Skip to main content
Log in

Computer simulation of the segmental neural network generating locomotion in lamprey by using populations of network interneurons

  • Published:
Biological Cybernetics Aims and scope Submit manuscript

Abstract

Realistic computer simulations of the experimentally established local spinal cord neural network generating swimming in the lamprey have been performed. Populations of network interneurons were used in which cellular properties, like cell size and membrane conductance including voltage dependent ion channels were randomly distributed around experimentally obtained mean values, as were synaptic conductances (kainate/AMPA, NMDA, glycine) and delays. This population model displayed more robust burst activity over a wider frequency range than the more simple subsample model used previously, and the pattern of interneuronal activity was appropriate. The strength of the reciprocal inhibition played a very important role in the regulation of burst frequency, and just by changing the inhibitory bias the entire physiological range could be covered. At the lower frequency range of bursting the segmental excitatory interneurons provide stability as does the activation of voltage dependent NMDA receptors. Spike frequency adaptation by means of summation of afterhyperpolarization (AHP) serves as a major burst terminating factor, and at lower rates the membrane properties conferred by the NMDA receptor activation. The lateral interneurons were not of critical importance for the burst termination. They may, however, be of particular importance for inducing a rapid burst termination during for instance steering and righting reactions. Several cellular factors combine to provide a secure and stable motor pattern in the entire frequency range.

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

  • Alford S, Grillner S (1990) CNQX and DNQX block non-NMDA synaptic transmission but not NMDA-evoked locomotion in lamprey spinal cord. Brain Res 506:297–302

    Google Scholar 

  • Arshavsky YI, Beloozerova IN, Orlovsky GN, Panchin YV, Pavlova GA (1985) Control of locomotion in the marine mollusc, Clione limacina IV. Role of type 12 interneurons. Exp Brain Res 58:285–293

    Google Scholar 

  • Brodin L, Grillner S (1985) The role of putative excitatory amino acid neurotransmitters in the initiation of locomotion in the lamprey spinal cord. I. The effects of excitatory amino acid antagonists. Brain Res 360:139–148

    Google Scholar 

  • Brodin L, Grillner S (1986) Effects of magnesium on fictive locomotion induced by activation of N-methyl-D-aspartate (NMDA) receptors in the lamprey spinal cord in vitro. Brain Res 380:244–252

    Google Scholar 

  • Brodin L, Grillner S, Rovainen CM (1985) N-methyl-D-aspartate (NMDA), kainate and quisqualate receptors and the generation of fictive locomotion in the lamprey spinal cord. Brain Res 325:302–306

    Google Scholar 

  • Brodin L, Tråvén HGC, Lansner A, Wallén P, Ekeberg Ö, Grillner S (1991) Computer simulations of N-methyl-D-aspartate receptorinduced membrane properties in a neuron model. J Neurophysio 158:66:473–484

    Google Scholar 

  • Buchanan JT (1982) Identification of interneurons with contralateral, caudal axons in the lamprey spinal cord: synaptic interactions and morphology. J Neurophysiol 47:961–975

    Google Scholar 

  • Buchanan JT (1986) Premotor interneurons in the lamprey spinal cord: morphology, synaptic interactions and activities during fictive swimming. In: Grillner S, Stein PSG, Stuart DG, Forssberg H, Herman RM (eds) Neurobiology of vertebrate locomotion, Macmillan, London, pp 321–333

    Google Scholar 

  • Buchanan JT (1992) Neural network simulations of coupled locomotor oscillators in the lamprey spinal cord. Biol Cybern 66:367–374

    Google Scholar 

  • Buchanan JT, Grillner S, Cullheim S, Risling M (1989) Identification of excitatory interneurons contributing to generation of locomotion in lamprey: structure, pharmacology, and function. J Neurophysiol 62:59–69

    Google Scholar 

  • Dale N (1986) Excitatory synaptic drive for swimming mediated by amino acid receptors in the lamprey. J Neurosci 6:2662–2675

    Google Scholar 

  • Dale N, Grillner S (1986) Dual-component synaptic potentials in the lamprey mediated by excitatory amino acid receptors. J Neurosci 6:2653–2661

    Google Scholar 

  • Ekeberg Ö, Stensmo M, Lansner A (1990) SWIM — A simulator for real neural networks. Tech Rep TRITA-NA-P9014, Dept. of Numerical Analysis and Computing Science, Royal Institute of Technology, Stockholm, Sweden

    Google Scholar 

  • Ekeberg Ö, Wallén P, Lansner A, Tråvén H, Brodin L, Grillner S (1991) A computer based model for realistic simulations of neural networks. I. The single neuron and synaptic interaction. Biol Cybern 65:81–90

    Google Scholar 

  • Friesen WO, Stent GS (1978) Neural circuits for generating rhythmic movements. Ann Rev Biophys Bioeng 7:37–61

    Google Scholar 

  • Getting PA (1983) Mechanisms of pattern generation underlying swimming in tritonia. II. Network reconstruction. J Neurophysiol 49:1017–1035

    Google Scholar 

  • Getting PA (1989) Emerging principles governing the operation of neural networks. Annu Rev Neurosci 12:185–204

    Google Scholar 

  • Grillner S (1975) Locomotion in vertebrates: central mechanisms and reflex interaction. Physiol Rev 55:247–304

    Google Scholar 

  • Grillner S (1981) Control of locomotion in bipeds, tetrapods and fish. In: Brooks VB (ed) Handbook of Physiology. Sect 1. The Nervous system, vol II. Motor Control, American Physiological Society, Bethesda, Maryland, pp 1179–1236

    Google Scholar 

  • Grillner S (1985) Neurobiological bases of rhythmic motor acts in vertebrates. Science 228:143–149.

    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, McClellan A, Sigvardt K, Wallén P, Wilén M (1981) Activation of NMDA-receptors elicits “fictive locomotion” in lamprey spinal cord in vitro. Acta Physiol Scand 113:549–551

    Google Scholar 

  • Grillner S, Buchanan JT, Lansner A (1988) Simulation of the segmental burst generating network for locomotion in lamprey. Neurosci Lett 89:31–35

    Google Scholar 

  • Grillner S, Wallén P, Viana di Prisco G (1990) Cellular network underlying locomotion as revealed in a lower vertebrate model: transmitters, membrane properties, circuitry, and simulation. In: Symposia on quantitative biology, vol LV, The Brain, Cold Spring Harbor, New York, pp 779–789

    Google Scholar 

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

    Google Scholar 

  • Gustafsson B (1974) Afterhyperpolarisation and the control of repetitive firing in spinal neurons of the cat. Acta Physiol Scand 416 (Suppl)

  • Kahn JA (1982) Patterns of synaptic inhibition in motoneurons and interneurons during fictive swimming in the lamprey, as revealed by Cl injections. J Comp Physiol 147:189–194

    Google Scholar 

  • Kasicki S, Grillner S, Ohta Y, Dubuc R, Brodin L (1989) Phasic modulation of reticulospinal neurones during fictive locomotion and other types of spinal motor activity in lamprey. Brain Res 484:203–216

    Google Scholar 

  • Matsushima T, Grillner S (1990) Intersegmental co-ordination of undulatory movements — a “trailing oscillator” hypothesis. NeuroRep 1:97–100

    Google Scholar 

  • Matsushima T, Grillner S (1992) Neural mechanisms of intersegmental coordination in lamprey: local excitability changes modify the phase coupling along the spinal cord. J Neurophysiol 67:373–388

    Google Scholar 

  • McClellan AD, Grillner S (1984) Activation of “fictive swimming” by electrical microstimulation of brainstem locomotor regions in an in vitro preparation of the lamprey central nervous system. Brain Res 300:357–361

    Google Scholar 

  • Ohta Y, Grillner S (1989) Monosynaptic excitatory amino acid transmission from the posterior rhombencephalic reticular nucleus to spinal neurons involved in the control of locomotion in lamprey. J Neurophysiol 62:1079–1089

    Google Scholar 

  • Roberts A, Soffe SR, Dale N (1986) Spinal interneurones and swimming in frog embryos. In: Grillner S, Stein PSG, Stuart DG, Forssberg H, Herman RM (eds) Neurobiology of vertebrate locomotion, Macmillan, London, pp 279–306

    Google Scholar 

  • Roberts A, Tunstall MJ (1990) Mutual re-excitation with post-inhibitory rebound: a simulation study on the mechanisms for locomotor rhythm generation in the spinal cord of Xenopus embryos. Eur J Neurosci 2:11–23

    Google Scholar 

  • Rovainen C, (1979) Electrophysiology of vestibulospinal and vestibu-loreticulospinal systems in lampreys. J Neurophysiol 42:745–766

    Google Scholar 

  • Russell DF, Wallén P (1983) On the control of myotomal motoneurones during “fictive swimming” in the lamprey spinal cord in vitro. Acta Physiol Scand 117:161–170

    Google Scholar 

  • Selverston AI (1980) Are central pattern generators understandable? Behav Brain Sci 3:535–571

    Google Scholar 

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

    Google Scholar 

  • Tråvén HGC, Brodin L, Lansner A, Ekeberg Ö, Wallén P, Grillner S (1992) Computer simulations of NMDA and non-NMDA receptor-mediated synaptic drive and modulation of neurons and small networks (submitted)

  • Viana Di Prisco G, Wallén P, Grillner S (1990) Synaptic effects of intraspinal stretch receptor neurons mediating movement-related feedback during locomotion. Brain Res 530:161–166

    Google Scholar 

  • Wadden T, Grillner S, Matsushima T, Lanser A (1992) Trailing oscillator hypothesis of undulatory locomotion — realistic simulation of verified experimental network. J. Neurophysiol (under revision)

  • Wallén P, Grillner S (1987) N-methyl-D-aspartate receptor-induced, inherent oscillatory activity in neurons active during fictive locomotion in the lamprey. J Neurosci 7:2745–2755

    Google Scholar 

  • Wallén P, Lansner A (1984) Do the motoneurones constitute a part of the spinal network generating the swimming rhythm in the lamprey? J Exp Biol 113:493–497

    Google Scholar 

  • Wallén P, Williams T (1984) Fictive locomotion in the lamprey spinal cord in vitro compared with swimming in the intact and spinal animal. J Physiol 347:225–239

    Google Scholar 

  • Wallén P, Buchanan JT, Grillner S, Hill RH, Christenson J, Hökfelt T (1989) Effects of 5-hydroxytryptamine on the afterhyperpolarization, spike frequency regulation, and oscillatory membrane properties in lamprey spinal cord neurons. J Neurophysiol 61:759–768

    Google Scholar 

  • Wallén P, Ekeberg Ö, Lansner A, Brodin L, Tråvén H, Grillner S (1992a) A computer based model for realistic simulations of neural networks. II: The segmental network generating locomotor rhythmicity in the lamprey J. Neurophysiol 68

  • Wallén P, Shupliakov O, Hill RH (1992b) Origin of phasic synaptic inhibition to motoneurons during fictive locomotion in the lamprey (submitted)

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hellgren, J., Grillner, S. & Lansner, A. Computer simulation of the segmental neural network generating locomotion in lamprey by using populations of network interneurons. Biol. Cybern. 68, 1–13 (1992). https://doi.org/10.1007/BF00203132

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00203132

Keywords

Navigation