Abstract
Recent experimental evidence has implicated neurotrophic factors (NTs) in the competitive process believed to drive the development of ocular dominance (OD) columns. Application of excess amounts of particular NTs can prevent the segregation process, suggesting that they could be the substance for which geniculocortical afferents compete during development. We have previously presented a model that accounts for normal OD development as well as the prevention of that development with excess NT. The model uses a Hebbian learning rule in combination with competition for a limiting supply of cortical trophic factor to drive OD segregation, without any weight normalization procedures.
Subsequent experimental evidence has further suggested that NTs may be causally involved in the competitive process. Application of NT antagonist can prevent OD columns by causing inputs from both eyes to be eliminated, suggesting that NTs may be the substance for which geniculocortical afferents compete. Also, excess NT can mitigate the shift to the open eye normally caused by monocular deprivation (MD). In this article, we show that the current model can account for these subsequent experiments. We show that deprivation of NT causes inputs from both eyes to decay and that excess NT can mitigate the shift to the open eye normally seen with MD. We then present predictions of the model concerning the effects of NT on the length of the critical period during which MD is effective. The model presents a novel mechanism for competition between neural populations inspired by particular biological evidence. It accounts for three specific experimental results, and provides several testable predictions.
Similar content being viewed by others
References
Akaneya Y, Tsumoto T, Kinoshita S, Hatanaka H (1997) Brain-derived neurotrophic factor enhances long-term potentiation in rat visual cortex. J. Neurosci. 17:6707-6716.
Berardi N, Cellerino A, Domenici L, Fagiolini M, Pizzorusso T, Cattaneo A (1994) Monoclonal antibodies to nerve growth factor affect the postnatal development of the visual system. Proc. Natl. Acad. Sci. USA 91:684-688.
Blochl A, Thoenen H (1995) Characterization of nerve growth factor (NGF) release from hippocampal neurons: Evidence for a constitutive and an unconventional sodium-dependent regulated pathway. Eur. J. Neurosci. 7:1220-1228.
Brown TH, Ganong AH, Kairiss EW, Keenan CL (1990) Hebbian synapses: Biophysical mechanisms and algorithms. Ann. Rev. Neurosci. 13:475-511.
Cabelli RJ, Hohn A, Shatz CJ (1995) Inhibition of ocular dominance column formation by infusion of NT-4/5 or BDNF. Science 267:1662-1666.
Cabelli RJ, Shelton DL, Segal RA, Shatz CJ (1997) Blockade of endogenous ligands of TrkB inhibits formation of ocular dominance columns. Neuron 19:63-76.
Carmignoto GC, Canella R, Candeo P, Comelli MC, Maffei L (1993) Effects of nerve growth factor on neuronal plasticity of the kitten visual cortex. J. Physiol. 464:343-360.
Castrén E, Zafra F, Thoenen H, Lindholm D (1992) Light regulates expression of brain-derived neurotrophic factor mRNA in rat visual cortex. Proc. Natl. Acad. Sci. USA 89:9444-9448.
Duffy F, Snodgrass R, Burchfiel J, Conway JL (1976) Bicucculine reversal of deprivation amblyopia in the cat. Nature 260:256-257.
Elliot T, Shadbolt NR (1998) Competition for neurotrophic factors: Mathematical analysis. Neural Computation 10:1939-1982.
Erwin E, Obermayer K, Schulten K (1995) Models of orientation and ocular dominance columns in the visual cortex: A critical comparison. Neural Comp. 7:425-468.
Feidler JC, Saul AB, Murthy A, Humphrey AL (1997) Hebbian learning and the development of direction selectivity: The role of geniculate response timings. Network 8:195-214.
Gu G, Singer W (1993) Effects of intracortical infusion of anticholinergic drugs on neuronal plasticity in kitten striate cortex. Eur. J. Neurosci. 5:475-485.
Gu G, Singer W (1995) Involvement of serotonin in developmental plasticity of kitten visual cortex. Eur. J. Neurosci. 7:1146-1153.
Harris AE (1997) A Model of Ocular Dominance Column Development by Competition for Neurotrophic Factor. Ph.D. thesis, University of Pittsburgh.
Harris AE, Ermentrout GB, Small SL (1997) A model of ocular dominance column development by competition for trophic factor. Proc. Natl. Acad. Sci. USA 94:9944-9949.
Hata Y, Katsuyama N, Fukuda M, Ohshima M, Tsumoto T, Hatanaka H (1996) Brain-derived neurotrophic factor disrupts effects of monocular deprivation in kitten visual cortex. In: Society for Neuroscience Abstracts, Society for Neuroscience, Washington, D.C., 1996.
Horton JC, Hocking DR (1996) An adult-like pattern of ocular dominance columns in striate cortex of newborn monkeys prior to visual experience. J. Neurosci. 16:1791-1807.
Hubel D, Wiesel T, LeVay S (1977) Plasticity of ocular dominance columns in monkey striate cortex. Phil. Trans. R. Soc. Lond. B 278:377-409.
Hubel DH, Wiesel TN (1970) The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J. Physiol. 206:419-436.
Kleinschmidt A, Bear MF, Singer W (1987) Blockade of NMDA receptors disrupts experience-dependent plasticity of kitten striate cortex. Science 238:355-358.
Korte M, Carroll P, Wolf E, Brem G, Thoenen H, Bonhoeffer T (1995) Hippocampal long-term potentiation is impaired in mice lacking brain-drived neurotrophic factor. Proc. Natl. Acad. Sci. USA 92:8856-8860.
Korte M, Griesbeck O, Gravel C, Carrol P, Staiger V, Thoenen H, Bonhoeffer T (1996) Virus-mediated gene transfer into hippocampal CA1 region restores long-term potentiation in brain-derived neurotrophic factor mutant mice. Proc. Natl. Acad. Sci. USA 93:12547-12552.
Kyriazi H, Simons DJ (1993) Thalamocortical response transformations in simulated whisker barrels. J. Neurosci. 13:1601-1615.
LeVay SW, Torsten N, Hubel DH (1980) The development of ocular dominance columns in normal and visually deprived monkeys. J. Comp. Neurol. 191:1-51.
Levay S, Stryker M, Shatz CJ (1978) Ocular dominance columns and their development in layer IV of the cat's visual cortex: A quantitative study. J. Comp. Neurol. 179:223-244.
Linden DJ (1994) Long-term synaptic depression in the mammalian brain. Neuron 12:457-472.
Lindholm D, Castrén E, Berzaghi M, Blöchl A, Thoenen H (1994) Activity-dependent and hormonal regulation of neurotrophin mRNA levels in the brain: Implications for neuronal plasticity. J. Neurobio. 25:1362-1372.
Linsker R (1986) From basic network principles to neural architecture. Proc. Natl. Acad. Sci. USA 83:7508-7512, 8390-8394, 8779-8783.
Lowel S (1994) Ocular dominance column development: Strabismus changes the spacing of adjacent columns in cat visual cortex. J. Neurosci. 14:7451-7468.
Miller KD (1990) Correlation-based mechanisms of neural development. In: Gluck MA, Rumelhart DE, eds. Neuroscience and Connectionist Theory. Lawrence Erlbaum, Hillsdale, NJ. pp. 267-353.
Miller KD, Keller JB, Stryker MP (1989) Ocular dominance column development: Analysis and simulation. Science 245:605-615.
Montague PR, Gally JA, Edelman GM (1991) Spatial signalling in the development and function of neural connections. Cerebral Cortex 1:199-220.
Mower GD, Christen WG, Burchfiel JL, Duffy EH (1984). Microiontophoretic bicucculine restores binocular responses to visual cortical neurons in strabismic cats. Brain Res. 309:168-172.
Pinto DJ, Brumberg JC, Simons DJ, Ermentrout GB (1996) A quantitative population model of whisker barrels: Reexamining the Wilson-Cowan equations. J. Comput. Neurosci. 3:247-264.
Reiter HO, Stryker MP (1988) Neural plasticity without postsynaptic action potentials: Less-active inputs become dominant when kitten visual cortical cells are pharmacologically inhibited. Proc. Natl. Acad. Sci. USA 85:3623-3627.
Reiter HO, Waitzman DM, Stryker MP (1986) Cortical activity blockade prevents ocular dominance plasticity in the kitten visual cortex. Exp. Brain Res. 65:182-188.
Shatz C (1990) Impulse activity and the patterning of connections during CNS development. Neuron 5:745-756.
Shatz CJ, Lindstrom S, Wiesel TN (1977) The distribution of afferents representing the right and left eyes in the cat's visual cortex. Brain Res. 131:103-116.
Shatz CJ, Stryker MP (1978) Ocular dominance in layer IV of the cat's visual cortex and the effects of monocular deprivation. J. Physiol. 281:267-283.
Sirosh J, Miikkulainen R (1994) Cooperative self-organization of afferent and lateral connections in cortical maps. Biol. Cybern. 71:65-78.
Stryker MP, Harris WA (1986) Binocular impulse blockade prevents the formation of ocular dominance columns in cat visual cortex. J. Neurosci. 6:2117-2133.
Stryker SL, Strickland MP (1984) Physiological segregation of ocular dominance columns depends on the pattern of afferent electrical activity. Invest. Opthal. Vis. Sci. (suppl.) 25:278.
Swindale NV (1980) A model for the formation of ocular dominance stripes. Proc. R. Soc. Lond. B 208:243-264.
Swindale NV (1988) Role of visual experience in promoting segregation of eye dominance patches in the visual cortex of the cat. J. Comp. Neurol. 267:472-488.
Swindale NV (1996) The development of topography in the visual cortex: A review of models. Network 7:161-247.
Van Sluyters RC, Levitt FB (1980) Experimental strabismus in the kitten. J. Neurophys. 43:686-699.
von der Malsburg C (1973) Self-organization of orientation sensitive cells in the striate cortex. Kybernetik 14:85-100.
Wiesel TN, Hubel DH (1965) Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J. Neurophys. 28:1029-1040.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Harris, A.E., Ermentrout, G.B. & Small, S.L. A Model of Ocular Dominance Column Development by Competition for Trophic Factor: Effects of Excess Trophic Factor with Monocular Deprivation and Effects of Antagonist of Trophic Factor. J Comput Neurosci 8, 227–250 (2000). https://doi.org/10.1023/A:1008997926773
Issue Date:
DOI: https://doi.org/10.1023/A:1008997926773