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Modeling the leech heartbeat elemental oscillator I. Interactions of intrinsic and synaptic currents

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Abstract

We have developed a biophysical model of a pair of reciprocally inhibitory interneurons comprising an elemental heartbeat oscillator of the leech. We incorporate various intrinsic and synaptic ionic currents based on voltage-clamp data. Synaptic transmission between the interneurons consists of both a graded and a spike-mediated component. By using maximal conductances as parameters, we have constructed a canonical model whose activity appears close to the real neurons. Oscillations in the model arise from interactions between synaptic and intrinsic currents. The inhibitory synaptic currents hyperpolarize the cell, resulting in activation of a hyperpolarization-activated inward currentI h and the removal of inactivation from regenerative inward currents. These inward currents depolarize the cell to produce spiking and inhibit the opposite cell. Spike-mediated IPSPs in the inhibited neuron cause inactivation of low-threshold Ca++ currents that are responsible for generating the graded synaptic inhibition in the opposite cell. Thus, although the model cells can potentially generate large graded IPSPs, synaptic inhibition during canonical oscillations is dominated by the spike-mediated component.

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References

  • Angstadt JD, Calabrese RL (1989) A hyperpolarization-activated inward current in heart interneurons of the medicinal leech.J. Neurosci. 9:2846–2857.

    Google Scholar 

  • Angstadt JD, Calabrese RL (1991) Calcium currents and graded synaptic transmission between heart interneurons of the leech.J. Neurosci. 11:746–759.

    Google Scholar 

  • Arbas EA, Calabrese RL (1987) Slow oscillations of membrane potential in interneurons that control heartbeat in the medicinal leech.J. Neurosci. 7:3953–3960.

    Google Scholar 

  • Arshavsky YI, Orlovsky GN, Panchin YV, Roberts A, Soffe SR (1993) Neuronal control of swimming locomotion: Analysis of the pteropod molluscClione and embryos of the amphibian.Xenopus, TINS 16:227.

    Google Scholar 

  • Beeler GW, Reuter H (1977) Reconstruction of the action potential of ventricular myocardial fibers.J. Physiol. London 268:177–210.

    Google Scholar 

  • Calabrese RL, Angstadt JD, Arbas EA (1989) A neural oscillator based on reciprocal inhibition, In: TJ Carew, D Kelley, eds. Perspectives in Neural Systems and Behavior, Alan R. Liss, New York. pp. 33–50.

    Google Scholar 

  • Calabrese RL, De Schutter E (1992) Motor-pattern-generating networks in invertebrates: Modeling our way toward understanding:TINS 15:439–445.

    Google Scholar 

  • Calabrese RL, Peterson EL (1983) Neural control of heartbeat in the leech, Hirudo medicinalis. In: A Roberts, B Roberts, eds. Neural Origin of Rhythmic MovementsSymp. Soc. Exp. Biol. 37:195–221.

  • Connor JA, Stevens CF (1971) Inward and delayed outward membrane currents in isolated neural somata under voltage clamp.J. Physiol. London 213:1–19.

    Google Scholar 

  • De Schutter E (1986) Alternative equations for the molluscan ion currents described by Connor and Stevens.Brain Res. 382:134–138.

    Google Scholar 

  • De Schutter E, Angstadt JD, Calabrese RL (1993) A model of graded synaptic transmission for use in dynamic network simulations.J. Neurophysiol. 69:1225–1235.

    Google Scholar 

  • Friesen WO (1989) Neuronal control of leech swimming movements. In: JW Jacklet, ed. Neuronal and Cellular Oscillators, Marcel Dekker, Inc, New York and Basel.

    Google Scholar 

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

    Google Scholar 

  • Olsen ØH (1994) Exploring temporal computation in neuronal systems, University of Glasgow, PhD thesis, Department of Electronics and Electrical Engineering.

  • Olsen ØH, Nadim F, Calabrese RL (1995) Modeling the leech heartbeat elemental oscillator: II. Exploring the parameter space.J. Comp. Neurosci. 2:237–257.

    Google Scholar 

  • Opdyke CA, Calabrese RL (1994) A persistent sodium current contributes to oscillatory activity in heart interneurons of the medicinal leech.J. Comp. Physiol. A 175:781–789.

    Google Scholar 

  • Peterson EL (1983) Generation and coordination of heartbeat timing oscillation in the medicinal leech: II. Intersegmental coordinationJ. Neurophysiol. 49:626–638.

    Google Scholar 

  • Peterson EL (1983) Generation and coordination of heartbeat timing oscillation in the medicinal leech: I. Oscillation in isolated ganglia.J. Neurophysiol. 49:611–626.

    Google Scholar 

  • Satterlie RA (1985) Reciprocal inhibition and postinhibitory rebound produces reverbation in a locomotor pattern generator,Science 229:402–404.

    Google Scholar 

  • Schmidt J, Calabrese RL (1992) Evidence that acetylcholine is an inhibitory transmitter of heart interneurons in the leech.J. Exp. Biol. 171:329–347.

    Google Scholar 

  • Selverston AI, Moulins M (1985) Oscillatory neural networks.Ann. Rev. Physiol. 47:29–48.

    Google Scholar 

  • Simon TW, Opdyke CA, Calabrese RL (1992) Modulatory effects of FMRF-NH2 on outward currents and oscillatory activity in heart interneurons of the medicinal leech.J. Neurosci. 12:525–537.

    Google Scholar 

  • Simon TW, Schmidt J, Calabrese RL (1994) Modulation of high-threshold transmission between heart interneurons of the medicinal leech by FMRF-NH2.J. Neurophysiol. 71:454–466.

    Google Scholar 

  • Wang X-J, Rinzel J (1992) Alternating and synchronous rhythms in reciprocally inhibitory model neurons.Neural Comp. 4:84–97.

    Google Scholar 

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Nadim, F., Olsen, Ø.H., de Schutter, E. et al. Modeling the leech heartbeat elemental oscillator I. Interactions of intrinsic and synaptic currents. J Comput Neurosci 2, 215–235 (1995). https://doi.org/10.1007/BF00961435

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  • DOI: https://doi.org/10.1007/BF00961435

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