A comparison of resonance tuning with positive versus negative sensory feedback

We used a computational model of rhythmic movement to analyze how the connectivity of sensory feedback affects the tuning of a closed-loop neuromechanical system to the mechanical resonant frequency (ωr). Our model includes a Matsuoka half-center oscillator for a central pattern generator (CPG) and a linear, one-degree-of-freedom system for a mechanical component. Using both an open-loop frequency response analysis and closed-loop simulations, we compared resonance tuning with four different feedback configurations as the mechanical resonant frequency, feedback gain, and mechanical damping varied. The feedback configurations consisted of two negative and two positive feedback connectivity schemes. We found that with negative feedback, resonance tuning predominantly occurred when ωr was higher than the CPG’s endogenous frequency (ωCPG). In contrast, with the two positive feedback configurations, resonance tuning only occurred if ωr was lower than ωCPG. Moreover, the differences in resonance tuning between the two positive (negative) feedback configurations increased with increasing feedback gain and with decreasing mechanical damping. Our results indicate that resonance tuning can be achieved with positive feedback. Furthermore, we have shown that the feedback configuration affects the parameter space over which the endogenous frequency of the CPG or resonant frequency the mechanical dynamics dominates the frequency of a rhythmic movement.

[1]  J. Hollerbach,et al.  Time-varying stiffness of human elbow joint during cyclic voluntary movement , 2005, Experimental Brain Research.

[2]  J. Hamill,et al.  Energetic Cost and Stability During Human Walking at the Preferred Stride Velocity. , 1995, Journal of motor behavior.

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

[4]  L. Stark,et al.  Muscle models: What is gained and what is lost by varying model complexity , 1987, Biological Cybernetics.

[5]  W. Megill,et al.  Frequency tuning in animal locomotion. , 2006, Zoology.

[6]  H Barbeau,et al.  Treadmill walking in incomplete spinal-cord-injured subjects: 1. Adaptation to changes in speed , 2003, Spinal Cord.

[7]  Matthew M. Williamson,et al.  Neural control of rhythmic arm movements , 1998, Neural Networks.

[8]  K. G. Holt,et al.  The hybrid mass-spring pendulum model of human leg swinging: stiffness in the control of cycle period , 1995, Biological Cybernetics.

[9]  M. MacKay-Lyons Central pattern generation of locomotion: a review of the evidence. , 2002, Physical therapy.

[10]  S. Jeng,et al.  Optimization of walking in children. , 1997, Medicine and science in sports and exercise.

[11]  Kiyotoshi Matsuoka,et al.  Mechanisms of frequency and pattern control in the neural rhythm generators , 1987, Biological Cybernetics.

[12]  E. Marder,et al.  Central pattern generators and the control of rhythmic movements , 2001, Current Biology.

[13]  S. Grillner,et al.  Central modulation of stretch receptor neurons during fictive locomotion in lamprey. , 1996, Journal of neurophysiology.

[14]  J. Konczak,et al.  Identification of time-varying stiffness, damping, and equilibrium position in human forearm movements. , 1999, Motor control.

[15]  Norimasa Yamada,et al.  Modulation of elbow joint stiffness in a vertical plane during cyclic movement at lower or higher frequencies than natural frequency , 2003, Experimental Brain Research.

[16]  John M. Gosline,et al.  Mechanics of Jet Propulsion in the Hydromedusan Jellyfish, Polyorchis Pexicillatus: III. A Natural Resonating Bell; The Presence and Importance of a Resonant Phenomenon in the Locomotor Structure , 1988 .

[17]  David L. Raney,et al.  Mechanization and Control Concepts for Biologically Inspired Micro Air Vehicles , 2004 .

[18]  A. Ménard,et al.  The Modulation of Presynaptic Inhibition in Single Muscle Primary Afferents during Fictive Locomotion in the Cat , 1999, The Journal of Neuroscience.

[19]  K. Pearson,et al.  The role of proprioceptive feedback in the regulation and adaptation of locomotor activity. , 2002, Advances in experimental medicine and biology.

[20]  M. E. Demont,et al.  Tuned oscillations in the swimming scallop Pecten maximus , 1990 .

[21]  J. L. Fanson,et al.  Positive position feedback control for large space structures , 1990 .

[22]  D. Ann Pabst,et al.  Springs in Swimming Animals , 1996 .

[23]  R E Burke,et al.  Spindle model responsive to mixed fusimotor inputs and testable predictions of beta feedback effects. , 2003, Journal of neurophysiology.

[24]  M. Turvey,et al.  Advantages of Rhythmic Movements at Resonance: Minimal Active Degrees of Freedom, Minimal Noise, and Maximal Predictability , 2000, Journal of motor behavior.

[25]  Daniel J. Inman,et al.  The relationship between positive position feedback and output feedback controllers , 1999 .

[26]  T. Brown On the nature of the fundamental activity of the nervous centres; together with an analysis of the conditioning of rhythmic activity in progression, and a theory of the evolution of function in the nervous system , 1914, The Journal of physiology.

[27]  W. Warren,et al.  Resonance Tuning in Rhythmic Arm Movements. , 1996, Journal of motor behavior.

[28]  Ronald L Calabrese,et al.  Detailed model of intersegmental coordination in the timing network of the leech heartbeat central pattern generator. , 2004, Journal of neurophysiology.

[29]  E. Zehr,et al.  Regulation of Arm and Leg Movement during Human Locomotion , 2004, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[30]  H Barbeau,et al.  Treadmill walking in incomplete spinal-cord-injured subjects: 2. Factors limiting the maximal speed , 2003, Spinal Cord.

[31]  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 .

[32]  M G Pandy,et al.  Computer modeling and simulation of human movement. , 2001, Annual review of biomedical engineering.

[33]  J. Hamill,et al.  The force-driven harmonic oscillator as a model for human locomotion , 1990 .

[34]  Frans C. T. van der Helm,et al.  Energy efficient and robust rhythmic limb movement by central pattern generators , 2006, Neural Networks.

[35]  A. Willsky,et al.  Signals and Systems , 2004 .

[36]  T. K. Caughey,et al.  On the stability problem caused by finite actuator dynamics in the collocated control of large space structures , 1985 .

[37]  J. Hamill,et al.  Energetic Cost and Stability during Human Walking at the Preferred Stride Frequency , 1995 .

[38]  K. Sillar,et al.  Phase-dependent reversal of reflexes mediated by the thoracocoxal muscle receptor organ in the crayfish, Pacifastacus leniusculus. , 1986, Journal of neurophysiology.

[39]  Nicholas G. Hatsopoulos,et al.  Coupling the Neural and Physical Dynamics in Rhythmic Movements , 1996, Neural Computation.

[40]  Tetsuya Iwasaki,et al.  Sensory Feedback Mechanism Underlying Entrainment of Central Pattern Generator to Mechanical Resonance , 2006, Biological Cybernetics.

[41]  John H. Long,et al.  The Importance of Body Stiffness in Undulatory Propulsion , 1996 .

[42]  K. Sillar,et al.  Identified proprioceptive afferents and motor rhythm entrainment in the crayfish walking system. , 1992, Journal of neurophysiology.

[43]  A. Prochazka,et al.  Implications of positive feedback in the control of movement. , 1997, Journal of neurophysiology.

[44]  Mark Halaki,et al.  Systematic nonlinear relations between displacement amplitude and joint mechanics at the human wrist. , 2006, Journal of biomechanics.

[45]  D J Kriellaars,et al.  Mechanical entrainment of fictive locomotion in the decerebrate cat. , 1994, Journal of neurophysiology.

[46]  Kiyotoshi Matsuoka,et al.  Sustained oscillations generated by mutually inhibiting neurons with adaptation , 1985, Biological Cybernetics.

[47]  F. Delcomyn Neural basis of rhythmic behavior in animals. , 1980, Science.

[48]  W. O. Friesen,et al.  Reciprocal inhibition: A mechanism underlying oscillatory animal movements , 1994, Neuroscience & Biobehavioral Reviews.

[49]  A. Cohen,et al.  Impact of movement and movement-related feedback on the lamprey central pattern generator for locomotion. , 2001, The Journal of experimental biology.

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

[51]  Weiping Li,et al.  Applied Nonlinear Control , 1991 .

[52]  K. Sigvardt,et al.  Features of entrainment of spinal pattern generators for locomotor activity in the lamprey spinal cord , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.