation alters development of synaptic function in inner retina after eye opening. Neuron 32, 439–449.CrossRefGoogle Scholar
Tian, N. & Copenhagen, D.R. (2003). Visual stimulation is required for refinement of ON and OFF pathways in postnatal retina. Neuron 39, 85–96.CrossRefGoogle Scholar
Tian, N. & Slaughter, M.M. (1995). Correlation of dynamic responses in the ON bipolar neuron and the b-wave of the electroretinogram. Vision Research 35, 1359–1364.CrossRefGoogle Scholar
Tootle, J.S. (1993). Early postnatal development of visual function in ganglion cells of the cat retina. Journal of Neurophysiology 69, 1645–1660.CrossRefGoogle Scholar
Tucker, G.S., Hamasaki, D.I., Labbie, A., & Bradford, N. (1982). Physiologic and anatomic development of the photoreceptors of normally-reared and dark-reared rabbits. Experimental Brain Research 48, 263–271.Google Scholar
Wachtmeister, L. (1980). Further studies of the chemical sensitivity of the oscillatory potentials of the electroretinogram (ERG) I. GABA- and glycine antagonists. Acta Ophthalmologica (Copenhagen) 58, 712–725.Google Scholar
Wachtmeister, L. (1998). Oscillatory potentials in the retina: What do they reveal. Progress in Retina and Eye Research 17, 485–521.CrossRefGoogle Scholar
Wachtmeister, L. & Dowling, J.E. (1978). The oscillatory potentials of the mudpuppy retina. Investigative Ophthalmology and Visual Science 17, 1176–1188.Google Scholar
Wang, G.Y., Liets, L.C., & Chalupa, L.M. (2001). Unique functional properties of on and off pathways in the developing mammalian retina. Journal of Neuroscience 21, 4310–4317.Google Scholar
Weidman, T.A. & Kuwabara, T. (1968). Postnatal development of the rat retina. An electron microscopic study. Archives of Ophthalmology 79, 470–484.CrossRefGoogle Scholar
Weidman, T.A. & Kuwabara, T. (1969). Development of the rat retina. Investigative Ophthalmology 8, 60–69.Google Scholar
Weisse, I. (1995). Changes in the aging rat retina. Ophthalmic Research 27 (Suppl. 1), 154–163.CrossRefGoogle Scholar
Weleber, R.G. (1981). The effect of age on human cone and rod ganzfeld electroretinograms. Investigative Ophthalmology and Visual Science 20, 392–399.Google Scholar
Westall, C.A., Panton, C.M., & Levin, A.V. (1998–99). Time courses for maturation of electroretinogram responses from infancy to adulthood. Documenta Ophthalmologica 96, 355–379.Google Scholar
Wingate, R.J. & Thompson, I.D. (1994). Targeting and activity-related dendritic modification in mammalian retinal ganglion cells. Journal of Neuroscience 14, 6621–6637.Google Scholar
Xue, J. & Cooper, N.G. (2001). The modification of NMDA receptors by visual experience in the rat retina is age dependent. Brain Research, Molecular Brain Research 91, 196–203.CrossRefGoogle Scholar