Skip to main content
Log in

A Model of a Segmental Oscillator in the Leech Heartbeat Neuronal Network

  • Published:
Journal of Computational Neuroscience Aims and scope Submit manuscript

Abstract

We modeled a segmental oscillator of the timing network that paces the heartbeat of the leech. This model represents a network of six heart interneurons that comprise the basic rhythm-generating network within a single ganglion. This model builds on a previous two cell model (Nadim et al., 1995) by incorporating modifications of intrinsic and synaptic currents based on the results of a realistic waveform voltage-clamp study (Olsen and Calabrese, 1996). Due to these modifications, the new model behaves more similarly to the biological system than the previous model. For example, the slow-wave oscillation of membrane potential that underlies bursting is similar in form and amplitude to that of the biological system. Furthermore, the new model with its expanded architecture demonstrates how coordinating interneurons contribute to the oscillations within a single ganglion, in addition to their role of intersegmental coordination.

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.

Institutional subscriptions

Similar content being viewed by others

References

  • Abbott L, Marder E (1998) Modeling small networks. In: Koch C, Segev I, eds. Methods in Neuronal Modeling: From Ions to Networks (2nd ed.). MIT Press, Cambridge, MA, pp. 361-410.

    Google Scholar 

  • 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 (1984) Rate modification in the heartbeat central pattern generator of the medicinal leech. J. Comp. Physiol. A 155:783-794.

    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 

  • Booth V, Rinzel J, Kiehn O (1997) Compartmental model of vertebrate motoneurons for Ca2+-dependent spiking and plateau potentials under pharmacological treatment. J. Neurophysiol. 78:3371-3385.

    Google Scholar 

  • Boroffka I, Hamp R (1969) Topographie des Kreislaufsystems und Zirkulation bei Hirudo medicinalis. Zeitschrift fur Morphologie der Tiere 64:59-76.

    Google Scholar 

  • Bower JM, Beeman D (1998) The Book of GENESIS: Exploring Realistic Neural Models with the GEneral Neural SImulation System (2nd ed.). Springer-Verlag, New York.

    Google Scholar 

  • Brodfuehrer PD, Debski EA, O'Gara BA, Friesen WO (1995) Neuronal control of leech swimming. J. Neurobiol. 27:403-418.

    Google Scholar 

  • Calabrese RL (1980) Control of multiple impulse-initiation sites in a leech interneuron. J. Neurophysiol. 44:878-896.

    Google Scholar 

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

    Google Scholar 

  • Cohen AH, Ermentrout GB, Kiemel T, Kopell N, Sigvardt KA, Williams TL (1992) Modelling of intersegmental coordination in the lamprey central pattern generator for locomotion. Trends Neurosci. 15:434-438.

    Google Scholar 

  • Cymbalyuk GS, Calabrese RL (2000) Oscillatory behaviors in pharmacologically isolated heart interneurons from the medicinal leech. Neurocomputing 32-33:97-104.

    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, Pearce RA (1993) Mechanisms of intersegmental coordination in leech locomotion. Semin. Neurosci. 5:41-47.

    Google Scholar 

  • Grillner S (1999) Bridging the gap-from ion channels to networks and behavior. Curr. Opin. Neurobiol. 9:663-669.

    Google Scholar 

  • Grillner S, Wallén P (1980) Does the central pattern generation for locomotion in lamprey depend on glycine inhibition? Acta Physiol. Scand. 110:103-105.

    Google Scholar 

  • Grillner S, Wallén P, Brodin L, Lansner A (1991) Neuronal network generating locomotor behavior in lamprey: Circuitry, transmitters, membrane properties and simulation. Ann. Rev. Neurosci. 14:169-199.

    Google Scholar 

  • Hille (1992) Ionic channels of excitable membranes. Sinauer Associates, Sunderland, MA.

    Google Scholar 

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

    Google Scholar 

  • Ikeda K, Wiersma CAG (1964) Autogenic rhythmicity in the abdominal ganglia of the crayfish: The control of swimmeret movements. Comp. Biochem. Physiol. 12:107-115.

    Google Scholar 

  • Ivanov AI, Calabrese RL (1999) Correlation of presynaptic intracelluar Ca2+ concentration with homosynaptic plasticity between leech inhibitory heart interneurons. Soc. Neurosci. Abs. 25:658.1.

    Google Scholar 

  • Kopell N, Ermentrout GB (1988) Coupled oscillators and the design of central pattern generators. Math. Biosci. 90:87-109.

    Google Scholar 

  • Krahl B, Zerbst-Boroffka I (1983) Blood pressure in the leech, Hirudo medicinalis. J. Exp. Biol. 107:163-168.

    Google Scholar 

  • Lu J, Dalton JF, Stokes DR, Calabrese RL (1997) Functional role of Ca2+ currents in graded and spike-mediated synaptic transmission between leech heart interneurons. J. Neurophysiol. 77:1779-1794.

    Google Scholar 

  • Maranto AR (1982) Neuronal mapping: A photoxidation reaction makes Lucifer yellow useful for electron microscopy. Science 217:953-955.

    Google Scholar 

  • Marder E, Calabrese RL (1996) Principles of rhythmic motor pattern generation. Physiol. Rev. 76:687-717.

    Google Scholar 

  • Masino MA, Calabrese RL (1999) Differences in inherent cycle periods between coupled segmental oscillators can produce phase differences in the leech heartbeat central pattern generator. Soc. Neurosci. Abst. 25:659.13.

    Google Scholar 

  • Mulloney B, Skinner FK, Namba H, Hall WM (1998) Intersegmental coordination of swimmeret movements: Mathematical models and neural circuits. Ann. N.Y. Acad. Sci. 860:266-280.

    Google Scholar 

  • Murchison D, Chrachri A, Mulloney B (1993) A separate local pattern-generating circuit controls the movements of each swimmeret in crayfish. J. Neurophysiol. 70:2620-2631.

    Google Scholar 

  • Nadim F, Calabrese RL (1997) A slow outward current activated by FMRFamide in heart interneurons of the medicinal leech. J. Neurosci. 17:4461-4472.

    Google Scholar 

  • Nadim F, Olsen OH, De Schutter E, Calabrese RL (1995) Modeling the leech heartbeat elemental oscillator: I. Interactions of intrinsic and synaptic currents. J. Comput. Neurosci. 2:215-235.

    Google Scholar 

  • Namba H, Mulloney B (1999) Coordination of limb movements: Three types of intersegmental interneurons in the swimmeret system and their responses to changes in excitation. J. Neurophysiol. 81:2437-2450.

    Google Scholar 

  • Nicholls JG, Baylor DA (1968) Specific modalities and receptive fields of sensory neurons in the CNS of the leech. J. Physiol. (Lond.) 31:740-756.

    Google Scholar 

  • Nicholls JG, Wallace BG (1978a) Modulation of transmission at an inhibitory synapse in the central nervous system of the leech. J. Physiol. (Lond.) 281:157-170.

    Google Scholar 

  • Nicholls JG, Wallace BG (1978b) Quantal analysis of transmitter release at an inhibitory synapse in the central nervous system of the leech. J. Physiol. (Lond.) 281:171-185.

    Google Scholar 

  • Olsen OH, Calabrese RL (1996) Activation of intrinsic and synaptic currents in leech heart interneurons by realistic waveforms. J. Neurosci. 16:4958-4970.

    Google Scholar 

  • Olsen OH, Nadim F, Calabrese RL (1995) Modeling the leech heartbeat elemental oscillator: II. Exploring the parameter space. J. Comput. 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 

  • Paul DH, Mulloney B (1986) Intersegmental coordination of swimmeret rhythms in isolated nerve cords of crayfish. J. Comp. Physiol. A 158:215-224.

    Google Scholar 

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

    Google Scholar 

  • Peterson EL (1983b) Generation and coordination of heartbeat timing oscillation in the medicinal leech. II. Intersegmental coordination. J. Neurophysiol. 49:627-638.

    Google Scholar 

  • Pinsky PF, Rinzel J (1994) Intrinsic and network rhythmogenesis in a reduced Traub model for CA3 neurons. J. Comput. Neurosci. 1:39-60.

    Google Scholar 

  • Roberts A, Soffe SR, Wolf ES, Yoshida M, Zhao FY (1998) Central circuits controlling locomotion in young frog tadpoles. Ann. N.Y. Acad. Sci. 860:19-34.

    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 

  • Schweighofer N, Doya K, Kawato M (1999) Electrophysiological properties of inferior olive neurons: A compartmental model. J. Neurophysiol. 82:804-817.

    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 highthreshold transmission between heart interneurons of the medicinal leech by FMRF-NH2. J. Neurophysiol. 71:454-466.

    Google Scholar 

  • Skinner FK, Kopell N, Marder E (1994) Mechanisms for oscillation and frequency control in reciprocally inhibitory model neural networks. J. Comput. Neurosci. 1:69-87.

    Google Scholar 

  • Skinner FK, Kopell N, Mulloney B (1997) How does the crayfish swimmeret system work? Insights from nearest-neighbor coupled oscillator models. J. Comput. Neurosci. 4:151-160.

    Google Scholar 

  • Stein PSG (1971) Intersegmental coordination of swimmeret motor neuron activity in crayfish. J. Neurophysiol. 34:310-318.

    Google Scholar 

  • Thompson WJ, Stent GS (1976) Neuronal control of heartbeat in the medicinal leech. III. Synaptic relations of the heart interneurons. J. Comp. Physiol. 111:309-333.

    Google Scholar 

  • Tolbert LP, Calabrese RL (1985) Anatomical analysis of contacts between identified neurons that control heartbeat in the leech Hirudo medicinalis. Cell Tissue Res. 242:257-267.

    Google Scholar 

  • Wadden T, Hellgren J, Lansner A, Grillner S (1997) Intersegmental coordination in the lamprey: Simulations using a network model without segmental boundaries. Biol. Cybern. 76:1-9.

    Google Scholar 

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

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hill, A., Lu, J., Masino, M. et al. A Model of a Segmental Oscillator in the Leech Heartbeat Neuronal Network. J Comput Neurosci 10, 281–302 (2001). https://doi.org/10.1023/A:1011216131638

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1011216131638

Navigation