A Simple Experimentally Based Model Using Proprioceptive Regulation of Motor Primitives Captures Adjusted Trajectory Formation in Spinal Frogs

• Published in: Journal of neurophysiology 2010-01, Vol.103 (1), p.573-590
• Main Authors: Kargo, William J, Ramakrishnan, Arun, Hart, Corey B, Rome, Lawrence C, Giszter, Simon F
• Format: Article
• Language: English
• Subjects: Action Potentials; Algorithms; Animals; Biomechanical Phenomena; Computer Simulation; Electromyography; Feedback, Physiological - physiology; Hindlimb - physiology; Models, Neurological; Motor Activity - physiology; Muscle Spindles - physiology; Muscle, Skeletal - physiology; Proprioception - physiology; Rana catesbeiana; Spinal Cord - physiology
• ISSN: 0022-3077; 1522-1598
• DOI: 10.1152/jn.01054.2007

1 Department of Neurobiology and Anatomy, Drexel University College of Medicine; 2 School of Bioengineering and Health Sciences, Drexel University; 3 Biology Department, University of Pennsylvania, Philadelphia, Pennsylvania; and 4 Vertex Pharmaceuticals, San Diego, California Submitted 31 May 2008; accepted in final form 15 July 2009 ABSTRACT Spinal circuits may organize trajectories using pattern generators and synergies. In frogs, prior work supports fixed-duration pulses of fixed composition synergies, forming primitives. In wiping behaviors, spinal frogs adjust their motor activity according to the starting limb position and generate fairly straight and accurate isochronous trajectories across the workspace. To test whether a compact description using primitives modulated by proprioceptive feedback could reproduce such trajectory formation, we built a biomechanical model based on physiological data. We recorded from hindlimb muscle spindles to evaluate possible proprioceptive input. As movement was initiated, early skeletofusimotor activity enhanced many muscle spindles firing rates. Before movement began, a rapid estimate of the limb position from simple combinations of spindle rates was possible. Three primitives were used in the model with muscle compositions based on those observed in frogs. Our simulations showed that simple gain and phase shifts of primitives based on published feedback mechanisms could generate accurate isochronous trajectories and motor patterns that matched those observed. Although on-line feedback effects were omitted from the model after movement onset, our primitive-based model reproduced the wiping behavior across a range of starting positions. Without modifications from proprioceptive feedback, the model behaviors missed the target in a manner similar to that in deafferented frogs. These data show how early proprioception might be used to make a simple estimate initial limb state and to implicitly plan a movement using observed spinal motor primitives. Simulations showed that choice of synergy composition played a role in this simplicity. To generate froglike trajectories, a hip flexor synergy without sartorius required motor patterns with more proprioceptive knee flexor control than did patterns built with a more natural synergy including sartorius. Such synergy choices and control strategies may simplify the circuitry required for reflex trajectory construction and adaptation. Address for reprint requests and other cor