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Simulation of the Aii amacrine cell of mammalian retina: Functional consequences of electrical coupling and regenerative membrane properties

Published online by Cambridge University Press:  02 June 2009

Robert G. Smith  and
Noga Vardi
Robert G. Smith
Affiliation:
Department of Neuroscience, University of Pennsylvania, Philadelphia
Noga Vardi
Affiliation:
Department of Neuroscience, University of Pennsylvania, Philadelphia
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Abstract

The Aii amacrine cell of mammalian retina collects signals from several hundred rods and is hypothesized to transmit quantal “single-photon” signals at scotopic (starlight) intensities. One problem for this theory is that the quantal signal from one rod when summed with noise from neighboring rods would be lost if some mechanism did not exist for removing the noise. Several features of the Aii might together accomplish such a noise removal operation: The Aii is interconnected into a syncytial network by gap junctions, suggesting a noise-averaging function, and a quantal signal from one rod appears in five Aii cells due to anatomical divergence. Furthermore, the Aii contains voltage-gated Na+ and K+ channels and fires slow action potentials in vitro, suggesting that it could selectively amplify quantal photon signals embedded in uncorrelated noise. To test this hypothesis, we simulated a square array of AII somas (Rm = 25,000 Ohm-cm2) interconnected by gap junctions using a compartmental model. Simulated noisy inputs to the Aii produced noise (3.5 mV) uncorrelated between adjacent cells, and a gap junction conductance of 200 pS reduced the noise by a factor of 2.5, consistent with theory. Voltage-gated Na+ and K+ channels (Na+: 4 nS, K+: 0.4 nS) produced slow action potentials similar to those found in vitro in the presence of noise. For a narrow range of Na+ and coupling conductance, quantal photon events (-5–10 mV) were amplified nonlinearly by subthreshold regenerative events in the presence of noise. A lower coupling conductance produced spurious action potentials, and a greater conductance reduced amplification. Since the presence of noise in the weakly coupled circuit readily initiates action potentials that tend to spread throughout the AII network, we speculate that this tendency might be controlled in a negative feedback loop by up-modulating coupling or other synaptic conductances in response to spiking activity.

Keywords

Neural networkSynaptic noiseComputer simulationGap junction
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 5 , September 1995 , pp. 851 - 860
Copyright
Copyright © Cambridge University Press 1995

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References

REFERENCES

Ashmore, J.F. & Falk, G. (1980). The single-photon signal in rod bipolar cells of the dogfish retina. Journal of Physiology (London) 352, 151–166.CrossRefGoogle Scholar
Barlow, H.B., Levick, W.R. & Yoon, M. (1971). Responses to single quanta of light in retinal ganglion cells of the cat. Vision Research (Suppl.) 3, 87–101.CrossRefGoogle Scholar
Baylor, D.A., Nunn, B.J. & Schnapf, J.L. (1984). The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca Fascicularis. Journal of Physiology 375, 575–607.CrossRefGoogle Scholar
Bernander, O., Douglas, R.J., Martin, K.A.C. & Koch, C. (1991). Synaptic background activity influences spatiotemporal integration in single pyramidal cells. Proceedings of the National Academy of Sciences of the U.S.A. 88, 11569–11573.Google Scholar
Boos, R., Schneider, H. & Wässle, H. (1993). Voltage- and transmitter-gated currents of AII-amacrine cells in a slice preparation of the rat retina. Journal of Neuroscience 13, 2874–2888.Google Scholar
Dacheux, R.F. & Raviola, E. (1986). The rod pathway of the rabbitretina: A depolarizing bipolar and amacrine cell. Journal of Neuroscience 6, 331–345.Google Scholar
Faber, D.S., Young, W.S., Legendre, P. & Korn, H. (1992). Intrinsic quantal variability due to stochastic properties of receptor-transmitter interactions. Science 258, 1494–1498.Google Scholar
Famiglietti, E.V. & Kolb, H. (1975). A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Research 84, 293–300.CrossRefGoogle Scholar
Freed, M.A., Smith, R.G. & Sterling, D. (1987). Rod bipolar array in the cat retina: Pattern of input from rods and GABA-accumulating amacrine cells. Journal of Comparative Neurology 266, 445–455.Google Scholar
Hodgkin, A.L. & Huxley, A.F. (1952). A quantitative description of membrane current and its application to conduction and excitation in nerve. Journal of Physiology 117, 500–544.CrossRefGoogle ScholarPubMed
Kolb, H. & Famiglietti, E.V. (1974). Rod and cone bipolar connections in the inner plexiform layer of the cat retina. Science 186, 47–49.Google Scholar
Lamb, T.D. & Simon, E.J. (1976). The relation between intercellular coupling and electrical noise in turtle photoreceptors. Journal of Physiology 263, 257–286.Google Scholar
Makous, W. (1990). Absolute sensitivity. In Scotopic Vision, ed. Hess, R.F., Sharpe, L.T. III & Nordby, K., pp. 146–175. New York: Cambridge University Press.Google Scholar
Mastronarde, D.N. (1983). Correlated firing of cat retinal ganglion cells. II. Responses of X- and Y-cells to single quantal events. Journal of Neurophysiology 49, 325–349.Google Scholar
Nelson, R. (1982). Aii amacrine cells quicken the time course of rod signals in the cat retina. Journal of Neurophysiology 47, 928–947.CrossRefGoogle ScholarPubMed
Robson, J.L., Frishman, L.J., Du, L., Harwerth, R.S. & Smith, E.L. III (1994). Positive and negative components of the scotopic ERG in the macaque monkey. Investigative Ophthalmology and Visual Science 35, 2049.Google Scholar
Sakitt, B. (1972). Counting every quantum. Journal of Physiology 223, 131–150.Google Scholar
Sakmann, B. & Creutzfeldt, O.D. (1969). Scotopic and mesopic light adaptation in the cat's retina. Pflugers Archiv 313, 168–185.Google Scholar
Schnapf, J.L., Schneeweis, D.M. & Kraft, T.W. (1994). Phototransduction in primate photoreceptors. Investigative Ophthalmology and Visual Science 35, 2001.Google Scholar
Smith, R.G., Freed, M.A. & Sterling, P. (1986). Microcircuitry of the dark-adapted cat retina: functional architecture of the rod-cone network. Journal of Neuroscience 6, 3505–3517.Google Scholar
Smith, R.G. (1992). NeuronC: a computational language for investigating functional architecture of neural circuits. Journal of Neuroscience Methods 43, 83–108.CrossRefGoogle ScholarPubMed
Sterling, P., Freed, M.A. & Smith, R.G. (1988). Architecture of rod and cone circuits to the On-beta ganglion cell. Journal of Neuroscience 8, 623–642.CrossRefGoogle Scholar
Tessier-Lavigne, M. & Attwell, D. (1988). The effect of photoreceptor coupling and synapse nonlinearity on signal:noise ratio in early visual processing. Proceedings of the Royal Society B (London) 234, 171–197.Google ScholarPubMed
Vaney, D.I. (1985). The morphology and topographic distribution of Aii amacrine cells in the cat retina. Proceedings of the Royal Society B (London) 224, 475–488.Google ScholarPubMed
Vaney, D.I. (1991). Many diverse types of retinal neurons show tracer coupling when injected with biocytin or neurobiotin. Neuroscience Letters 125, 187–190.Google Scholar
Vaney, D.I., Gynther, I.C. & Young, H.M. (1991). Rod-signal interneurons in the rabbit retina: 2. Aii amacrine cells. Journal of Comparative Neurology 310, 154–169.CrossRefGoogle ScholarPubMed
Vardi, N. & Sterling, P. (1989). Gap junctions between Aii amacrine somas. Society for Neuroscience Abstracts 15, 968.Google Scholar