Abstract
One of the most striking features of mammalian sensory systems is the extremely precise way that peripheral receptors are mapped onto the brain. A fundamental task of developmental neurobiology is to understand how these highly specific connection patterns arise. The development of the nervous system can be conveniently divided into 2 stages. The first one, which includes neurogenesis, differentiation, migration and axonal guidance, is usually regarded as being activity-independent. The second stage, which is primarily concerned with the fine-tuning of initial connections to produce the highly specific connection patterns characteristic of the adult, is often regarded as being activity-dependent. The visual system of some mammalian species has proven very useful for examination of the role which activity plays in the refinement of connections. The focus of the work described here is upon the developmental mechanisms through which the characteristic organization of the retinogeniculate pathway in the ferret is produced. This article will review this work in the context of other relevant literature in the field.
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References
Abe, K., A. Mizutani and H. Saito (1994) Possible role of nitic oxide in long-term potentiation in the dentate gyrus. In: Nitric Oxide: roles in neuronal communication and neurotoxicity. H. Takagi, N. Toda and R.D. Hawkins (eds). Japan Scientific Series. Tokyo. pp149–159.
Allendoerfer, K.L., R.J. Cabelli, E. Escandon, D.R. Kaplan, K. Nikolics and C.J. Shatz (1994) Regulation of neurotrophin receptors during the maturation of the mammalian visual system. J. Neurosci., 14: 1795–1811.
Arancio, O., E.R. Kandel and R.D. Hawkins (1995) Activity-dependent long-term enhancement of transmitter release by presynaptic 3′,5′-cyclic cGMP in cultured hippocampal neurons. Nature, 376: 74–80.
Arancio, O., M. Kiebler, C. Justin-Lee, V. Lev-Ram, R.Y. Tsien, E.R. Kandel and R.D. Hawkins (1996) Nitric oxide acts directly in the presynaptic neuron to produce long-term potentiation. Cell, 87: 1025–1035.
Baader, S.L., S. Bucher and K. Schilling (1997) The developmental expression of neuronal nitric oxide synthase in cerebellar granule cells is sensitive to GABA and neurotrophins. Developmental Neuroscience, 19: 283–290.
Bear, M.F., W.A. Press and B.W. Connors (1992) Long-term potentiation in slices of kitten visual cortex and the effects of NMD A receptor blockade.
Bekkers, J.M. and C.F. Stevens (1990) Presynaptic mechanism for long-term potentiation in the hippocampus. Nature, 346: 724–729.
Cabelli, R.J., A. Hohn and C.J. Shatz (1995) Inhibition of ocular dominance column formation by infusion of NT4/5 or BDNF. Science, 267: 1662–1666
Cabelli, R.J., K.L. Allendoerfer, M.J. Radeke, A.A. Welcher, S.C. Feinstein and C.J. Shatz. (1996) Changing patterns of expression and subcellular localization of TrkB in the developing visal system. J. Neurosci., 16: 7965–7980.
Cabelli, R.J., B.L. Shelton, R.A. Segal and C.J. Shatz (1997) Blockade of endogenous ligands of TrkB inhibits formation of ocular dominance columns. Neuron, 19: 63–76.
Carmignoto, G. and S. Vicini (1992) Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. Science, 258: 1007–1011.
Cohen-Cory, S. and S.E. Fraser (1995) Effects of brain-derived neurotrophic factor on optic axon remodelling in vivo. Nature, 378: 192–196.
Collingridge, G.L. and T.V.P. Bliss (1987) NMDA receptors — their role in long-term potentiation. TINS, 10: 288–293.
Cook, P.M., G. Prusky and A.S. Ramoa (1996) Role of spontaneous activity in reorganization of retinogeniculate connections. Soc. Neurosci. Abst., 22: 761.
Crair, M.C. and R.C. Malenka (1995) A critical period for long-term potentiation at thalamocortical synapses. Nature, 365: 325–328.
Cramer, K.S. and M. Sur (1997) Blockade of afferent impulse activity disrupts on/off sublamination in the ferret lateral geniculate nucleus. Dev. Brain Res., 98: 287–290.
Cramer, K.S. and M. Sur (1996) The role of NMDA receptors and nitric oxide in retinogeniculate development. Progress in Brain Research, 108: 235–244.
Cramer, K.S., C.I. Moore and M. Sur (1995) Transient expression of NADPH-diaphorase in the lateral geniculate nucleus of the ferret during early postnatal development. J. Comp. Neurol., 353: 306–316.
Cramer, K.S., A. Angelucci, J-O. Hahm, M. Bogdanov and M. Sur (1996) A role for nitric oxide in the development of the ferret retinogeniculate projection. J. Neurosci., 16: 7995–8004.
East, S.J. and J. Garthwaite (1991) NMDA receptor activation in rat hipocampus induces cyclic GMP formation through the L-arginine-nitiric oxide pathway. Neurosci. Lett., 123: 17–19.
Ernfos, P., J. Bengzon, Z. Kokaia, H. Persson and O. Lindvall (1992) Increased levels of messenger RNAs for neurotrophic factors in the brain during kindling eliptogenesis. Neuron, 7: 165–176.
Ferreira, A., K.S. Kosikl, P. Greengard and H.-Q. Han (1994) Aberrant neurites and synaptic vesicle protein deficiency in synapsin II depleted neurons. Science, 264: 977–979.
Galli, L. and L. Maffei (1988) Spontaneous impulse activity of rat retinal ganglion cells in prenatal life. Science, 242:90–91.
Galuske, R.A., D.-S. Kim, E. Castren, H. Thoenen and W. Singer, (1996) Brain-derived neurotrophic factor reverses experience-dependent synaptic modifications in kitten visual cortex. Eur. J. Neurosci., 8: 1554–1559.
Green, L.A. and D.R. Kaplan (1995) Early events in neurotrophin signalling via Trk and p75 receptors. Curr. Op. Neurobiol., 5: 579–587.
Greengard, P., F. Valtorta, A.J. Czernik and F. Benfenati (1993) Synaptic vesicle phosphoproteins and regulation of synaptic function. Science, 259: 780–785.
Hahm, J.-O., R.B. Langdon and M. Sur (1991) Disruption of retinogeniculate afferent segregation by antagonists to NMDA receptors. Nature, 351: 568–570.
Hahm, J., K. Cramer and M. Sur (1997) Pattern formation by retinal afferents in the ferret lateral geniculate nucleus: Developmental segregation and the role of NMDA receptors. J. Comp. Neurol., submitted.
Han, H.-Q., R.A. Nichols, M.R. Rubin, M. Bahler and P. Greengard (1991) Induction of formation of presynaptic terminals in neuroblastoma cells by synapsin IIb. Nature, 349: 697–800.
Hindley, S., B.H. Juurlink, J.W. Gysbers, P.J. Middlemas, M.A. Herman and M.P. Rathbone. Nitric oxide donors enhance neurotrophin-induced neurite outgrowth through a cGMP-dependent mechanism. J. Neurosci. Res., 47: 427–439.
Holscher, C. (1997) Nitric oxide, the enigmatic neuronal messenger: its role in synaptic plasticity. TINS, 20: 298–303.
Holtzman, D.M., J. Kilbridge, D.S. Bredt, S.M. Black, Y. Li, D.O. Clary, L.F. Reichardt and W.C. Mobley (1994) NOS induction by NGF in basal forebrain cholinergic neurones: evidence for regulation of brain NOS by a neurotrophin. Neurobiology of Disease, 1: 51–60.
Johnson, J.K. and V.A. Casagrande (1993) Prenatal development of axon outgrowth and connectivity in the ferret visual system. Vis. Neurosci., 10: 117–130.
Jovanovic, J., F. Benfenati, Y.L. Siow, T.S. Sihra, J.S. Sanghera, S.L. Pelech, P. Greengard and A.J. Czernik (1996) Neurotrophins stimulate phosphorylation of synapsin I by MAP kinase and regulate synapsin I-actjn interactions. Proc. Natl Acad. Sci., 93: 3679–3683.
Kang, H. and E.M. Schuman (1995) Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science, 267: 1658–1662.
Kantor, D.B., M. Lanzrein, S.J. Stary, G.M. Sandoval, W.B. Smith, B.M. Sullivan, N. Davidson and E.M. Schuman (1996) A role for endothelial NO synthase in LTP revealed by adenovirus-mediated inhibition and rescue. Science, 274: 1744–1748.
Kirkwood, A. and M.F. Bear, (1992) Long-term potentiation in slices of kitten visual cortex and the effects of NMDA receptor blockade. J. Neurophysiol., 67: 841–851.
Kirkwood, A. and M.F. Bear (1994a) Hebbian synapses in visual cortex. J. Neurosci., 14: 1634–1645.
Kirkwood, A. and M.F. Bear (1994b) Homosynaptic long-term depression in the visual cortex. J. Neurosci., 14: 3404–3412.
Kirkwood, A., S.M. Dudek, J.T. Gold, C.C. Aizenman and M.F. Bear (1993) Common forms of synaptic plasticity in the hippocampus and neocortex in vitro. Science, 260: 1518–1521.
Kirkwood, A., H.-K. Lee and M.F. Bear (1995) Co-regulation of long-term potentiation and experience-dependent synaptic plasticity in visual cortex by age and experience. Nature, 375: 328–331.
Kornhauser, J. M. and M.E. Greenberg (1997) A kinase to remember: dual roles for MAP kinase in long-term memory. Neuron, 18: 839–842.
Korte, M., P. Carroll, E. Wolff, G. Brem, H. Thoenen and T. Bonhoeffer (1995) Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc. Nat’l Acad. Sci. USA, 92: 8856–8860.
Kwon, Y.H., M. Esguerra and M. Sur (1991) NMDA and non-NMDA receptors mediate visual responses of neurons in the cat’s lateral geniculate nucleus. J. Neurophysiol., 66: 414–428.
Linden, D.J., R.W. Guillery and J. Cucchiaro (1981) The dorsal lateral geniculate nucleus of the normal ferret and its postnatal development. J. Comp. Neurol., 203: 189–211.
Lo, D.C. (1995) Neurotrophic factors and synaptic plasticity. Neuron, 15: 979–981.
Lohof, A.M., N.Y. Yip and M.-M. Poo (1993) Potentiation of developing neuromuscular synapses by the neurotro-phins NT-3 and BDNF. Nature, 363: 350–353.
Lu, B., P. Greengard and M.-M. Poo (1992) Exogenous synapsin I promotes functional maturation of developing neuromuscular synapses. Neuron, 8: 521–529.
Madison, D. V., R.C. Malenka and R.A. Nicoli (1991) Mechanisms underlying long-term potentiation of synaptic transmission. Ann. Rev. Neurosci., 14: 379–397.
McAllister, A.K., D.C. Lo and L.C. Katz (1995) Neurotrophins regulate dendritic growth in developing visual cortex. Neuron, 15:791–803.
McAllister, A.K., L.C. Katz and D.C. Lo (1996) Neurotrophin regulation of cortical dendritic growth requires activity. Neuron, 17: 1057–1064.
McAllister, A.K., L.C. Katz and D.C. Lo (1997) Opposing roles for endogenous BDNF and NT-3 in regulating cortical dendritic growth. Neuron, 18: 767–778.
Malgoroli, A., A.E. Ting, B. Wendland, A. Bergamaschi, A. Villa, R.W. Tsien, R.H. Scheller (1995) Presynaptic component of long-term potentiation visualised at individual hippocampal synapses. Science, 268: 1624–1628.
Malinow, R. and R.W. Tsien (1990) Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices. Nature, 346: 177–180.
Meister, M., R.O.L. Wong, D.A. Baylor and C.J. Shatz (1991) Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science, 252: 939–943.
Mooney, R., D.V. Madison and Shatz (1993) Enhancement of transmission at the developing retinogeniculate synapse. Neuron, 10: 815–825.
Mooney, R., A.A. Penn, R. Gallego and C.J. Shatz (1996) Thalamic relay of spontaneous retinal activity prior to vision. Neuron, 17: 863–874.
Patterson, S.L., L.M. Grover, P.A. Schwartzkroin and M. Bothwell (1992) Neurotrophin expression in rat hippocampal slices: a stimulus paradigm inducing LTP in CA1 evokes increases in BDNF and NT-3 mRNAs. Neuron, 9: 1081–1088.
Patterson, S.L., T. Abel, T.A.S. Deuel, K.C. Martin, J.C. Rose and E.R. Kandel (1996) Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron, 16: 1137–1145.
Pieribone, V.A., O. Shupliakov, L. Brodin, S. Hilfoker-Rothenfluh, A.J. Czernik and P. Greengard (1995) Distinct pools of synaptic vesicles in neurotransmitter release. Nature, 375, 493–497.
Ramoa, A.S. and D.A. McCormick (1994a) Developmental changes in electrophysiological properties of LGNd neurons during reorganization of retinogeniculate connections. J. Neurosci., 14: 2089–2097.
Ramoa, A.S. amd D.A. McCormick (1994b) Enhanced activation of NMDA receptor responses at the immature retinogeniculate synapse. J. Neurosci., 14: 2098–2105.
Ramoa, A.S. and G. Prusky (1997) Retinal activity regulates developmental switches in functional properties and ifenprodil sensitivity of NMDA receptors in the lateral geniculate nucleus. Dev. Brain Res., 101: 165–175.
Riddle, D.R., D.C. Lo and L.C. Katz (1995) NT-4-mediated rescue of lateral geniculate neurons from effects of monocualr deprivation. Nature, 378: 189–191.
Rocha, M. and M. Sur (1995) Rapid acquisition of dendritic spines by visual thalamic neurons after blockade of N-methyl-D-aspartate receptors. Proc. Natl. Acad. Sci., USA, 92: 8026–8030.
Schoups, A.A., R.C. elliot, W.J. Friedman and I.B. Black, 1995. NGF and BDNF are differentially modified by visual experience in the developing geniculocortical pathway. Dev. Brain Res., 86: 326–334.
Schuman, E.M. and D.V. Madison (1994a) Locally distributed synaptic potentiation in the hippocampus. Science, 263: 532–536.
Schuman, E.M. and D.V. Madison (1994b) Nitric oxide and synpatic function. Ann. Rev. Neurosci., 17: 153–183.
Schuman, E.M., M.K. Meffert, H. Schulman and D.V. Madison (1994) An ADP-ribosyltransferase as a potential target for nitric oxide action in hippocampal long-term potentiation. Proc. Natl. Acad. Sci., USA, 91: 11958–11962.
Segal, R.A. and M.E. Greenberg (1996) Intracellular signalling pathways activated by neurotrophic factors. Ann. Rev. Neurosci., 19: 463–489.
Shatz, C.J. (1983) The prenatal development of the cat’s retinogeniculate pathway. J. Neurosci., 3: 482–499.
Shatz, C.J. and M.P. Stryker (1988) Prenatal tetrodotoxin infusion blocks segregation of retinogeniculate afferents. Science, 242: 87–89.
Sillito, A.M., P.C. Murphy and T.E. Salt (1990) The contribution of the non-N-methyl-D-aspartate group of excitatory amino acid receptors to retinogeniculate transmission in the cat. Neuroscience, 34: 273–280.
Smetters, D.K., J. Hahm and M. Sur (1994) An N-methyl-D-aspartate receptor antagonist does not prevent eye-specific segregation in the ferret retinogeniculate pathway. Brain Res., 658: 168–178.
Son, H., R.D. Hawkins, K. Martin, M. Kiebler, P.L. Huang, M.C. Fishman and E.R. Kandel (1996) Long-term potentiation is reduced in mice that are doubly mutant in endothelial and neuronal nitric oxide synthase. Cell, 87: 1015–1023.
Stretavan, D.W. and C.J. Shatz (1986) Prenatal development of retinal ganglion cell axons: segregation into eye-specific layers within the cat’s lateral geniculate nucleus. J. Neurosci., 6: 234–251.
Styker, M.P. and K.R. Zahs (1983) ON and OFF sublaminae in the lateral geniculate nucleus of the ferret. J. Neurosci., 3: 1943–1951.
Wong, R.O.L., M. Meister and C.J. Shatz (1993) Transient period of correlated bursting activity during development of the mammalian retina. Neuron, 11: 923–938.
Wong, R.O.L., A. Chernjavsky, S.J. Smith and C.J. Shatz (1995) Early functional neural networks in the developing retina. Nature, 374: 716–718.
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Leamey, C.A., Cramer, K.S., Sur, M. (1998). The Role of Activity-Dependent Mechanisms in Pattern Formation in the Retinogeniculate Pathway. In: Chalupa, L.M., Finlay, B.L. (eds) Development and Organization of the Retina. NATO ASI Series, vol 299. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-5333-5_17
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