Multimodal behavior in a four neuron ring circuit: mode switching

We study a four-neuron ring circuit comprised of oscillating burst-type neurons unidirectionally coupled via inhibitory synapses. Simple circuits of this type have been used previously to study gait patterns. The ring circuit itself is a variant of the basic reciprocal inhibition network, and it exhibits the property of multistability (multiple stable modes of behavior). That is, different gait modes can be achieved via appropriate initialization of and parameterization of this self-excited oscillatory network. We demonstrate three common gait modes with this circuit: the walk, the bound, and a slightly rotated trot mode. Attention is focused mainly on the mechanisms of rapidly and effectively switching between these modes. Our simulations suggest that neuron membrane dynamics, as well as synaptic junctional properties, strongly influence phase sensitivity in the network; each synapse is a combination of both and can be characterized by a transient phase response curve (PRC). We use the same bursting neuron model to characterize all network neurons, and shape different transient PRCs by using different synaptic properties. The characteristics of these PRCs determine the gait modes sustained in any network configuration, as well as, the ability to switch between modes. The mechanisms explored in this simple circuit, may find application in the switching of more complicated gait pattern networks, as well as, in the design of neuromorphic gait pattern circuits.

[1]  John W. Clark,et al.  Control of multistability in ring circuits of oscillators , 1999, Biological Cybernetics.

[2]  R. Douglas,et al.  A silicon neuron , 1991, Nature.

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

[4]  M. Golubitsky,et al.  Symmetry in locomotor central pattern generators and animal gaits , 1999, Nature.

[5]  S. Grillner Locomotion in vertebrates: central mechanisms and reflex interaction. , 1975, Physiological reviews.

[6]  John W. Clark,et al.  A mathematical criterion based on phase response curves for stability in a ring of coupled oscillators , 1999, Biological Cybernetics.

[7]  Eve Marder,et al.  Mechanisms for oscillation and frequency control in reciprocally inhibitory model neural networks , 1994, Journal of Computational Neuroscience.

[8]  Ian Stewart,et al.  A modular network for legged locomotion , 1998 .

[9]  Frank Pasemann,et al.  Characterization of periodic attractors in neural ring networks , 1995, Neural Networks.

[10]  P. Stein Motor systems, with specific reference to the control of locomotion. , 1978, Annual review of neuroscience.

[11]  Teuvo Kohonen,et al.  Self-Organization and Associative Memory , 1988 .

[12]  M. L. Shik,et al.  Neurophysiology of locomotor automatism. , 1976, Physiological reviews.

[13]  John W. Clark,et al.  Analysis of the effects of modulatory agents on a modeled bursting neuron: Dynamic interactions between voltage and calcium dependent systems , 1995, Journal of Computational Neuroscience.

[14]  R Huerta,et al.  Dynamic control of irregular bursting in an identified neuron of an oscillatory circuit. , 1999, Journal of neurophysiology.

[15]  John W. Clark,et al.  Phase response characteristics of model neurons determine which patterns are expressed in a ring circuit model of gait generation , 1997, Biological Cybernetics.

[16]  Philip D. Wasserman,et al.  Advanced methods in neural computing , 1993, VNR computer library.

[17]  Carver A. Mead,et al.  A single-transistor silicon synapse , 1996 .

[18]  T. Brown The intrinsic factors in the act of progression in the mammal , 1911 .

[19]  K L Magleby,et al.  A quantitative description of end‐plate currents , 1972, The Journal of physiology.

[20]  D. J. Woodward,et al.  Bistability, switches and working memory in a two-neuron inhibitory-feedback model , 1993, Biological Cybernetics.

[21]  S Grillner,et al.  Central pattern generators for locomotion, with special reference to vertebrates. , 1985, Annual review of neuroscience.

[22]  H. Yuasa,et al.  Coordination of many oscillators and generation of locomotory patterns , 1990, Biological Cybernetics.

[23]  Shik Ml,et al.  Control of walking and running by means of electric stimulation of the midbrain , 1966 .

[24]  Carver Mead,et al.  Analog VLSI and neural systems , 1989 .

[25]  J. J. Collins,et al.  Hexapodal gaits and coupled nonlinear oscillator models , 1993, Biological Cybernetics.

[26]  I. Stewart,et al.  Coupled nonlinear oscillators and the symmetries of animal gaits , 1993 .

[27]  C. Mead,et al.  Neuromorphic analogue VLSI. , 1995, Annual review of neuroscience.

[28]  A. Hindmarsh,et al.  CVODE, a stiff/nonstiff ODE solver in C , 1996 .

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

[30]  Pozin Nv,et al.  Analysis of the work of autooscillating neuron combinations , 1970 .

[31]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1952, The Journal of physiology.

[32]  D. Perkel,et al.  Motor Pattern Production in Reciprocally Inhibitory Neurons Exhibiting Postinhibitory Rebound , 1974, Science.

[33]  M. Golubitsky,et al.  Models of central pattern generators for quadruped locomotion I. Primary gaits , 2001, Journal of mathematical biology.

[34]  Sorin Draghici,et al.  Neural Networks in Analog Hardware - Design and Implementation Issues , 2000, Int. J. Neural Syst..

[35]  John W. Clark,et al.  Dissection and reduction of a modeled bursting neuron , 1996, Journal of Computational Neuroscience.

[36]  J. J. Collins,et al.  Hard-wired central pattern generators for quadrupedal locomotion , 1994, Biological Cybernetics.

[37]  S. Grillner Neurobiological bases of rhythmic motor acts in vertebrates. , 1985, Science.

[38]  D. Perkel,et al.  Motor-pattern production: interaction of chemical and electrical synapses , 1981, Brain Research.

[39]  D. Noble,et al.  Reconstruction of the electrical activity of cardiac Purkinje fibres. , 1975, The Journal of physiology.

[40]  M. Golubitsky,et al.  Models of central pattern generators for quadruped locomotion II. Secondary gaits , 2001, Journal of mathematical biology.

[41]  W. O. Friesen,et al.  Neural circuits for generating rhythmic movements. , 1978, Annual review of biophysics and bioengineering.

[42]  J. J. Collins,et al.  A group-theoretic approach to rings of coupled biological oscillators , 1994, Biological Cybernetics.

[43]  W. O. Friesen,et al.  Generation of a locomotory rhythm by a neural network with recurrent cyclic inhibition , 1977, Biological Cybernetics.