Skip to main content
Log in

The distribution of the intervals between neural impulses in the maintained discharges of retinal ganglion cells

  • Published:
Biological Cybernetics Aims and scope Submit manuscript

Abstract

Simulated neural impulse trains were generated by a digital realization of the integrate-and-fire model. The variability in these impulse trains had as its origin a random noise of specified distribution. Three different distributions were used: the normal (Gaussian) distribution (no skew, normokurtic), a first-order gamma distribution (positive skew, leptokurtic), and a uniform distribution (no skew, platykurtic). Despite these differences in the distribution of the variability, the distributions of the intervals between impulses were nearly indistinguishable. These inter-impulse distributions were better fit with a hyperbolic gamma distribution than a hyperbolic normal distribution, although one might expect a better approximation for normally distributed inverse intervals. Consideration of why the inter-impulse distribution is independent of the distribution of the causative noise suggests two putative interval distributions that do not depend on the assumed noise distribution: the log normal distribution, which is predicated on the assumption that long intervals occur with the joint probability of small input values, and the random walk equation, which is the diffusion equation applied to a random walk model of the impulse generating process. Either of these equations provides a more satisfactory fit to the simulated impulse trains than the hyperbolic normal or hyperbolic gamma distributions. These equations also provide better fits to impulse trains derived from the maintained discharges of ganglion cells in the retinae of cats or goldfish. It is noted that both equations are free from the constraint that the coefficient of variation (CV) have a maximum of unity. The concluding discussion argues against the random walk equation because it embodies a constraint that is not valid, and because it implies specific parameters that may be spurious.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Berger D, Pribram K, Wild H, Bridges C (1990) An analysis of neural spike-train distributions: determinants of the response of visual cortex neurons to changes in orientation and spatial frequency. Exp Brain Res 80:129–134

    Google Scholar 

  • Cleland BG, Lee BB (1985) A comparison of visual responses of cat lateral geniculate nucleus neurones with those of ganglion cells afferent to them. J Physiol (Lond) 369:249–268

    Google Scholar 

  • Frishman LJ, Levine MW (1983) Statistics of the maintained discharge of cat retinal ganglion cells. J Physiol (Lond) 339:475–494

    Google Scholar 

  • Gerstein GL, Mandelbrot B (1964) Random walk models for the spike activity of a single neuron. Biophys J 4:41–68

    Google Scholar 

  • Gestri G, Mastebroek HAK, Zaagman WH (1980) Stochastic constancy variability and adaptation of spike generation: performance of a giant neuron in the visual system of the fly. Biol Cybern 38:31–40

    Google Scholar 

  • Goldberg JM, Smith CE, Fernández C (1984) Relation between discharge regularity and response to externally applied galvanic currents in vestibular nerve afferents in the squirrel monkey. J Neurophysiol 51:1236–1256

    Google Scholar 

  • Hanson FB, Tuckwell HC (1983) Diffusion approximations for neuronal activity including synaptic reversal potentials. J Theor Neurobiol 2:127–153

    Google Scholar 

  • Johannesma PIM (1968) Diffusion models for the stochastic activity of neurons. In: Caianiello ER (ed) Neural networks. Springer, Berlin Heidelberg New York, pp 116–144

    Google Scholar 

  • Knight BW (1972) Dynamics of encoding in a population of neurons. J Gen Physiol 59:734–766

    Google Scholar 

  • Kuffler SW, FitzHugh R, Barlow HB (1957) Maintained activity in the cat's retina in light and darkness. J Gen Physiol 40:683–702

    Google Scholar 

  • Levine MW (1982) Retinal processing of intrinsic and extrinsic noise. J Neurophysiol 48:992–1010

    Google Scholar 

  • Levine MW (1987) Variability in the maintained discharges of retinal ganglion cells. JOSA A 4:2308–2320

    Google Scholar 

  • Levine MW, Shefner JM (1977a) The effects of photic stimulation upon the variability of the interspike intervals in goldfish ganglion cells. Vision Res 17:793–797

    Google Scholar 

  • Levine MW, Shefner JM (1977b) A model for the variability of interspike intervals during sustained firing of a retinal neuron. Biophys J 19:241–252

    Google Scholar 

  • Levine MW, Saleh EJ, Yarnold P (1988) Statistical properties of the maintained discharge of chemically isolated ganglion cells in goldfish retina. Vis Neurosci 1:31–46

    Google Scholar 

  • Montroll EW, Shlesinger MF (1982) On 1/f noise and other distributions with long tails. PNAS 79:3380–3383

    Google Scholar 

  • Pernier J (1972) Ajustement automatique des densités de probabilité d'intervalles entre potentiels d'action selon la loi de Wiener. Biometrics 28:737–745

    Google Scholar 

  • Pernier J, Gerin P (1975) Temporal pattern analysis of spontaneous unit activity in the neocortex. Biol Cybern 18:123–136

    Google Scholar 

  • Rodieck RW (1967) Maintained activity of cat retinal ganglion cells. J Neurophysiol 30:1043–1071

    Google Scholar 

  • Schwartz M, Shaw L (1975) Signal processing. McGraw-Hill, New York, pp 104–109

    Google Scholar 

  • Shefner JM and Levine MW (1979) A comparison of properties of goldfish retinal ganglion cells as a function of lighting conditions during dissection. Vision Res 19:83–89

    Google Scholar 

  • Smith CE (1979) A comment on a retinal neuron model. Biophys J 25:385–386

    Google Scholar 

  • Stein RB (1965) A theoretical analysis of neuronal variability. Biophys J 5:173–194

    Google Scholar 

  • Ten Hoopen M (1966) Probabilistic firing of neurons considered as a first passage problem. Biophys J 6:435–451

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Levine, M.W. The distribution of the intervals between neural impulses in the maintained discharges of retinal ganglion cells. Biol. Cybern. 65, 459–467 (1991). https://doi.org/10.1007/BF00204659

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00204659

Keywords

Navigation