Predictive and reactive tuning of the locomotor CPG

The neural control of locomotion involves a constant interplay between the actions of a central pattern generator (CPG) and sensory input elicited by bodily movement. With respect to the CPG, recent analysis of fictive locomotion has shown that durations of flexion and extension tend to covary along specific lines in plots of phase duration versus cycle duration. The slopes of these lines evidently depend on internal states that vary among preparations, but, within a preparation, remain rather steady from one sequence to the next. These relationships can be reproduced in a simple oscillator model having two pairs of preset parameters, suggesting that steady internal drives to flexor and extensor half-centers determine how phase durations covary. Regarding the role of sensory inputs, previous experiments have revealed state-dependent rules that govern phase-switching independently of the CPG rhythm. In addition, sensory input is known to modulate motoneuronal activation through stretch reflexes. To explore how sensory input combines with the locomotor CPG, we used a neuromechanical model with muscle actuators, proprioceptive feedback, sensory phase-switching rules, and a CPG. Interestingly, sequences of stable locomotion were always associated with phase durations that conformed to an extensor-dominated phase-duration characteristic (where extension durations vary more than flexion durations). This is the characteristic seen in normal animals, but not necessarily in fictive locomotion, where movement and associated sensory input are absent. This suggests that to produce the biomechanical events required for stability, an extensor-dominated phase-duration characteristic is required. In the model, when the preset CPG phase durations were well matched to coincide the biomechanical requirements, CPG-mediated phase switching produced stable cycles. When CPG phase durations were too short, phases switched prematurely and the model soon fell. When CPG phase durations were too long, sensory rules fired and overrode the CPG, maintaining stability. We posit that under normal circumstances, descending input from higher centers continually adjusts the operating point of the CPG on the preset phase-duration characteristic according to anticipated biomechanical requirements. When the predictions are good, CPG-generated phase durations closely match those required by the kinetics and kinematics, and little or no sensory adjustment occurs. We propose the term "neuromechanical tuning" to describe this process of matching the CPG to the biomechanical requirements.

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