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Shrinkage of X cells in the lateral geniculate nucleus after monocular deprivation revealed by FoxP2 labeling

  • KEVIN R. DUFFY (a1), KAITLYN D. HOLMAN (a1) and DONALD E. MITCHELL (a1)
Abstract

The parallel processing of visual features by distinct neuron populations is a central characteristic of the mammalian visual system. In the A laminae of the cat dorsal lateral geniculate nucleus (dLGN), parallel processing streams originate from two principal neuron types, called X and Y cells. Disruption of visual experience early in life by monocular deprivation has been shown to alter the structure and function of Y cells, but the extent to which deprivation influences X cells remains less clear. A transcription factor, FoxP2, has recently been shown to selectively label X cells in the ferret dLGN and thus provides an opportunity to examine whether monocular deprivation alters the soma size of X cells. In this study, FoxP2 labeling was examined in the dLGN of normal and monocularly deprived cats. The characteristics of neurons labeled for FoxP2 were consistent with FoxP2 being a marker for X cells in the cat dLGN. Monocular deprivation for either a short (7 days) or long (7 weeks) duration did not alter the density of FoxP2-positive neurons between nondeprived and deprived dLGN layers. However, for each deprived animal examined, measurement of the cross-sectional area of FoxP2-positive neurons (X cells) revealed that within deprived layers, X cells were smaller by approximately 20% after 7 days of deprivation, and by approximately 28% after 7 weeks of deprivation. The observed alteration to the cross-sectional area of X cells indicates that perturbation of this major pathway contributes to the functional impairments that develop from monocular deprivation.

Copyright
Corresponding author
Address correspondence to: Kevin Duffy, Department of Psychology and Neuroscience, Dalhousie University, Life Sciences Center, 1459 Oxford St, Halifax, Nova Scotia B3H 4R2, Canada. E-mail: kevin.duffy@dal.ca
References
Hide All
Antonini, A. & Stryker, M.P. (1993). Rapid remodeling of axonal arbors in the visual cortex. Science 260, 18191821.
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. The Journal of Neuroscience 18, 65496557.
Cleland, B.G., Dubin, M.W. & Levick, W.R. (1971). Sustained and transient neurones in the cat’s retina and lateral geniculate nucleus. The Journal of Physiology (London) 217, 473496.
Derrington, A.M. & Hawken, M.J. (1981). Spatial and temporal properties of cat geniculate neurones after prolonged deprivation. The Journal of Physiology (London) 314, 107120.
Dreher, B., Fukada, Y. & Rodieck, R.W. (1976). Identification, classification and anatomical segregation of cells with X-like and Y-like properties in the lateral geniculate nucleus of old-world primates. The Journal of Physiology (London) 258, 433452.
Dreher, B. & Sefton, A.J. (1979). Properties of neurons in cat’s dorsal lateral geniculate nucleus: A comparison between medial interlaminar and laminated parts of the nucleus. The Journal of Comparative Neurology 183, 4764.
Duffy, K.R., Crowder, N.A. & LeDue, E.E. (2012). Investigation of cytoskeleton proteins in neurons of the cat lateral geniculate nucleus. The Journal of Comparative Neurology 520, 186199.
Duffy, K.R. & Mitchell, D.E. (2013). Darkness alters maturation of visual cortex and promotes fast recovery from monocular deprivation. Current Biology: CB 23, 382386.
Duffy, K.R. & Slusar, J.E. (2009). Monocular deprivation provokes alteration of the neuronal cytoskeleton in developing cat lateral geniculate nucleus. Visual Neuroscience 26, 319328.
Enroth-Cugell, C. & Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells of the cat. The Journal of Physiology (London) 187, 517552.
Friedlander, M.J., Lin, C.S., Stanford, L.R. & Sherman, S.M. (1981). Morphology of functionally identified neurons in lateral geniculate nucleus of the cat. Journal of Neurophysiology 46, 80129.
Friedlander, M.J. & Stanford, L.R. (1984). Effects of monocular deprivation on the distribution of cell types in the LGNd: A sampling study with fine-tipped micropipettes. Experimental Brain Research 53, 451461.
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. The Journal of Neuroscience 2, 321330.
Fukuda, Y. (1973). Differentiation of principal cells of the rat lateral geniculate body into two groups; fast and slow cells. Experimental Brain Research 17, 242260.
Garraghty, P.E., Roe, A.W., Chino, Y.M. & Sur, M. (1994). Abnormal development of retinogeniculate X axons in strabismic cats: A possible substrate for visual dysfunction. Neuroscience Letters 165, 223226.
Goldstein, M.E., Sternberger, L.A. & Sternberger, N.H. (1987). Varying degrees of phosphorylation determine microheterogeneity of the heavy neurofilament polypeptide (Nf-H). The Journal of Neuroimmunology 14, 135148.
Groszer, M., Keays, D.A., Deacon, R.M., de Bono, J.P., Prasad-Mulcare, S., Gaub, S., Baum, M.G., French, C.A., Nicod, J. & Coventry, J.A. (2008). Impaired synaptic plasticity and motor learning in mice with a point mutation implicated in human speech deficits. Current Biology: CB 18, 354362.
Guillery, R.W. (1966). A study of Golgi preparations from the dorsal lateral geniculate nucleus of the adult cat. The Journal of Comparative Neurology 128, 2150.
Guillery, R.W. (1973). The effect of lid suture upon the growth of cells in the dorsal lateral geniculate nucleus of kittens. The Journal of Comparative Neurology 148, 417422.
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. The Journal of Comparative Neurology 139, 413421.
Haesler, S., Wada, K., Nshdejan, A., Morrisey, E.E., Lints, T., Jarvis, E.D. & Scharff, C. (2004). FoxP2 expression in avian vocal learners and non-learners. The Journal of Neuroscience 24, 31643175.
Headon, M.P. & Powell, T.P. (1973). Cellular changes in the lateral geniculate nucleus of infant monkeys after suture of the eyelids. Journal of Anatomy 116, 135145.
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, 854862.
Hickey, T.L. (1980). Development of the dorsal lateral geniculate nucleus in normal and visually deprived cats. The Journal of Comparative Neurology 189, 467481.
Hockfield, S. & Sur, M. (1990). Monoclonal antibody Cat-301 identifies Y-cells in the dorsal lateral geniculate nucleus of the cat. The Journal of Comparative Neurology 300, 320330.
Hoffmann, K.P. & Sireteanu, R. (1977). Interlaminar differences in the effects of early and late monocular deprivation on the visual acuity of cells in the lateral geniculate nucleus of the cat. Neuroscience Letters 5, 171175.
Hoffmann, K.P., Stone, J. & Sherman, S.M. (1972). Relay of receptive-field properties in dorsal lateral geniculate nucleus of the cat. Journal of Neurophysiology 35, 518531.
Horton, J.C. & Hocking, D.R. (1997). Timing of the critical period for plasticity of ocular dominance columns in macaque striate cortex. The Journal of Neuroscience 17, 36843704.
Ikeda, H. & Wright, M.J. (1976). Properties of LGN cells in kittens reared with convergent squint: A neurophysiological demonstration of amblyopia. Experimental Brain Research 25, 6377.
Iwai, L., Ohashi, Y., van der List, D., Usrey, W.M., Miyashita, Y. & Kawasaki, H. (2012). FoxP2 is a parvocellular-specific transcription factor in the visual thalamus of monkeys and ferrets. Cerebral Cortex 23, 22042212.
Jones, K.R., Kalil, R.E. & Spear, P.D. (1984). Effects of strabismus on responsivity, spatial resolution, and contrast sensitivity of cat lateral geniculate neurons. Journal of Neurophysiology 52, 538552.
Julien, J.P. & Mushynski, W.E. (1982). Multiple phosphorylation sites in mammalian neurofilament polypeptides. The Journal of Biological Chemistry 257, 1046710470.
Kutcher, M.R. & Duffy, K.R. (2007). Cytoskeleton alteration correlates with gross structural plasticity in the cat lateral geniculate nucleus. Visual Neuroscience 24, 775785.
Lai, C.S., Fisher, S.E., Hurst, J.A., Vargha-Khadem, F. & Monaco, A.P. (2001). A forkhead-domain gene is mutated in a severe speech and language disorder. Nature 413, 519523.
Lehmkuhle, S., Kratz, K.E., Mangel, S.C. & Sherman, S.M. (1980). Effects of early monocular lid suture on spatial and temporal sensitivity of neurons in dorsal lateral geniculate nucleus of the cat. Journal of Neurophysiology 43, 542556.
LeVay, S. & Ferster, D. (1977). Relay cell classes in the lateral geniculate nucleus of the cat and the effects of visual deprivation. The Journal of Comparative Neurology 172, 563584.
LeVay, S., Wiesel, T.N. & Hubel, D.H. (1980). The development of ocular dominance columns in normal and visually deprived monkeys. The Journal of Comparative Neurology 191, 151.
MacDermot, K.D., Bonora, E., Sykes, N., Coupe, A.M., Lai, C.S., Vernes, S.C., Vargha-Khadem, F., McKenzie, F., Smith, R.L., Monaco, A.P. & Fisher, S.E. (2005). Identification of FOXP2 truncation as a novel cause of developmental speech and language deficits. The American Journal of Human Genetics 76, 10741080.
Matsubara, J.A. & Boyd, J.D. (2002). Relationship of LGN afferents and cortical efferents to cytochrome oxidase blobs. In The Cat Primary Visual Cortex, ed. Payne, P.R. & Peters, A., pp. 221258. San Diego, CA: Academic Press.
Mitchell, D.E., Kennie, J. & Duffy, K.R. (2011). Preference for binocular concordant visual input in early postnatal development remains despite prior monocular deprivation. Vision Research 51, 13511359.
Mooney, R.D., Dubin, M.W. & Rusoff, A.C. (1979). Interneuron circuits in the lateral geniculate nucleus of monocularly deprived cats. The Journal of Comparative Neurology 187, 533544.
Mower, G.D. & Christen, W.G. (1982). Effects of early monocular deprivation on the acuity of lateral geniculate neurons in the cat. Brain Research 255, 475480.
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. The Journal of Neuroscience 7, 15261536.
Nassi, J.J. & Callaway, E.M. (2009). Parallel processing strategies of the primate visual system. Nature Reviews. Neuroscience 10, 360372.
Noda, H. & Iwama, K. (1967). Unitary analysis of retino-geniculate response time in rats. Vision Research 7, 205213.
Olson, C.R. & Freeman, R.D. (1980). Profile of the sensitive period for monocular deprivation in kittens. Experimental Brain Research 39, 1721.
Robson, J.A. & Martin-Elkins, C.L. (1985). The effects of monocular deprivation on the size of GAD+ neurons in the cat’s dorsal lateral geniculate nucleus. The Journal of Comparative Neurology 239, 6274.
Sanderson, K.J. (1971). The projection of the visual field to the lateral geniculate and medial interlaminar nuclei in the cat. The Journal of Comparative Neurology 143, 101108.
Saul, A.B. & Humphrey, A.L. (1990). Spatial and temporal response properties of lagged and nonlagged cells in cat lateral geniculate nucleus. Journal of Neurophysiology 64, 206224.
Shapley, R. & So, Y.T. (1980). Is there an effect of monocular deprivation on the proportions of X and Y cells in the cat lateral geniculate nucleus? Experimental Brain Research 39, 4148.
Sherman, S.M., Hoffmann, K.P. & Stone, J. (1972). Loss of a specific cell type from dorsal lateral geniculate nucleus in visually deprived cats. Journal of Neurophysiology 35, 532541.
Sherman, S.M., Wilson, J.R., Kaas, J.H. & Webb, S.V. (1976). X- and Y-cells in the dorsal lateral geniculate nucleus of the owl monkey (Aotus trivirgatus). Science 192, 475477.
Sireteanu, R. & Hoffman, K.P. (1979). Relative frequency and visual resolution of X- and Y-cells in the LGN of normal and monocularly deprived cats: Interlaminar differences. Experimental Brain Research. 34, 591603.
So, Y.T. & Shapley, R. (1979). Spatial properties of X and Y cells in the lateral geniculate nucleus of the cat and conduction velocities of their inputs. Experimental Brain Research 36, 533550.
Stone, J. & Hoffman, K.P. (1971). Conduction velocity as a parameter in the organisation of the afferent relay in the cat’s lateral geniculate nucleus. Brain Research 32, 454459.
Teramitsu, I. & White, S.A. (2006). FoxP2 regulation during undirected singing in adult songbirds. The Journal of Neuroscience 26, 73907394.
Vital-Durand, F., Garey, L.J. & Blakemore, C. (1978). Monocular and binocular deprivation in the monkey: Morphological effects and reversibility. Brain Research 158, 4564.
von Noorden, G.K. & Crawford, M.L. (1978). Morphological and physiological changes in the monkey visual system after short-term lid suture. Investigative Ophthalmology & Visual Science 17, 762768.
Weng, C., Yeh, C.I., Stoelzel, C.R. & Alonso, J.M. (2005). Receptive field size and response latency are correlated within the cat visual thalamus. Journal of Neurophysiology 93, 35373547.
Wiesel, T.N. & Hubel, D.H. (1963 a). Effects of visual deprivation on morphology and physiology of cells in the cats lateral geniculate body. Journal of Neurophysiology 26, 978993.
Wiesel, T.N. & Hubel, D.H. (1963 b). Single-cell responses in striate cortex of kittens deprived of vision in one eye. Journal of Neurophysiology 26, 10031017.
Wilson, P.D., Rowe, M.H. & Stone, J. (1976). Properties of relay cells in cat’s lateral geniculate nucleus: A comparison of W-cells with X- and Y-cells. Journal of Neurophysiology 39, 11931209.
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