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Structural and functional composition of the developing retinogeniculate pathway in the mouse

Published online by Cambridge University Press:  06 December 2005

LISA JAUBERT-MIAZZA
Affiliation:
Department of Cell Biology and Anatomy, Louisiana State Health Sciences Center, New Orleans
ERICK GREEN
Affiliation:
Department of Cell Biology and Anatomy, Louisiana State Health Sciences Center, New Orleans
FU-SUN LO
Affiliation:
Department of Cell Biology and Anatomy, Louisiana State Health Sciences Center, New Orleans
KIM BUI
Affiliation:
Department of Cell Biology and Anatomy, Louisiana State Health Sciences Center, New Orleans
JEREMY MILLS
Affiliation:
Department of Cell Biology and Anatomy, Louisiana State Health Sciences Center, New Orleans
WILLIAM GUIDO
Affiliation:
Department of Cell Biology and Anatomy, Louisiana State Health Sciences Center, New Orleans

Abstract

The advent of transgenic mice has made the developing retinogeniculate pathway a model system for targeting potential mechanisms that underlie the refinement of sensory connections. However, a detailed characterization of the form and function of this pathway is lacking. Here we use a variety of anatomical and electrophysiological techniques to delineate the structural and functional changes occurring in the lateral geniculate nucleus (LGN) of dorsal thalamus of the C57/BL6 mouse. During the first two postnatal weeks there is an age-related recession in the amount of terminal space occupied by retinal axons arising from the two eyes. During the first postnatal week, crossed and uncrossed axons show substantial overlap throughout most of the LGN. Between the first and second week retinal arbors show significant pruning, so that by the time of natural eye opening (P12–14) segregation is complete and retinal projections are organized into distinct eye-specific domains. During this time of rapid anatomical rearrangement, LGN cells could be readily distinguished using immunocytochemical markers that stain for NMDA receptors, GABA receptors, L-type Ca2+ channels, and the neurofilament protein SMI-32. Moreover, the membrane properties and synaptic responses of developing LGN cells are remarkably stable and resemble those of mature neurons. However, there are some notable developmental changes in synaptic connectivity. At early ages, LGN cells are binocularly responsive and receive input from as many as 11 different retinal ganglion cells. Optic tract stimulation also evokes plateau-like depolarizations that are mediated by the activation of L-type Ca2+ channels. As retinal inputs from the two eyes segregate into nonoverlapping territories, there is a loss of binocular responsiveness, a decrease in retinal convergence, and a reduction in the incidence of plateau potentials. These data serve as a working framework for the assessment of phenotypes of genetically altered strains as well as provide some insight as to the molecular mechanisms underlying the refinement of retinogeniculate connections.

Type
Research Article
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

Bartlett, E. & Smith, P.H. (1999). Anatomic, intrinsic, and synaptic properties of dorsal and ventral division in rat medial geniculate body. Journal of Neurophysiology 81, 19992016.Google 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(16), 65496557.Google Scholar
Budde, T., Munsch, T., & Pape, H.C. (1998). Distribution of L-type calcium channels in rat thalamic neurones. European Journal of Neuroscience 10(2), 586597.Google 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, 58.Google Scholar
Chapman, B. (2000). Necessity for afferent activity to maintain eye-specific segregation in ferret lateral geniculate nucleus. Science 287, 24792482.Google Scholar
Chen, C. & Regehr, W.G. (2000). Developmental remodeling of the retinogeniculate synapse. Neuron 28(3), 955966.Google Scholar
Cork, R.J., Namkung, Y., Shin, H.S., & Mize, R.R. (2001). Development of the visual pathway is disrupted in mice with a targeted disruption of the calcium channel beta(3)-subunit gene. Journal of Comparative Neurology 440, 177191.Google Scholar
Cramer, K.S. & Sur, M. (1995). Activity dependent remodeling of connections in the mammalian visual system. Current Opinion in Neurobiology 5(1), 106111.Google Scholar
Crunelli, V., Haby, M., Jassik-Gerschenfeld, D., Leresche, N., & Pirchio, M. (1988). Cl- and K+ dependent inhibitory postsynaptic potentials evoked by interneurones of the rat lateral geniculate nucleus. Journal of Physiology 399, 153176.Google Scholar
Crunelli, V., Kelly, J.S., Leresche, N., & Pirchio, M. (1987). The ventral and lateral geniculate nucleus of the rat: Intracellular recordings. Journal of Physiology 384, 587601.Google Scholar
Demas, J., Eglen, S.J., & Wong, R.O. (2003). Developmental loss of synchronous spontaneous activity in the mouse retina is independent of visual experience. Journal of Neuroscience, 28512860.Google Scholar
Dicaprio, R. (1997). Plateau potentials in motor neurons in the ventilatory system of the crab. Journal of Experimental Biology 200, 17251736.Google Scholar
Feller, M.B. (2002). The role of nAChR-mediated spontaneous retinal activity in visual system development. Journal of Neurobiology 53, 556567.Google Scholar
Feller, M.B., Wellis, D.P., Stellwagen, D., Werblin, F.S., & Shatz, C.J. (1996). Requirement for cholinergic synaptic transmission in the propagation of spontaneous retinal waves. Science 272, 11821187.Google Scholar
Ghosh, A. & Greenberg, M.E. (1995). Calcium signaling in neurons: Molecular mechanisms and cellular consequences. Science 268, 239247.Google Scholar
Godement, P., Salaun, J., & Imbert, M. (1984). Prenatal and postnatal development of retinogeniculate and retinocollicular projections in the mouse. Journal of Comparative Neurology 230(4), 552575.Google Scholar
Goodman, C.S. & Shatz, C.J. (1993). Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 72 (Suppl.) 7798.Google Scholar
Greenberg, M.E. & Ziff, E.B. (2001). Activity dependent regulation of gene expression. In Synapses, eds. Cowan, W.M., Sudhof, T.C. & Stevens, C.F., pp. 357392. Baltimore, Maryland: Johns Hopkins University Press.
Grossman, A., Lieberman, A.R., & Webster, K.E. (1973). A Golgi study of the rat lateral geniculate nucleus. Journal of Comparative Neurology 150, 441446.Google Scholar
Grubb, M.S., Rossi, F.M., Changeux, J.-P., & Thompson, I.D. (2003). Abnormal functional organization in the dorsal lateral geniculate nucleus of mice lacking the beta 2 subunit of the nicotinic acetylcholine receptor. Neuron 40, 11611172.Google Scholar
Grubb, M.S. & Thompson, I.D. (2003). Quantitative characterization of visual response properties in the mouse dorsal lateral geniculate nucleus. Journal of Neurophysiology 90, 35943607.Google Scholar
Grubb, M.S. & Thompson, I.D. (2004). The influence of early experience on the development of sensory systems. Current Opinion in Neurobiology 14, 503512.Google Scholar
Guido, W., Günhan-Agar, E., & Erzurumlu, R.S. (1998). Developmental changes in the electrophysiological properties of brainstem trigeminal neurons during pattern (barrelette) formation. Journal of Neurophysiology 79, 12951306.Google Scholar
Guido, W., Lo, F.S., & Erzurumlu, R.S. (1997). An in vitro model of kitten retinogeniculate pathway. Journal of Neurophysiology 77, 511516.Google Scholar
Guido, W., Lo, F.S., & Erzurumlu, R.S. (2001). Synaptic plasticity in the trigeminal nucleus during the period of barrelette formation and consolidation. Developmental Brain Research 132, 97102.Google Scholar
Guido, W., Ziburkus, J., & Lo, F.S. (2003). Synaptic plasticity in the developing visual thalamus. In The Brain and Sensory Plasticity: Language Acquisition and Hearing, ed. Berlin, C.I. & Weyand, T.G., pp. 75100. New York: Thompson Delmar Learning Press.
Horikawa, K. & Armstrong, W.E. (1988). A versatile means of intracellular labeling: Injection of biocytin and its detection with avidin conjugates. Journal of Neuroscience Methods 25, 111.Google Scholar
Hu, B. (1993). Membrane potential oscillations and corticothalamic connectivity in rat associational thalamic neurons in vitro. Acta Physiologica Scandanavia 148, 109113.Google Scholar
Huberman, A.D., Stellwagen, D., & Chapman, B. (2002). Decoupling eye specific segregation from lamination in the lateral geniculate nucleus. Journal of Neuroscience 22(21), 94199429.Google Scholar
Huh, G.S., Boulanger, L.M., Du, H., Riquelme, P.A., Brotz, T.M., & Shatz, C.J. (2000). Functional requirement for class I MHC in CNS development and plasticity. Science 290(5499), 21552159.Google Scholar
Jeffery, G. (1984). Retinal ganglion cell death and terminal field retraction in the developing rodent visual system. Developmental Brain Research 13, 8196.Google Scholar
Kiehn, O. & Eken, T. (1998). Functional role of plateau potentials in vertebrate motor neurons. Currrent Opinion in Neuroscience 8, 746752.Google Scholar
Li, J., Bickford, M.E., & Guido, W. (2003). Distinct firing properties of higher order thalamic relay neurons. Journal of Neurophysiology 90, 291199.Google Scholar
Lo, F.S. & Erzurumlu, R.S. (2002). L-type calcium channel-mediated plateau potentials in barrelette cells during structural plasticity. Journal of Neurophysiology 88, 794801.Google Scholar
Lo, F.S. & Mize, R.R. (2000). Synaptic regulation of L-type Ca2+ channel activity and long-term depression during refinement of the retinocollicular pathway in developing rodent superior colliculus. Journal of Neuroscience 20, 16.Google Scholar
Lo, F.S., Ziburkus, J., & Guido, W. (2002). Synaptic mechanisms regulating the activation of a Ca2+ mediated plateau potential in developing relay cells of the lateral geniculate nucleus. Journal of Neurophysiology 87, 11751185.Google Scholar
Lu, W. & Constantine-Paton, M. (2004). Eye opening rapidly induces synaptic potentiation and refinement. Neuron 43, 237249.Google Scholar
Maffei, L. & Galli-Resta, L. (1990). Correlation in the discharges of neighboring rat retinal ganglion cells during prenatal life. Proceedings of the National Academy of Sciences of the U.S.A. 87(7), 28612864.Google Scholar
Magee, J.C. & Johnston, D. (1997). A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275(5297), 209213.Google Scholar
Mastronarde, D.N. (1987). Two classes of single input X cells in cat lateral geniculate nucleus. II Retinal inputs and the generation of receptive field properties. Journal of Neurophysiology 57, 381413.Google Scholar
McCormick, D.A. (1991). Functional properties of a slowly inactivating potassium current in guinea pig dorsal lateral geniculate relay neurons. Journal of Neurophysiology 66, 11761189.Google Scholar
Meister, M., Wong, R.O., Baylor, D.A., & Shatz, C.J. (1991). Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 252, 939943.Google Scholar
Mermelstein, P.G., Bito, H., Deisseroth, K., & Tsien, R.W. (2000). Critical dependence of cAMP response element-binding protein phosphorylation on L-type calcium channels supports a selective response to EPSPs in preference to action potentials. Journal of Neuroscience 20(1), 266273.Google Scholar
Montero, V.M. & Singer, W. (1985). Ultrastructural identification of somata and neural processes immunoreactive to antibodies against glutamic acid decarboxylase (GAD) in the dorsal lateral geniculate of the cat. Experimental Brain Research 59, 151165.Google Scholar
Mooney, R., Madison, D.V., & Shatz, C.J. (1993). Enhancement of transmission at the developing retinogeniculate synapse. Neuron 10(5), 815825.Google Scholar
Mooney, R., Penn, A.A., Gallego, R., & Shatz, C.J. (1996). Thalamic relay of spontaneous retinal activity prior to vision. Neuron 17(5), 863874.Google Scholar
Muir-Robinson, G., Hwang, B.J., & Feller, M.B. (2002). Retinogeniculate axons undergo eye specific segregation in the absence of eye specific layers. Journal of Neuroscience 22(13), 52595264.Google Scholar
Parnavelas, J.G., Mounty, E.J., Bradford, R., & Lieberman, A.R. (1977). The postnatal development of neurons in the dorsal lateral geniculate nucleus of the rat: A Golgi study. Journal of Comparative Neurology 171, 481500.Google Scholar
Penn, A.A., Riquelme, P.A., Feller, M.B., & Shatz, C.J. (1998). Competition in retinogeniculate patterning driven by spontaneous activity. Science 279(5359), 21082112.Google Scholar
Pham, T.A., Rubenstein, J.L., Silva, A.J., Storm, D.R., & Stryker, M.P. (2001). The CRE/CREB pathway is transiently expressed in thalamic circuit development and contributes to refinement of retinogeniculate axons. Neuron 31(3), 409420.Google Scholar
Rekling, J.C. & Feldman, J.L. (1997). Calcium-dependent plateau potentials in rostral ambiguous neurons in the newborn mouse brain stem in vitro. Journal of Neurophysiology 78, 24832492.Google Scholar
Reese, B.E. (1988). ‘Hidden lamination’ in the dorsal lateral geniculate nucleus: The functional organization of this thalamic region in the rat. Brain Research 472(2), 119137.Google Scholar
Rossi, F.M., Pizzorusso, T., Porciatti, V., Marubio, L.M., Maffei, L., & Changeux, J.P. (2001). Requirement of the nicotinic acetylcholine receptor beta 2 subunit for the anatomical and functional development of the visual system. Proceedings of the National Academy of Sciences of the U.S.A. 98(11), 64536458.Google Scholar
Shatz, C.J. (1983). The prenatal development of the cat's retinogeniculate pathway. Journal of Neuroscience 3, 482489.Google Scholar
Shatz, C.J. (1990). Impulse activity and the patterning of connections during CNS development. Neuron 5(6), 745756.Google Scholar
Shatz, C.J. (1996). Emergence of order in visual system development. Proceedings of the National Academy of Sciences of the U.S.A. 93(2), 602608.Google Scholar
Shatz, C.J. & Kirkwood, P.A. (1984). Prenatal development of functional connections in the cat's retinogeniculate pathway. Journal of Neuroscience 3, 482489.Google Scholar
Shatz, C.J. & Stryker, M.P. (1988). Prenatal tetrodotoxin infusion blocks segregation of retinogeniculate afferents. Science 242(4875), 8789.Google Scholar
Sherman, S.M. & Spear, P.D. (1982). Organization of visual pathways in normal and visually deprived cats. Physiological Reviews 62(2), 738855.Google Scholar
Sretavan, D.W., Shatz, C.J., & Stryker, M.P. (1988). Modification of retinal ganglion cell axon morphology by prenatal infusion of tetrodotoxin. Nature 336(6198), 468471.Google Scholar
Stellwagen, D. & Shatz, C.J. (2002). An instructive role for retinal waves in the development of retinogeniculate connectivity. Neuron 33, 357367.Google Scholar
Tavazoie, S.F. & Reid, R.C. (2000). Diverse receptive fields in the lateral geniculate nucleus during thalamocortical development. Nature Neuroscience 3(6), 608616.Google Scholar
Tootle, J.S. & Friedlander, M.J. (1986). Postnatal development of receptive field surround inhibition in kitten dorsal lateral geniculate nucleus. Journal of Neuroscience 56, 523541.Google Scholar
Torborg, C.L. & Feller, M.B. (2004). Unbiased analysis of bulk axonal segregation patterns. Journal of Neuroscience Methods 135, 1726.Google Scholar
Torborg, C.L., Hansen, K.A., & Feller, M.B. (2005). High frequency, synchronized bursting drives eye-specific segregation of retinogeniculate projections. Nature Neuroscience 8(1), 7278.Google Scholar
Usrey, W.M., Reppas, J.B., & Reid, C.R. (1999). Specificity and strength of retinogeniculate connections. Journal of Neurophysiology 82, 35273540.Google Scholar
Webster, M.J. & Rowe, M H. (1984). Morphology of identified relay cells and interneurons in the dorsal lateral geniculate nucleus. Experimental Brain Research 56, 468474.Google Scholar
Williams, S.R., Turner, J.P., Anderson, C.M., & Crunelli, V. (1996). Electrophysiological and morphological properties of interneurons in the rat dorsal lateral geniculate nucleus. Journal of Physiology 490, 129147.Google Scholar
Wong, R.O. (1999). Retinal waves and visual system development. Annual Review of Neuroscience 22, 2947.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, 187196.Google Scholar
Ziburkus, J. & Guido, W. (2005). Loss of binocular responses and reduced retinal convergence during the period of retinogeniculate axon segregation. Journal of Neurophysiology (accepted with revision).Google Scholar
Ziburkus, J., Lo, F.-S., & Guido, W. (2003). Nature of inhibitory postsynaptic activity in developing relay cells of the lateral geniculate nucleus. Journal of Neurophysiology 90, 10631070.Google Scholar