Journal of Computational Neuroscience

, Volume 8, Issue 1, pp 5–18 | Cite as

Simulation Studies of Vestibular Macular Afferent-Discharge Patterns Using a New, Quasi-3-D Finite Volume Method

  • Muriel D. Ross
  • Samuel W. Linton
  • Bruce R. Parnas


A quasi-three-dimensional finite-volume numerical simulator was developed to study passive voltage spread in vestibular macular afferents. The method, borrowed from computational fluid dynamics, discretizes events transpiring in small volumes over time. The afferent simulated had three calyces with processes. The number of processes and synapses, and direction and timing of synapse activation, were varied. Simultaneous synapse activation resulted in shortest latency, while directional activation (proximal to distal and distal to proximal) yielded most regular discharges. Color-coded visualizations showed that the simulator discretized events and demonstrated that discharge produced a distal spread of voltage from the spike initiator into the ending. The simulations indicate that directional input, morphology, and timing of synapse activation can affect discharge properties, as must also distal spread of voltage from the spike initiator. The finite volume method has generality and can be applied to more complex neurons to explore discrete synaptic effects in four dimensions.

finite volume simulator vestibular maculae calyx backpropagation 


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  1. Ades HW, Engström H (1965) Form and innervation of the vestibular epithelia. In: Graybiel A, ed. The Role of the Vestibular Organs in the Exploration of Space. NASA, Washington, DC. pp. 23-41.Google Scholar
  2. American Veterinary Medical Association (1993) Report of the AVMA Panel on Euthansia. J. Am. Vet. Med. Assoc. 202:229-249.Google Scholar
  3. Baird RA, Desmadryl G, Ferńandez C, Goldberg JM (1988) The vestibular nerve of the chinchilla. II. Relation between afferent response properties and peripheral innervation patterns in the semicircular canals. J. Neurophysiol. 60:182-203.Google Scholar
  4. Vestibular Macular Afferent-Discharge Patterns 17 Bhalla US, Bilitch DH, Bower JM (1992) Rallpacks: A set of benchmarks for neuronal simulators. Trends Neurosci. 15:453-458.Google Scholar
  5. Chimento TC, Doshay DG, Ross MD (1994) Compartmental modeling of rat macular primary afferents from three-dimensional reconstructions of transmission electron micrographs of serial sections. J. Neurophysiol. 71:1883-1896.Google Scholar
  6. Chimento TC, Ross MD (1996) Evidence for a sensory processing unit in the vestibular macula. In: Highstein S, Cohen B, Buttner-Ennever J, eds. New Directions in Vestibular Research. Ann. NY Acad. Sci. New York, NY, 196-212.Google Scholar
  7. Destexhe A, Mainen ZF, Sejnowski TJ (1994) An efficient method for computing synaptic conductances based on a kinetic model of receptor binding. Neural Comput. 6:14-18.Google Scholar
  8. Estes MS, Blanks RHI, Markham CH (1975) Physiologic characteristics of vestibular first-order canal neurons in the cat. I. Response plane determination and resting discharge characteristics. J. Neurophysiol. 38:1232-1249.Google Scholar
  9. Ferńandez C, Baird RA, Goldberg, JM (1988) The vestibular nerve of the chinchilla. I. Peripheral innervation patterns in the horizontal and superior semicircular canals. J. Neurophysiol. 60:167-181.Google Scholar
  10. Ferńandez C, Goldberg JM (1976) Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. I. Response to static tilts and to long-duration centrifugal force. J. Neurophysiol. 39:970-984.Google Scholar
  11. Flock Å (1964) Structure of the Macula utriculi with special reference to directional interplay of sensory responses as revealed by morphological polarization. J. Cell Biol. 22:413-431.Google Scholar
  12. Goldberg JM, Ferńandez C (1971) Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. III. Variations among units in their discharge properties. J. Neurophysiol. 34:676-684.Google Scholar
  13. Goldberg JM, Smith CE, Ferńandez C (1984) Relation between discharge regularity and responses to externally applied galvanic currents in vestibular nerve afferents of the squirrel monkey. J. Neurophysiol. 51:1236-1256.Google Scholar
  14. Hill AV (1936) Excitation and accommodation in nerve. Proc. Roy. Soc. 119:305-355.Google Scholar
  15. Jung HY, Mickus T, Spruston N (1997) Prolonged sodium channel inactivation contributes to dendritic action potential attenuation in hippocampal pyramidal neurons. J. Neurosci. 17:6639-6646.Google Scholar
  16. Lewis ER, Parnas BR (1994) Theoretical bases of short-latency spike volleys in the peripheral vestibular system. J. Vest. Res. 4:189-202.Google Scholar
  17. Linton SW, Ross MD (1995) An object-oriented electrophysiological numerical simulator for parallel computers. High Performance Computing Proc. 239-246.Google Scholar
  18. Lorente de Nó R (1931) Ausgewahlte Kapitel aus der vergleichenden Physiologie des Labyrinthes. Die Augenmuskelreflexe beim Kanincen und ihre Grundlagen. Ergebn Physiol. 32:73-242.Google Scholar
  19. Lysakowski A, Minor LB, Ferńandez C, Goldberg JM (1995) Physiological identification of morphologically distinct afferent classes innervating the cristae ampullares of the squirrel monkey. J. Neurophysiol. 73:1270-1281.Google Scholar
  20. Magee JC, Johnston D (1997) A synaptically controlled, associative signal for hebbian plasticity in hippocampal neurons. Science 275:209-213.Google Scholar
  21. Markram H, Lübke J, Frotscher M, Sakmann B (1997) Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275:213-215.Google Scholar
  22. Mellon D Jr, Kennedy D (1964) Impulse origin and propagation in a bipolar sensory neuron. J. Gen. Physiol. 47:487-499.Google Scholar
  23. Pabst A (1977) Number and location of the sites of impulse generation in the lateral line of Xenopus laevis. J. Comp. Physiol. [A] 114:51-67.Google Scholar
  24. Parnas BR (1994) Analysis of the response properties of a computationally efficient spike initiator model. Biol. Cybern. 71:319-332.Google Scholar
  25. Parnas BR, Lewis ER (1993) A computationally efficient spike initiator model that produces a wide variety of neural responses. In: Eeckman FH, ed. Neural Systems: Analysis and Modeling. Kluwer, Norwell, MA. pp. 67-75.Google Scholar
  26. Rall, W (1967) Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input. J. Neurophysiol. 30:1138-1168.Google Scholar
  27. Rall W, Shepherd GM (1968) Theoretical reconstruction of field potentials and dendrodendritic synaptic interactions in olfactory bulb. J. Neurophysiol. 31:884-915.Google Scholar
  28. Ross MD (1985) Anatomic evidence for peripheral neural processing in mammalian graviceptors. Aviation Space Environ. Med. 56:338-343.Google Scholar
  29. Ross MD (1997) Morphological evidence for local microcircuits in vestibular maculae. J. Comp. Neurol. 379:333-346.Google Scholar
  30. Ross MD, Cutler L, Meyer G, Lam T, Vaziri P (1990a) 3-D components of a biological neural network visualized in computer generated imagery. I. Macular receptive field organization. Acta Otolaryngol. (Stockh.) 109:83-92.Google Scholar
  31. Ross MD, Meyer G, Lam T, Cutler L, Vaziri P (1990b) 3-D components of a biological neural network visualized in computer generated imagery. II. Macular neural network organization. Acta Otolaryngol. (Stockh.) 109:235-244.Google Scholar
  32. Ross MD, Cutler L, Chee O, Black S (1991) Ultrastructural and Cytochemical Evidence for single impulse initiation zones in vestibular macular nerve fibers. Ann. Otol. Rhino. Laryngol. 100:398-406.Google Scholar
  33. Ross MD, Chimento T, Doshay D, Cheng R (1992) Computerassisted three-dimensional reconstruction and simulations of vestibular macular neural connectivities. In: Highstein S, Cohen B, Buttner-Ennever J, eds. New Directions in Vestibular Research. Ann. NY Acad. Sci. New York, NY, 656:75-91.Google Scholar
  34. Saidel WM (1988) Variations of trigger zones in vestibular afferent fibers of fish. Neurosci. Lett. 84:161-166.Google Scholar
  35. Sakmann B (1992) Elementary steps in synaptic transmission revealed by currents through single ion channels. Science 256:503-512.Google Scholar
  36. Schessel DA (1982) Chemical synaptic transmission between type I vestibular hair cells and the primary afferent nerve chalice: An intracellular study utilizing horseradish peroxidase. Ph.D. dissertation, Albert Einstein College of Medicine, Bronx, NY.Google Scholar
  37. Schmitt FO (1979) The role of structural, electrical and chemical circuitry in brain function. In: Schmitt FO, ed. The Neurosciences: Fourth Study Program. Rockefeller University Press, New York. pp. 5-20.Google Scholar
  38. Schneider LW, Anderson DJ (1976) Transfer characteristics of firstand second-order lateral canal vestibular neurons in gerbil. Brain Res. 112:61-76.Google Scholar
  39. Segev I, Fleshman JW, Burke RE (1990) Computer simulation of group Ia EPSPs using morphological realistic models of cat Æmotoneurons. J. Neurophysiol. 64:648-660.Google Scholar
  40. Shepherd GM (1970) The olfactory bulb as a simple cortical system: Experimental analysis and functional implications. In: Schmitt FO, ed. The Neurosciences: Second Study Program. Rockefeller University Press, New York. pp. 539-552.Google Scholar
  41. Smith CA, Goldberg JM (1986) A stochastic after hyperpolarization model of repetitive activity in vestibular afferents. Biol. Cybern. 54:41-51.Google Scholar
  42. Spoendlin H (1965) Ultrastructural studies of the labyrinth in squirrel monkeys. In: The Role of the Vestibular Organs in the Exploration of Space. NASA, Washington, DC. pp. 7-22.Google Scholar
  43. Spruston N, Schiller Y, Stuart G, Sakmann G (1995) Activitydependent action potential invasion and calcium influx into hippocampal CA1 dendrites. Science 268:297-303.Google Scholar
  44. Strassberg AF, DeFelice LJ (1993) Limitations of the Hodgkin-Huxley formalism: Effects of single channel kinetics on transmembrane voltage. Neur. Comput. 5:843-855.Google Scholar
  45. Stuart GJ, Sakmann B (1994) Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367:69-72.Google Scholar
  46. Tomko DL, Peterka R, Schor RH, O'Leary DP (1981) Response dynamics of horizontal canal afferents in barbiturate-anesthetized cats. J. Neurophysiol. 45:376-396.Google Scholar
  47. Tsubokawa H, Ross WN (1997) Muscarinic modulation of spike backpropagation in the apical dendrites of hippocampal CA1 pyramidal neurons. J. Neurosci. 17:5782-5791.Google Scholar
  48. Usami S, Ottersen OP (1995) Differential cellular distribution of glutamate and glutamine in the rat vestibular endorgans: An immunocytochemical study. Brain Res. 676:285-292.Google Scholar
  49. Walsh BT, Miller JB, Gacek RR, Kiang NYS (1972) Spontaneous activity in the eighth cranial nerve of the cat. Int. J. Neurosci. 3:221-236.Google Scholar
  50. Wersäll J (1956) Studies on the structure and innervation of the sensory epithelium of the cristae ampullares in the guinea pig: A light and electron microscopic investigation. Acta Otolaryngol. Suppl 126:1-85.Google Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Muriel D. Ross
    • 1
  • Samuel W. Linton
    • 2
  • Bruce R. Parnas
    • 2
  1. 1.Ames Center for BioinformaticsNASA Ames Research Center andMoffett Field
  2. 2.Ames Center for BioinformaticsMoffett Field

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