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Cytoskeleton alteration correlates with gross structural plasticity in the cat lateral geniculate nucleus

Published online by Cambridge University Press:  04 October 2007

MATTHEW R. KUTCHER  and
KEVIN R. DUFFY
MATTHEW R. KUTCHER
Affiliation:
Department of Psychology, Dalhousie University, Life Sciences Centre, Halifax, NS, Canada
KEVIN R. DUFFY
Affiliation:
Department of Psychology, Dalhousie University, Life Sciences Centre, Halifax, NS, Canada
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Abstract

Monocular deprivation during early development causes rearrangement of neural connections within the visual cortex that produces a shift in ocular dominance favoring the non-deprived eye. This alteration is manifested anatomically within deprived layers of the lateral geniculate nucleus (LGN) where neurons have smaller somata and reduced geniculocortical terminal fields compared to non-deprived counterparts. Experiments using monocular deprivation have demonstrated a spatial correlation between cytoskeleton alteration and morphological change within the cat LGN, raising the possibility that subcellular events mediating deprivation-related structural rearrangement include modification to the neuronal cytoskeleton. In the current study we compared the spatial and temporal relationships between cytoskeleton alteration and morphological change in the cat LGN. Cross-sectional soma area and neurofilament labeling were examined in the LGN of kittens monocularly deprived at the peak of the critical period for durations that ranged from 1 day to 7 months. After 4 days of deprivation, neuron somata within deprived layers of the LGN were significantly smaller than those within non-deprived layers. This structural change was accompanied by a spatially coincident reduction in neurofilament immunopositive neurons that was likewise significant after 4 days of deprivation. Both anatomical effects reached close to their maximum by 10 days of deprivation. Results from this study demonstrate that alteration to the neuronal cytoskeleton is both spatially and temporally linked to the gross structural changes induced by monocular deprivation.

Keywords

Monocular DeprivationCytoskeletonNeurofilamentCytostructureLateral Geniculate Nucleus
Type
Research Article
Information
Visual Neuroscience , Volume 24 , Issue 6 , November 2007 , pp. 775 - 785
Copyright
2007 Cambridge University Press

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References

REFERENCES

Antonini, A. & Stryker, M.P. (1993). Rapid remodeling of axonal arbors in the visual cortex. Science 260, 1819–1821.CrossRefGoogle Scholar
Antonini, A. & Stryker, M.P. (1998). Effects of sensory disuse on geniculate afferents to cat visual cortex. Visual Neuroscience 15, 401–409.CrossRefGoogle Scholar
Banik, N.L., Hogan, E.L., Powers, J.M. & Whetstine, L.J. (1982). Degradation of cytoskeletal proteins in experimental spinal cord injury. Neurochemical Research 7, 1465–1475.CrossRefGoogle Scholar
Bickford, M.E., Guido, W. & Godwin, D.W. (1998). Neurofilament proteins in Y-cells of the cat lateral geniculate nucleus: Normal expression and alteration with visual deprivation. Journal of Neuroscience 18, 6549–6557.CrossRefGoogle Scholar
Cabelli, R.J., Hohn, A. & Shatz, C.J. (1995). Inhibition of ocular dominance column formation by infusion of NT-4/5 or BDNF. Science 267, 1662–1666.CrossRefGoogle Scholar
Carden, W.B., Guido, W., Ziburkus, J., Datskovskaia, A., Godwin, D.W. & Bickford, M.E. (2000). A novel means of Y-cell identification in the developing lateral geniculate nucleus of the cat. Neuroscience Letters 295, 5–8.CrossRefGoogle Scholar
del Cerro, S., Arai, A., Kessler, M., Bahr, B.A., Vanderklish, P., Rivera, S. & Lynch, G. (1994). Stimulation of NMDA receptors activates calpain in cultured hippocampal slices. Neuroscience Letters 167, 149–152.CrossRefGoogle Scholar
Duffy, K.R. & Livingstone, M.S. (2005). Loss of neurofilament labeling in the primary visual cortex of monocularly deprived monkeys. Cerebral Cortex 15, 1146–1154.CrossRefGoogle Scholar
Duffy, K.R., Murphy, K.M., Frosch, M.P. & Livingstone, M.S. (2007). Cytochrome oxidase and neurofilament reactivity in monocularly deprived human primary visual cortex. Cerebral Cortex 17, 1283–1291.CrossRefGoogle 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.CrossRefGoogle Scholar
Friedlander, M.J., Martin, K.A.C. & Wassenhove-McCarthy, D. (1991). Effects of monocular visual deprivation on geniculocortical innervation of area 18 in cat. Journal of Neuroscience 11, 3268–3288.CrossRefGoogle Scholar
Friedlander, M.J., Stanford, L.R. & Sherman, S.M. (1982). Effects of monocular deprivation on the structure-function relationship of individual neurons in the cat's lateral geniculate nucleus. Journal of Neuroscience 2, 321–330.CrossRefGoogle Scholar
Greenwood, J.A., Troncoso, J.C., Costello, A.C. & Johnson, G.V. (1993). Phosphorylation modulates calpain-mediated proteolysis and calmodulin binding of the 200-kDa and 160-kDa neurofilament proteins. Journal of Neurochemistry 61, 191–199.CrossRefGoogle Scholar
Guillery, R.W. (1972). Binoocular competition in the control of geniculate cell growth. Journal of Comparative Neurology 144, 177–129.Google Scholar
Guillery, R.W. (1973). The effect of lid suture upon the growth of cells in the dorsal lateral geniculate nucleus of kittens. Journal of Comparative Neurology 148, 417–422.CrossRefGoogle Scholar
Guillery, R.W. & Stelzner, D.J. (1970). The differential effects of unilateral lid closure upon the monocular and binocular segments of the dorsal lateral geniculate nucleus in the cat. Journal of Comparative Neurology 139, 413–421.CrossRefGoogle Scholar
Hamakubo, T., Kannagi, R., Murachi, T. & Matus, A. (1986). Distribution of calpains I and II in rat brain. Journal of Neuroscience 11, 3103–3111.CrossRefGoogle Scholar
Haynes, R.L., Borenstein, N.S., DeSilva, T.M., Folkerth, R.D., Liu, L.G., Volpe, J.J. & Kinney, H.C. (2005). Axonal development in the cerebral white matter of the human fetus and infant. Journal of Comparative Neurology 484, 156–167.CrossRefGoogle Scholar
Hendry, S.H. & Bhandari, M.A. (1992). Neuronal organization and plasticity in adult monkey visual cortex: Immunoreactivity for microtubule-associated protein 2. Visual Neuroscience 9, 445–459.CrossRefGoogle Scholar
Heynen, A.J., Yoon, B.J., Liu, C.H., Chung, H.J., Huganir, R.L. & Bear, M.F. (2003). Molecular mechanism for loss of visual cortical responsiveness following brief monocular deprivation. Nature Neuroscience 6, 854–862.CrossRefGoogle Scholar
Hisanaga, S., Gonda, Y., Inagaki, M., Ikai, A. & Nobutaka, H. (1990). Effects of phosphorylation of the neurofilament L protein on filamentous structures. Cell Regulation 1, 237–248.CrossRefGoogle Scholar
Hisanaga, S., Kusubata, M., Okumura, E. & Kishimoto, T. (1991). Phosphorylation of neurofilament H subunit at the tail domain by CDC2 kinase dissociates the association to microtubules. The Journal of Biological Chemistry 266, 21798–21803.Google Scholar
Hof, P.R. & Morrison, J.H. (1995). Neurofilament protein defines regional patterns of cortical organization in the macaque monkey visual system: A quantitative immunohistochemical analysis. Journal of Comparative Neurology 352, 161–186.CrossRefGoogle Scholar
Hoffman, P.N., Cleveland, D.W., Griffin, J.W., Landes, P.W., Cowan, N.J. & Price, D.L. (1987). Neurofilament gene expression: A major determinant of axonal caliber. Proceedings of the National Academy of Sciences USA 84, 3472–3476.CrossRefGoogle Scholar
Hubel, D.H. & Wiesel, T.N. (1970). The period of susceptibility to the physiological effects of unilateral eye closure in kittens. Journal of Physiology 206, 419–436.CrossRefGoogle Scholar
Hubel, D.H., Wiesel, T.N., LeVay, S. (1977). Plasticity of ocular dominance columns in monkey striate cortex. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 278, 377–409.CrossRefGoogle Scholar
Johnson, G.V., Litersky, J.M. & Jope, R.S. (1991). Degradation of microtubule-associated protein 2 and brain spectrin by calpain: A comparative study. Journal of Neurochemistry 56, 1630–1638.CrossRefGoogle Scholar
Kalil, R. (1978). Development of the dorsal lateral geniculate nucleus in the cat. Journal of Comparative Neurology 182, 265–291.CrossRefGoogle Scholar
Kamakura, K., Ishiura, S., Suzuki, K., Sugita, H. & Toyokura, Y. (1985). Calcium-activated neutral protease in the peripheral nerve, which requires microM oder Ca2+, and its effect on the neurofilament triplet. Journal of Neuroscience Research 13, 391–403.CrossRefGoogle Scholar
Kleinschmidt, A., Bear, M.F. & Singer, W. (1987). Blockage of “NMDA” receptors disrupts experience-dependent plasticity of kitten striate cortex. Science 238, 355–358.CrossRefGoogle Scholar
Lee, V.M., Otvos, Y.L., Carden, M.J., Hollosi, M., Dietzschold, B. & Lazzarini, R.A. (1988). Identification of the major multiphosphorylation site in mammalian neurofilaments. Proceedings of the National Academy of Sciences USA 85, 1998–2002.CrossRefGoogle Scholar
Lin, C.S. & Sherman, S.M. (1978). Effects of early monocular eyelid suture upon development of relay cell classes in the cat's lateral geniculate nucleus. Journal of Comparative Neurology 181, 809–831.CrossRefGoogle Scholar
Mioche, L. & Singer, W. (1989). Chronic recordings from single sites of kitten striate cortex during experience-dependent modification of receptive-field properties. Journal of Neurophysiology 62, 185–197.CrossRefGoogle Scholar
Morris, J.R. & Lasek, R.J. (1982). Stable polymers of the axonal cytoskeleton: The axoplasmic ghost. Journal of Cell Biology 92, 192–198.CrossRefGoogle 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.CrossRefGoogle Scholar
Nakamura, Y., Takeda, M., Angelides, K.J., Tanaka, T., Tada, K. & Nishimura, T. (1990). Effect of phosphorylation on 68Kda neurofilament subunit protein assembly by the cyclic AMP dependent protein kinase in vitro. Biochemical and Biophysical Research Communications 169, 744–750.CrossRefGoogle Scholar
Olson, C.R. & Freeman, R.D. (1980). Profile of the sensitive period for monocular deprivation in kittens. Experimental Brain Research 39, 17–21.CrossRefGoogle Scholar
Pant, H.C. (1988). Dephosphorylation of neurofilament proteins enhances their susceptibility to degradation by calpain. Journal of Biochemistry 256, 665–668.CrossRefGoogle Scholar
Posmantur, R., Kampfl, A., Siman, R., Liu, J., Zaho, X., Clifton, G.L. & Haves, R.L. (1997). A calpain inhibitor attenuates cortical cytoskeleton protein loss after experimental traumatic brain-injury. Neuroscience 77, 875–888.CrossRefGoogle Scholar
Riddle, D.R., Lo, D.C. & Katz, L.C. (1995). NT-4-mediated rescue of lateral geniculate neurons from effects of monocular deprivation. Nature 378, 189–191.CrossRefGoogle Scholar
Sanderson, K.J. (1971). The projection of the visual field to the lateral geniculate and medial interlaminar nuclei in the cat. Journal of Comparative Neurology 143, 101–118.CrossRefGoogle Scholar
Schlaepfer, W.W. & Zimmerman, U.J. (1985). Calcium-activated proteolysis of intermediate filaments. Annals of the New York Academy of Sciences 455, 552–562.CrossRefGoogle Scholar
Schmidt, D. & Spillman, L. (2005). First research on developmental amplyopia due to early deprivation—Hans Berger's experiments in 1900. Perception 34, 765–767.CrossRefGoogle 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.CrossRefGoogle Scholar
Sihag, R.K., Jeng, A.Y. & Nixon, R.A. (1988). Phosphorylation of neurofilament proteins by protein kinase C. FEBS Letters 233, 181–185.CrossRefGoogle Scholar
Spear, P.D., McCall, M.A. & Tumosa, N. (1989). W- and Y-cells in the C layers of the cat's lateral geniculate nucleus: Normal properties and effects of monocular deprivation. Journal of Neurophysiology 61, 58–73.CrossRefGoogle Scholar
Sternberger, L.A. & Sternberger, L.A. (1983). Monoclonal antibodies distinguish phosphorylated and non-phosphorylated forms of neurofilament in situ. Proceedings of the National Academy of Sciences USA 80, 6126–6130.CrossRefGoogle Scholar
Tsuda, M., Tashiro, T. & Komiya, Y. (2000). Selective solublization of high molecular-mass neurofilament subunit during nerve regeneration. Journal of Neurochemistry 74, 860–868.Google Scholar
Wan, Y.K. & Cragg, B. (1976). Cell growth in the lateral geniculate nucleus of kittens following the opening or closing of one eye. Journal of Comparative Neurology 166, 365–371.CrossRefGoogle Scholar
Wiesel, T.N. & Hubel, D.H. (1963a). Singel-cell responses in striate cortex of kittens deprived of vision in one eye. Journal of Neurophysiology 26, 1003–1017.Google Scholar
Wiesel, T.N. & Hubel, D.H. (1963b). Effects of visual deprivation on morphology and physiology of cells in the cats lateral geniculate body. Journal of Neurophysiology 26, 978–993.Google Scholar
Ziburkus, J., Bickford, M.E. & Guido, W. (2000). NMDAR-1 staining in the lateral geniculate nucleus of normal and visually deprived cats. Visual Neuroscience 17, 187–196.CrossRefGoogle Scholar