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

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.

[1]  M. Ariel,et al.  Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells , 1982, The Journal of physiology.

[2]  I Segev,et al.  Electrotonic architecture of type-identified alpha-motoneurons in the cat spinal cord. , 1988, Journal of neurophysiology.

[3]  E. V. Famiglietti,et al.  Synaptic organization of starburst amacrine cells in rabbit retina: Analysis of serial thin sections by electron microscopy and graphic reconstruction , 1991, The Journal of comparative neurology.

[4]  T. Millar,et al.  Cholinergic amacrine cells in the rabbit retina synapse onto other cholinergic amacrine cells , 1987, Neuroscience Letters.

[5]  L. Glenn Overestimation of the electrical length of neuron dendrites and synaptic electrotonic attenuation , 1988, Neuroscience Letters.

[6]  E. V. Famiglietti,et al.  ‘Starburst’ amacrine cells and cholinergic neurons: mirror-symmetric ON and OFF amacrine cells of rabbit retina , 1983, Brain Research.

[7]  D. I. Vaney,et al.  Chapter 2 The mosaic of amacrine cells in the mammalian retina , 1990 .

[8]  S. Massey,et al.  The light evoked release of acetylcholine from the rabbit retina iN vivo and its inhibition by γ‐aminobutyric acid , 1979, Journal of neurochemistry.

[9]  H. Barlow,et al.  The mechanism of directionally selective units in rabbit's retina. , 1965, The Journal of physiology.

[10]  Y Yarom,et al.  Voltage behavior along the irregular dendritic structure of morphologically and physiologically characterized vagal motoneurons in the guinea pig. , 1990, Journal of neurophysiology.

[11]  K. Cole Membranes, ions, and impulses : a chapter of classical biophysics , 1968 .

[12]  N. Daw,et al.  Directionally sensitive ganglion cells in the rabbit retina: specificity for stimulus direction, size, and speed. , 1975, Journal of neurophysiology.

[13]  E. V. Famiglietti,et al.  On and off pathways through amacrine cells in mammalian retina: The synaptic connections of “starburst” amacrine cells , 1983, Vision Research.

[14]  S. Massey,et al.  The release of acetylcholine and amino acids from the rabbit retina in vivo , 1980, Neurochemistry International.

[15]  C. W. Oyster,et al.  The analysis of image motion by the rabbit retina , 1968, The Journal of physiology.

[16]  R. Poznanski Analysis of a postsynaptic scheme based on a tapering equivalent cable model. , 1990, IMA journal of mathematics applied in medicine and biology.

[17]  A R Maranto,et al.  Neuronal mapping: a photooxidation reaction makes Lucifer yellow useful for electron microscopy. , 1982, Science.

[18]  H. Barlow,et al.  Selective Sensitivity to Direction of Movement in Ganglion Cells of the Rabbit Retina , 1963, Science.

[19]  William R. Holmes,et al.  Effects of uniform and non-uniform synaptic ‘activation-distributions’ on the cable properties of modeled cortical pyramidal neurons , 1989, Brain Research.

[20]  S. Bloomfield,et al.  Electroanatomy of a unique amacrine cell in the rabbit retina. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[21]  R H Masland,et al.  Responses to acetylcholine of ganglion cells in an isolated mammalian retina. , 1976, Journal of neurophysiology.

[22]  T. Poggio,et al.  A synaptic mechanism possibly underlying directional selectivity to motion , 1978, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[23]  H. Wässle,et al.  Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and gamma-aminobutyrate immunoreactivity. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[24]  J Rinzel,et al.  Transient response in a dendritic neuron model for current injected at one branch. , 1974, Biophysical journal.

[25]  Nonuniform passive membrane properties of rat lumbar sympathetic ganglion cells. , 1987, Journal of neurophysiology.

[26]  S. Massey,et al.  A tonic gamma-aminobutyric acid-mediated inhibition of cholinergic amacrine cells in rabbit retina , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  N. Grzywacz,et al.  A model of the directional selectivity circuit in retina: transformations by neurons singly and in concert , 1992 .

[28]  R H Masland,et al.  The shape and arrangement of the cholinergic neurons in the rabbit retina , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[29]  J Rinzel,et al.  Branch input resistance and steady attenuation for input to one branch of a dendritic neuron model. , 1973, Biophysical journal.

[30]  W Rall,et al.  Changes of action potential shape and velocity for changing core conductor geometry. , 1974, Biophysical journal.

[31]  R. Tsien Fluorescent probes of cell signaling. , 1989, Annual review of neuroscience.

[32]  H. Barlow,et al.  Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit , 1964, The Journal of physiology.

[33]  R. Poznanski Membrane voltage changes in passive dendritic trees: a tapering equivalent cylinder model. , 1988, IMA journal of mathematics applied in medicine and biology.

[34]  Shaun P. Collin,et al.  Dendritic Relationships between Cholinergic Amacrine Cells and Direction-Selective Retinal Ganglion Cells , 1989 .

[35]  S. Redman The attenuation of passively propagating dendritic potentials in a motoneurone cable model , 1973, The Journal of physiology.

[36]  Richard H. Masland,et al.  The cholinergic amacrine cell , 1986, Trends in Neurosciences.

[37]  R R Poznanski,et al.  A generalized tapering equivalent cable model for dendritic neurons. , 1991, Bulletin of mathematical biology.

[38]  J. Dowling The Retina: An Approachable Part of the Brain , 1988 .

[39]  B. Boycott,et al.  Functional architecture of the mammalian retina. , 1991, Physiological reviews.

[40]  H B Barlow,et al.  Direction-Selective Units in Rabbit Retina: Distribution of Preferred Directions , 1967, Science.

[41]  R. Masland,et al.  Co-release of acetylcholine and gamma-aminobutyric acid by a retinal neuron. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[42]  J. Jack,et al.  Electric current flow in excitable cells , 1975 .

[43]  W. Rall Theory of Physiological Properties of Dendrites , 1962, Annals of the New York Academy of Sciences.

[44]  K. N. Leibovic Nervous System Theory: An Introductory Study , 1972 .

[45]  M Hines,et al.  A program for simulation of nerve equations with branching geometries. , 1989, International journal of bio-medical computing.

[46]  H. J. Wyatt,et al.  Specific effects of neurotransmitter antagonists on ganglion cells in rabbit retina. , 1976, Science.

[47]  J. Dowling,et al.  Organization of retina of the mudpuppy, Necturus maculosus. I. Synaptic structure. , 1969, Journal of neurophysiology.

[48]  G M Shepherd,et al.  Electrotonic structure of olfactory sensory neurons analyzed by intracellular and whole cell patch techniques. , 1991, Journal of neurophysiology.

[49]  H. Young,et al.  GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina , 1988, Brain Research.

[50]  J. Dowling,et al.  Synaptic organization of the frog retina: an electron microscopic analysis comparing the retinas of frogs and primates , 1968, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[51]  W. Rall Branching dendritic trees and motoneuron membrane resistivity. , 1959, Experimental neurology.

[52]  J. Caldwell,et al.  Effects of picrotoxin and strychnine on rabbit retinal ganglion cells: lateral interactions for cells with more complex receptive fields. , 1978, The Journal of physiology.

[53]  D. H. Paul The physiology of nerve cells , 1975 .

[54]  Christopher Brandon,et al.  Cholinergic neurons in the rabbit retina: dendritic branching and ultrastructural connectivity , 1987, Brain Research.

[55]  Vision: Fireworks in the retina , 1985, Nature.

[56]  R Nelson,et al.  A comparison of electrical properties of neurons in Necturus retina. , 1973, Journal of neurophysiology.

[57]  J. Dowling,et al.  Organization of vertebrate retinas. , 1970, Investigative ophthalmology.

[58]  R. Miller,et al.  Measurement of passive membrane parameters with whole-cell recording from neurons in the intact amphibian retina. , 1989, Journal of neurophysiology.

[59]  F. Amthor,et al.  Morphology of on-off direction-selective ganglion cells in the rabbit retina , 1984, Brain Research.

[60]  D. I. Vaney,et al.  ‘Coronate’ amacrine cells in the rabbit retina have the ‘starburst’ dendritic morphology , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.