Modelling Inter-Segmental Coordination of Neuronal Oscillators: Synaptic Mechanisms for Uni-Directional Coupling During Swimming in Xenopus Tadpoles

Locomotion requires longitudinal co-ordination. We have examined uni-directional synaptic coupling processes between two classes of neuronal network oscillators: autonomously active “intrinsic” oscillators, and “potential” oscillators that lack sufficient excitatory drive for autonomous activity. We model such oscillator networks in the bilaterally-symmetrical, Xenopus tadpole spinal cord circuits that co-ordinate swimming. “Glutamate” coupling EPSPs can entrain a second oscillator of lower frequency provided their strength is sufficient. Fast (AMPA) EPSPs advance spiking on each cycle, while slow (NMDA) EPSPs increase frequency over many cycles. EPSPs can also enable rhythmicity in “potential” oscillators and entrain them. IPSPs operate primarily on a cycle-by-cycle basis. They can advance or delay spiking to entrain a second “intrinsic” oscillator with higher, equal or lower frequency. Bilaterally symmetrical coupling connections operate twice per cycle: once in each half-cycle, on each side of the receiving oscillator. Excitatory and inhibitory coupling allow entrainment in complimentary areas of parameter space.

[1]  Örjan Ekeberg,et al.  A computer based model for realistic simulations of neural networks , 1991, Biological Cybernetics.

[2]  Stephen R. Soffe,et al.  Neuronal mechanisms for generating locomotor activity , 1998 .

[3]  S. Grillner,et al.  Neural mechanisms of intersegmental coordination in lamprey: local excitability changes modify the phase coupling along the spinal cord. , 1992, Journal of neurophysiology.

[4]  S. Grillner,et al.  The neurophysiological bases of undulatory locomotion in vertebrates , 1993 .

[5]  G. Ermentrout,et al.  Oscillator death in systems of coupled neural oscillators , 1990 .

[6]  T. Williams,et al.  Effects of local oscillator frequency on intersegmental coordination in the lamprey locomotor CPG: theory and experiment. , 1996, Journal of neurophysiology.

[7]  P. Wallén,et al.  Fictive locomotion in the lamprey spinal cord in vitro compared with swimming in the intact and spinal animal. , 1984, The Journal of physiology.

[8]  N Dale,et al.  Reciprocal inhibitory interneurones in the Xenopus embryo spinal cord. , 1985, The Journal of physiology.

[9]  A. Roberts,et al.  Asymmetries in sensory pathways from skin to motoneurons on each side of the body determine the direction of an avoidance response in hatchling Xenopus tadpoles , 1998, The Journal of physiology.

[10]  Ole Kiehn,et al.  Neuronal mechanisms for generating locomotor activity , 1998 .

[11]  S. Soffe,et al.  Spinal Interneurones and Swimming in Frog Embryos , 1986 .

[12]  A. Roberts,et al.  Longitudinal distribution of components of excitatory synaptic input to motoneurones during swimming in young Xenopus tadpoles: experiments with antagonists , 1998, The Journal of physiology.

[13]  F K Skinner,et al.  Intersegmental Coordination of Swimmeret Movements: Mathematical Models and Neural Circuitsa , 1998, Annals of the New York Academy of Sciences.

[14]  M J Tunstall,et al.  A longitudinal gradient of synaptic drive in the spinal cord of Xenopus embryos and its role in co‐ordination of swimming. , 1994, The Journal of physiology.

[15]  A. Roberts,et al.  The central nervous origin of the swimming motor pattern in embryos of Xenopus laevis. , 1982, The Journal of experimental biology.

[16]  S. Soffe.  Ionic and pharmacological properties of reciprocal inhibition in Xenopus embryo motoneurones. , 1987, The Journal of physiology.

[17]  S. Grillner,et al.  Intersegmental co-ordination of undulatory movements--a "trailing oscillator" hypothesis. , 1990, Neuroreport.

[18]  W. O. Friesen,et al.  A model for intersegmental coordination in the leech nerve cord , 1988, Biological Cybernetics.

[19]  N. Dale,et al.  Kinetic characterization of the voltage‐gated currents possessed by Xenopus embryo spinal neurons. , 1995, The Journal of physiology.

[20]  G. Ermentrout,et al.  Modelling of intersegmental coordination in the lamprey central pattern generator for locomotion , 1992, Trends in Neurosciences.

[21]  J. Bower,et al.  The Book of GENESIS , 1998, Springer New York.

[22]  G. Ermentrout,et al.  Coupled oscillators and the design of central pattern generators , 1988 .

[23]  A. Roberts,et al.  Mutual Re‐excitation with Post‐Inhibitory Rebound: A Simulation Study on the Mechanisms for Locomotor Rhythm Generation in the Spinal Cord of Xenopus Embryos , 1990, The European journal of neuroscience.

[24]  S. Soffe,et al.  Active and Passive Membrane Properties of Spinal Cord Neurons that Are Rhythmically Active during Swimming in Xenopus Embryos , 1990, The European journal of neuroscience.

[25]  S. Soffe,et al.  Tonic and phasic synaptic input to spinal cord motoneurons during fictive locomotion in frog embryos. , 1982, Journal of neurophysiology.

[26]  A. Roberts,et al.  Dual‐component amino‐acid‐mediated synaptic potentials: excitatory drive for swimming in Xenopus embryos. , 1985, The Journal of physiology.

[27]  K. Sigvardt.  Intersegmental coordination in the lamprey central pattern generator for locomotion , 1993 .

[28]  A. Roberts,et al.  Properties of networks controlling locomotion and significance of voltage dependency of NMDA channels: stimulation study of rhythm generation sustained by positive feedback. , 1995, Journal of neurophysiology.

[29]  P. Stein.  Intersegmental coordination of swimmeret motoneuron activity in crayfish. , 1971, Journal of neurophysiology.

[30]  W. O. Friesen,et al.  Sensory Modification of Leech Swimming: Rhythmic Activity of Ventral Stretch Receptors Can Change Intersegmental Phase Relationships , 2000, The Journal of Neuroscience.

[31]  K A Sigvardt,et al.  Analysis and Modeling of the Locomotor Central Pattern Generator as a Network of Coupled Oscillators , 1998, Annals of the New York Academy of Sciences.

[32]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1990 .

[33]  S. Soffe,et al.  Synaptic potentials in motoneurons during fictive swimming in spinal Xenopus embryos. , 1985, Journal of neurophysiology.

[34]  A Roberts,et al.  Longitudinal coordination of motor output during swimming in Xenopus embryos , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[35]  Joël Tabak,et al.  Simulation and Parameter Estimation Study of a Simple Neuronal Model of Rhythm Generation: Role of NMDA and Non-NMDA Receptors , 1998, Journal of Computational Neuroscience.

[36]  N. Dale,et al.  Experimentally derived model for the locomotor pattern generator in the Xenopus embryo. , 1995, The Journal of physiology.

[37]  James T. Buchanan,et al.  Neural network simulations of coupled locomotor oscillators in the lamprey spinal cord , 1992, Biological Cybernetics.