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Possible dual effect of synapses that are putatively purely excitatory or purely inhibitory: bases in stability theory and implications for neural network behavior

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Abstract

Depolarization of an excitable membrane has a dual effect; excitatory in that it causes rapid opening of calcium and/or sodium channels but inhibitory in that it also causes those channels to inactivate. We considered whether apparently paradoxical or dual behavior might be exhibited by excitatory and inhibitory synaptic inputs. We used the classic Hodgkin-Huxley model for voltage-gated channels plus leakage channels of appropriate selectivity for ligand-gated postsynaptic channels. We summarize a model cell's behavior by calculating elicited firing frequency as a function of reversal potential and conductance of summed synaptic inputs, using stability theory and direct simulations. Dual behavior is elicited in the model with reasonable densities of ligand-gated channels. Thus a particular synaptic input to a neuron may be either excitatory or inhibitory depending on simultaneous activity of other synaptic inputs to the cell. This input-output map may give rise to biologically realistic and rich behaviors as an element of computed neural networks, and still be computationally tractable.

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References

  • Agin D (1964) Hodgkin-Huxley equations: logarithmic relation between membrane current and frequency of repetitive activity. Nature 201:625–626.

    Google Scholar 

  • Bromm B, Frankenhauser B (1972) Repetitive discharge of the excitable membrane computed on the basis of voltage clamp data for the node of Ranvier. Pflügers Arch Ges Physiol 332:21–27.

    Google Scholar 

  • Catterall WA (1988) Structure and function of voltage-sensitive ion channels. Science 242:50–61.

    Google Scholar 

  • Chandler WK, Fitzhugh R, Cole KS (1962) Theoretical stability properties of a space-clamped axon. Biophys J 42:105–127.

    Google Scholar 

  • Chapman RA (1966) The repetitive responses of isolated axons from the crab, Carcinus maenus. J Exp Biol 45:475–488.

    Google Scholar 

  • Connor JA, Stevens CF (1971) Prediction of repetitive firing behavior from voltage clamp data on an isolated neurone soma. J Physiol 213:31–53.

    Google Scholar 

  • Cooley J, Dodge F, Cohen H (1965) Digital computer solutions for excitable membrane models. J Cell Comp Physiol 66:99–109.

    Google Scholar 

  • Creutzfeldt OD, Lux HD, Nacimento AC. (1964) Intracellulare Reizung Croticaler Nervanzellen. Pflügers Arch 281:129–151.

    Google Scholar 

  • Crick F (1989) The recent excitement about neural networks. Nature 337:129–132.

    Google Scholar 

  • Davenport RW, Jakobsson E, Gerber B (1989) Possible dual effect of synapses that are putatively purely excitatory or purely inhibitory: bases in stability theory and implications for neural network behavior. Soc Neurosci (abstr) 15:1308.

    Google Scholar 

  • Eyzaguirre C, Kuffler SW (1955) Processes of excitation in the dendrites and in the soma of single isolated sensory nerve cells of the lobster and crayfish. J Gen Physiol 39:87–119.

    Google Scholar 

  • Fitzhugh R (1961) Impulses and physiological states in theoretical models of nerve membrane. Biophys J 1:445–466.

    Google Scholar 

  • Granit R, Phillips GC (1956) Excitatory and inhibitory processes acting upon individual Purkinje cells of the cerebellum in cats. J Physiol 133:520–547.

    Google Scholar 

  • Granit R, Kernell D, Smith RS (1963) Delayed depolarization and the repetitive response to intracellular stimulation of mammalian motoneurones. J Physiol 168:890–910.

    Google Scholar 

  • Hille B (1984) Ionic channels of excitable membranes. Sinauer, Sunderland, Mass.

    Google Scholar 

  • Hodgkin AL, Huxley AF (1952a) The dual effect of membrane potential on sodium conductance in the giant axon of Loligo. J Physiol 116:497–506.

    Google Scholar 

  • Hodgkin AL, Huxley AF (1952b) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117:500–544.

    Google Scholar 

  • Hopfield J, Tank D (1986) Computing with neural circuits: a model. Science 233:625–633.

    Google Scholar 

  • Jack JJB, Noble D, Tsien RWY (1975) Repetitive activity in excitable cells. In: Electric current flow in excitable cells. Clarendon Press, Oxford University Press, London pp 305–378.

    Google Scholar 

  • Jakobsson E, Guttmann R (1980) The standard Hodgkin-Huxley model and squid axons in reduced external Ca++ fail to accommodate to slowly rising currents. Biophys J 31:293–298.

    Google Scholar 

  • Jakobsson E, Guttmann R (1981) Continuous stimulation and threshold of axons: The other legacy of Kenneth Cole. In: Adelman WJ Jr, Goldman DE (eds) The biophysical approach to excitable stystems. Plenum Press, New York, pp 197–211.

    Google Scholar 

  • Jordan PC (1987) Microscopic approaches to ion transport through transmembrane channels. The model system gramicidin. J Phys Chem 91:6581–6591.

    Google Scholar 

  • Kandel ER, Spencer WA (1961) Electrophysiology of hippocampal neurons. II. Afterpotentials and repetitive firing. J Neurophysiol 24:243–259.

    Google Scholar 

  • Nakajima S, Onodera K (1969) Membrane properties of the stretch receptor neurones of crayfish with particular reference to mechanisms of sensory adaptation. J Physiol 200:161–185.

    Google Scholar 

  • Perkel DH (1964) A digital-computer model of nerve functioning. Memorandum RM-4132-NIH. The Rand Corporation, Santa Monica, CA.

    Google Scholar 

  • Perkel DH, Schulman JH, Bullock TH, Moore GP, Segundo JP (1964) Pacemaker neurons: effects of regularly spaced synaptic input. Science 145:61–63.

    Google Scholar 

  • Rattay F (1986) High frequency electrostimulation of excitable cells. J Theor Biol 123:45–54.

    Google Scholar 

  • Rinzel J (1978) On repetitive activity in nerve. Fed Proc 37:2793–2802.

    Google Scholar 

  • Rinzel J, Baer SM (1988) Threshold for repetitive activity for a slow stimulus ramp: A memory effect and its dependence on fluctuation. Biophys J 54:551–555.

    Google Scholar 

  • Rogawski MA (1985) The A-current: how ubiquitous a feature of excitable cells is it? Trends Neurosci May:214–219.

    Google Scholar 

  • Rumelhart DE, Hinton GE, McClelland JL (1986) A general framework for parallel distributed processing. In: Parallel distributed processing, explorations in the microstructure of cognition, Vol 1: Foundations. Bradford/MIT Press, Cambridge, Mass, pp 45–77.

    Google Scholar 

  • Shapiro BI, Lenherr FK (1972) Hodgkin-Huxley axon. Increased modulation and linearity of response to constant current stimulus. Biophys J 12:1145–1158.

    Google Scholar 

  • Stein RB (1967) The frequency of nerve action potentials generated by applied currents. Proc R Soc London Ser B 167:64–86.

    Google Scholar 

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Davenport, R., Jakobsson, E. & Gerber, B. Possible dual effect of synapses that are putatively purely excitatory or purely inhibitory: bases in stability theory and implications for neural network behavior. Biol. Cybern. 65, 47–53 (1991). https://doi.org/10.1007/BF00197289

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  • DOI: https://doi.org/10.1007/BF00197289

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