Skip to main content
SpringerLink
Log in

Modelling the electrotonic structure of starburst amacrine cells in the rabbit retina: A functional interpretation of dendritic morphology

  • Published:
Bulletin of Mathematical Biology Aims and scope Submit manuscript

Abstract

A detailed morphometric analysis of a Lucifer yellow-filled Cb amacrine cell was undertaken to provide raw data for the construction of a neuronal cable model. The cable model was employed to determine whether distal input-output regions of dendrites were electrically isolated from the soma and each other. Calculations of steady state electrotonic current spread suggested reasonable electrical communication between cell body and dendrites. In particular, the centripetal voltage attenuation revealed that a synaptic signal introduced at the distal end of the equivalent dendrite could spread passively along the dendrite and reach the soma with little loss in amplitude. A functional interpretation of this results could favour a postsynaptic rather than a presynaptic scheme for the operation of directional selectivity in the rabbit retina. On the other hand, dendrites of starburst amacrine cells process information electrotonically with a bias towards the centrifugal direction and for a restricted range of membrane resistance values the voltage attenuation in the centripetal direction suggests that the action of these dendrites can be confined locally. A functional interpretation of this result favours a presynaptic version of Vaney's cotransmission model which attempts to explain how the neural network of starburst amacrine cells might account for directionally selective responses observed in the rabbit retina.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Literature

  • Amthor, F. R., C. W. Oyster and E. S. Takahashi. 1984. Morphology of on-off direction-selective ganglion cells in the rabbit retina.Brain Res. 298, 187–190.

    Article  Google Scholar 

  • Ariel, M. and N. W. Daw. 1982. Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells.J. Physiol. (Lond.) 324, 161–185.

    Google Scholar 

  • Barlow, H. B. and R. M. Hill. 1963. Selective sensitivity to direction of movement in ganglion cells of the rabbit retina.Science 139, 412–414.

    Google Scholar 

  • Barlow, H. B., R. M. Hill and W. R. Levick. 1964. Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit.J. Physiol. (Lond.) 173, 377–407.

    Google Scholar 

  • Barlow, H. B. and W. R. Levick. 1965. The mechanism of directionally selective units in rabbit's retina.J. Physiol. (Lond.) 178, 477–504.

    Google Scholar 

  • Borg-Graham, L. J. and N. M. Grzywacz. 1992. A model of the direction selectivity circuit in retina: transformations by neurons singly and in concert. InSingle Neuron Computation, T. McKenna, J. Davis and S. F. Zornetzer (eds), pp. 347–375. Orlando, FL: Academic Press.

    Google Scholar 

  • Bloomfield, S. A. 1991. A comparison of receptive field and dendritic field sizes of amacrine cells in the rabbit retina.Invest. Ophthalmol. Vis. Sci. Suppl. 32, 993.

    Google Scholar 

  • Brandon, C. 1987. Cholinergic neurons in the rabbit retina: dendritic branching and ultrastructural connectivity.Brain Res. 426, 119–130.

    Article  Google Scholar 

  • Brecha, N., D. Johnson, L. Peichl and H. Wassle. 1988. Cholinergic amacrine cells of rabbit retina contain glutamate decarboxylase and γ-aminobutyrate immunoreactivity.Proc. natn. Acad. Sci. U.S.A. 85, 6187–6191.

    Article  Google Scholar 

  • Caldwell, J. H., N. W. Daw and H. J. Wyatt. 1978. Effects of picrotoxin and strychnine on rabbit retinal ganglion cells: lateral interactions for cells with more complex receptive fields.J. Physiol. (Lond.) 276, 277–298.

    Google Scholar 

  • Cole, K. S. 1968.Membrane, Ions and Impulses: A Chapter of Classical Biophysics. Berkeley, CA: California University Press.

    Google Scholar 

  • Coleman, P. A. and R. F. Miller. 1989. Measurements of passive membrane parameters with whole-cell recording from neurons in the intact amphibian retina.J. Neurophysiol. 61, 218–230.

    Google Scholar 

  • Dowling, J. E. 1968. Synaptic organization of the frog retina: an electron microscopic analysis comparing the retinas of frogs and primates.Proc. R. Soc. (Lond.) B 170, 205–228.

    Google Scholar 

  • Dowling, J. E. 1970. Organization of vertebrate retinas.Invest. Ophthalmol. 9, 655–680.

    Google Scholar 

  • Dowling, J. E. 1987.The Retina: An Approachable Part of the Brain. Cambridge, MA: Harvard University Press.

    Google Scholar 

  • Dowling, J. E. and F. S. Werblin. 1969. Organization of the retina of the mudpuppy. I. Synaptic structure.J. Neurophysiol. 32, 315–338.

    Google Scholar 

  • Eccles, J. C. 1957.The Physiology of Nerve Cells. Baltimore: John Hopkins Press.

    Google Scholar 

  • Famiglietti, E. V. 1983a. ‘Starburst’ amacrine cells and cholinergic neurons: mirror-symmetric ON and OFF amacrine cells of rabbit retina.Brain Res. 261, 138–144.

    Article  Google Scholar 

  • Famiglietti, E. V. 1983b. On and off pathways through amacrine cells in mammalian retina: the synaptic connections of ‘starburst’ amacrine cells.Vision Res. 23, 1265–1279.

    Article  Google Scholar 

  • Famiglietti, E. V. 1985. Synaptic organization of on-off directionally selective ganglion cells in rabbit retina.Soc. Neurosci. Abstr. 1, 337.

    Google Scholar 

  • Famiglietti, E. V. 1991. Synaptic organization of starburst amacrine cells in rabbit retina: analysis of serial thin sections by electron microscopy and graphic reconstruction.J. Comp. Neurol. 309, 40–70.

    Article  Google Scholar 

  • Fleshman, J. W., I. Segev and R. E. Burke. 1988. Electrotonic architecture of type-identified α-motoneurons in the cat spinal cord.J. Neurophysiol. 60, 60–85.

    Google Scholar 

  • Glenn, L. L. 1988. Overestimation of the electrical length of neuron dendrites and synaptic electrotonic attenuation.Neurosci. Lett. 91, 112–119.

    Article  Google Scholar 

  • Hines, M. 1989. A program for simulation of nerve equations with branching geometries.Int. J. Biomed. Comput. 24, 55–68.

    Article  Google Scholar 

  • Holmes, W. R. and C. D. Woody. 1989. Effects of uniform and non-uniform synaptic ‘activation-distributions’ on the cable properties of modeled cortical pyramidal neurons.Brain Res. 505, 12–22.

    Article  Google Scholar 

  • Goldstein, S. S. and W. Rall. 1974. Changes of action potential shape and velocity for changing core conductor geometry.Biophys. J. 14, 731–757.

    Google Scholar 

  • Jack, J. J. B., D. Noble and R. W. Tsien. 1975.Electric Current Flow in Excitable Cells. Oxford: Clarendon Press.

    Google Scholar 

  • Leibovic, K. N. 1972.Nervous System Theory: An Introductory Study. New York: Academic Press.

    Google Scholar 

  • Maranto, A. R. 1982. Neuronal mapping: a photooxidation reaction makes Lucifer yellow useful for electron microscopy,Science 217, 953–955.

    Google Scholar 

  • Masland, R. H. and A. Ames. 1976. Responses to acetylcholine of ganglion cells in an isolated mammalian retina.J. Neurophysiol. 39, 1220–1235.

    Google Scholar 

  • Masland, R. H. and M. Tauchi. 1986. The cholinergic amacrine cell.Trends Neurosci. 9, 218–223.

    Article  Google Scholar 

  • Massey, S. C. and M. J. Neal. 1979. The light-evoked release of acetylcholine from the rabbit retina in vivo and its inhibition by gamma-aminobutyric acid.J. Neurochem. 32, 1327–1329.

    Google Scholar 

  • Massey, S. C. and D. A. Redburn. 1982. A tonic gamma-aminobutyric acid-mediated inhibition of cholinergic amacrine cells in rabbit retina.J. Neurosci. 2,1633–1643.

    Google Scholar 

  • Millar, T. J. and I. G. Morgan. 1987. Cholinergic amacrine cells in the rabbit retina synapse onto other cholinergic amacrine cells.Neurosci. Lett. 74, 281–285.

    Article  Google Scholar 

  • Miller, R. F. and S. A. Bloomfield. 1983. Electroanatomy of a unique amacrine cell in the rabbit retina.Proc. natn. Acad. Sci. U.S.A. 80, 3069–3073.

    Article  Google Scholar 

  • Morgan, I. G. and Z.-K. Li. 1990. Are there GABAa receptors on cholinergic amacrine cells?Proc. Aust. Neurosci. Soc. 1, 111.

    Google Scholar 

  • Neal, M. J. and S. C. Massey. 1980. The release of acetylcholine and amino acids from the rabbit retinain vivo.Neurochemistry 1, 191–208.

    Article  Google Scholar 

  • Nelson, R. 1973. A comparison of electrical properties of neurons in Necturus retina.J. Neurophysiol. 36, 519–535.

    Google Scholar 

  • Nitzan, R., I. Segev and Y. Yarom. 1990. Voltage behavior along the irregular dendritic structure of morphologically and physiologically characterized vagal motoneurons in the guinea pig.J. Neurophysiol. 63, 333–346.

    Google Scholar 

  • O'Malley, D. M. and R. H. Masland. 1989. Co-release of acetylcholine and γ-aminobutyric acid by a retinal neuron.Proc. natn. Acad. Sci. U.S.A. 86, 3414–3418.

    Article  Google Scholar 

  • Oyster, C. W. 1968. The analysis of image motion by the rabbit retina.J. Physiol. (Lond.) 199, 613–635.

    Google Scholar 

  • Oyster, C. W. 1989. Neural interactions underlying direction-selectivity in the rabbit retina. InVision: Coding and Efficiency, C. Blakemore (Ed.), pp. 92–102. New York: Cambridge University Press.

    Google Scholar 

  • Oyster, C. W. and H. B. Barlow. 1967. Direction-selective units in rabbit retina: distribution of preferred directions.Science 155, 841–842.

    Google Scholar 

  • Pongracz, F., S. Firestein and G. M. Shepherd. 1991. Electronic structure of olfactory sensory neurons analyzed by intracellular and whole cell patch techniques.J. Neurophysiol. 65, 747–758.

    Google Scholar 

  • Poznanski, R. R. 1988. Membrane voltage changes in passive dendritic trees: a tapering equivalent cylinder model.IMA J. Math. appl. Med. Biol. 5, 113–145.

    MATH  MathSciNet  Google Scholar 

  • Poznanski, R. R. 1990. Analysis of a postsynaptic scheme based on a tapering equivalent cable model.IMA J. Math. appl. Med. Biol. 7, 175–197.

    MATH  MathSciNet  Google Scholar 

  • Poznanski, R. R. 1991. A generalized tapering equivalent cable model for dendritic neurons.Bull. math. Biol. 53, 457–467.

    Article  MATH  Google Scholar 

  • Rall, W. 1959. Branching dendritic trees and motoneuron membrane resistivity.Exp. Neurol. 1, 491–527.

    Article  Google Scholar 

  • Rall, W. 1962. Theory of physiological properties of dendrites.Ann. N.Y. Acad. Sci. 96, 1071–1092.

    Google Scholar 

  • Rall, W. 1982. Theoretical models which increaseR m with dendritic distance help fit lower value ofC m.Soc. Neurosci. Abstr. 8, 414.

    Google Scholar 

  • Rall, W. 1990. Perspectives on neuron modeling. InThe Segmental Motor System, M. D. Binder and L.M. Mendell (Eds), pp. 129–149. Oxford: Oxford University Press.

    Google Scholar 

  • Rall, W. and J. Rinzel. 1973. Branch input resistance and steady attenuation for input to one branch of a dendritic neuron model.Biophys. J. 13, 648–688.

    Google Scholar 

  • Redman, S. J. 1973. The attenuation of passively propagating dendritic potentials in a motoneurone cable model.J. Physiol. (Lond.) 234, 637–664.

    Google Scholar 

  • Redman, S. J., E. M. McLachlan and G. D. S. Hirst. 1987. Nonuniform passive membrane properties of rat lumbar sympathetic ganglion cells.J. Neurophysiol. 57, 633–644.

    Google Scholar 

  • Rinzel, J. and W. Rall. 1974. Transient response in a dendritic neuron model for current injected at one branch.Biophys. J. 14, 759–790.

    Article  Google Scholar 

  • Tauchi, M. and R. H. Masland. 1984. The shape and arrangement of the cholinergic neurons in the rabbit retina.Proc. R. Soc. (Lond.) B 223, 101–119.

    Article  Google Scholar 

  • Torre, V. and T. Poggio. 1978. A synaptic mechanism possibly underlying directional selectivity to motion.Proc. R. Soc. (Lond.) B 202, 409–416.

    Google Scholar 

  • Tsien, R. Y. 1989. Fluorescent probs of cell signalling.Ann. Rev. Neurosci. 12, 227–253.

    Article  Google Scholar 

  • Vaney, D. I. 1984. ‘Coronate’ amacrine cells in the rabbit retina have the ‘starburst’ dendritic morphology.Proc. R. Soc. (Lond.) B 220, 501–508.

    Google Scholar 

  • Vaney, D. I. 1985. Fireworks in the retina.Nature 314, 672–673.

    Article  Google Scholar 

  • Vaney, D.I. 1990. The mosaic of amacrine cells in the mammalian retina. InProgress in Retinal Research, Vol. 9, N. Osborne and J. Chader (Eds), pp. 49–100. Oxford: Pergamon Press.

    Google Scholar 

  • Vaney, D. I. and H. M. Young. 1988. GABA like immunoreactivity in cholinergic amacrine cells of the rabbit retina.Brain Res. 438, 369–373.

    Article  Google Scholar 

  • Vaney, D. I., S. P. Collins and H. M. Young. 1989. Dendritic relationships between cholinergic amacrine cells and direction selective retinal ganglion cells. InNeurobiology of the Inner Retina, NATO ASI Series, Vol. H31, R. Weiler and N. N. Osborne (Eds), pp.157–168. Berlin: Springer-Verlag.

    Google Scholar 

  • Wassle, H. and B. B. Boycott. 1991. Functional architecture of the mammalian retina.Physiol. Rev. 71, 447–479.

    Google Scholar 

  • Wyatt, H. J. and N. W. Daw. 1975. Directionally sensitive ganglion cells in the rabbit retina: specificity for stimulus direction, size, and speed.J. Neurophysiol. 38, 613–626.

    Google Scholar 

  • Wyatt, H. J. and N. W. Daw. 1976. Specific effects of neurotransmitter antagonists on ganglion cells in rabbit retina.Science 191, 204–205.

    Google Scholar 

Download references

Author information

Author notes

  1. Roman R. Poznanski

    Present address: Neurobiology Research Centre and School of Mathematics, Carslaw Building F07, The University of Sydney, 2006, NSW, Australia

Authors and Affiliations

  1. Centre for Visual Sciences, Research School of Biological Sciences, Australia National University, 2601, Canberra, ACT, Australia

    Roman R. Poznanski

Authors
  1. Roman R. Poznanski
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Poznanski, R.R. Modelling the electrotonic structure of starburst amacrine cells in the rabbit retina: A functional interpretation of dendritic morphology. Bltn Mathcal Biology 54, 905–928 (1992). https://doi.org/10.1007/BF02460658

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02460658

Keywords

Search

Navigation