Simulations of neuromuscular control in lamprey swimming.

The neuronal generation of vertebrate locomotion has been extensively studied in the lamprey. Models at different levels of abstraction are being used to describe this system, from abstract nonlinear oscillators to interconnected model neurons comprising multiple compartments and a Hodgkin-Huxley representation of the most relevant ion channels. To study the role of sensory feedback by simulation, it eventually also becomes necessary to incorporate the mechanical movements in the models. By using simplifying models of muscle activation, body mechanics, counteracting water forces, and sensory feedback through stretch receptors and vestibular organs, we have been able to close the feedback loop to enable studies of the interaction between the neuronal and the mechanical systems. The neuromechanical simulations reveal that the currently known network is sufficient for generating a whole repertoire of swimming patterns. Swimming at different speeds and with different wavelengths, together with the performance of lateral turns can all be achieved by simply varying the brainstem input. The neuronal mechanisms behind pitch and roll manoeuvres are less clear. We have put forward a 'crossed-oscillators' hypothesis where partly separate dorsal and ventral circuits are postulated. Neuromechanical simulations of this system show that it is also capable of generating realistic pitch turns and rolls, and that vestibular signals can stabilize the posture during swimming.

[1]  S. Grillner,et al.  Entrainment of the spinal pattern generators for swimming by mechano-sensitive elements in the lamprey spinal cord in vitro , 1981, Brain Research.

[2]  P. Holmes,et al.  The nature of the coupling between segmental oscillators of the lamprey spinal generator for locomotion: A mathematical model , 1982, Journal of mathematical biology.

[3]  Ullén,et al.  Spatial orientation in the lamprey. I. Control of pitch and roll , 1995, The Journal of experimental biology.

[4]  J. Buchanan Identification of interneurons with contralateral, caudal axons in the lamprey spinal cord: synaptic interactions and morphology. , 1982, Journal of neurophysiology.

[5]  N. Curtin,et al.  Predicting force generation by lamprey muscle during applied sinusoidal movement using a simple dynamic model. , 1998, The Journal of experimental biology.

[6]  S. Grillner,et al.  Dorsal and ventral myotome motoneurons and their input during fictive locomotion in lamprey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  Ullén,et al.  Spatial orientation in the lamprey. II. Visual influence on orientation during locomotion and in the attached state , 1995, The Journal of experimental biology.

[8]  Örjan Ekeberg,et al.  The Neural Control of Fish Swimming Studied Through Numerical Simulations , 1995, Adapt. Behav..

[9]  Anders Lansner,et al.  Activity-dependent modulation of adaptation produces a constant burst proportion in a model of the lamprey spinal locomotor generator , 1998, Biological Cybernetics.

[10]  S. Grillner,et al.  Undulatory Locomotion — Simulations with Realistic Segmental Oscillator , 1993 .

[11]  R. A. Davidoff Neural Control of Rhythmic Movements in Vertebrates , 1988, Neurology.

[12]  S. Grillner,et al.  Activation of NMDA-receptors elicits "fictive locomotion" in lamprey spinal cord in vitro. , 1981, Acta physiologica Scandinavica.

[13]  S. Grillner,et al.  A new population of neurons with crossed axons in the lamprey spinal cord , 1991, Brain Research.

[14]  S. Grillner,et al.  Low-voltage-activated calcium channels in the lamprey locomotor network: simulation and experiment. , 1997, Journal of neurophysiology.

[15]  S. Grillner,et al.  Synaptic effects of intraspinal stretch receptor neurons mediating movement-related feedback during locomotion , 1990, Brain Research.

[16]  T. Williams,et al.  Anguilliform Body Dynamics: Modelling the Interaction between Muscle Activation and Body Curvature , 1991 .

[17]  Anders Lansner,et al.  Intersegmental coordination in the lamprey: simulations using a network model without segmental boundaries , 1997, Biological Cybernetics.

[18]  Ö. Ekeberg An Integrated Neuronal and Mechanical Model of Fish Swimming , 1994 .

[19]  P. Wallén,et al.  do the Motoneurones Constitute a Part of the Spinal Network Generating the Swimming Rhythm in the Lamprey , 1984 .

[20]  S. Grillner,et al.  Computer simulations of NMDA and non-NMDA receptor-mediated synaptic drive: sensory and supraspinal modulation of neurons and small networks. , 1993, Journal of neurophysiology.

[21]  S. Grillner,et al.  Calcium-dependent potassium channels play a critical role for burst termination in the locomotor network in lamprey. , 1994, Journal of neurophysiology.

[22]  S. Grillner,et al.  Computer simulations of N-methyl-D-aspartate receptor-induced membrane properties in a neuron model. , 1991, Journal of neurophysiology.

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

[24]  N. Curtin,et al.  Interactions between muscle activation, body curvature and the water in the swimming lamprey. , 1995, Symposia of the Society for Experimental Biology.

[25]  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.

[26]  S. Grillner,et al.  A computer-based model for realistic simulations of neural networks. II. The segmental network generating locomotor rhythmicity in the lamprey. , 1992 .

[27]  Anders Lansner,et al.  Intersegmental coordination in the lamprey: Simulations using a continuous network model , 1996 .

[28]  Anders Lansner,et al.  A computational and experimental study of rebound firing and modulatory effects on the Lamprey spinal network , 1997 .

[29]  S. Grillner,et al.  Neural networks that co-ordinate locomotion and body orientation in lamprey , 1995, Trends in Neurosciences.

[30]  T. Williams Phase coupling by synaptic spread in chains of coupled neuronal oscillators. , 1992, Science.