Predictive and reactive tuning of the locomotor CPG

The neural control of locomotion involves a constant interplaybetween the actions of a central pattern generator (CPG) andsensory input elicited by bodily movement. With respect to theCPG, recent analysis of fictive locomotion has shown that durationsof flexion and extension tend to covary along specific linesin plots of phase duration versus cycle duration. The slopesof these lines evidently depend on internal states that varyamong preparations, but, within a preparation, remain rathersteady from one sequence to the next. These relationships canbe reproduced in a simple oscillator model having two pairsof preset parameters, suggesting that steady internal drivesto flexor and extensor half-centers determine how phase durationscovary. Regarding the role of sensory inputs, previous experimentshave revealed state-dependent rules that govern phase-switchingindependently of the CPG rhythm. In addition, sensory inputis known to modulate motoneuronal activation through stretchreflexes. To explore how sensory input combines with the locomotorCPG, we used a neuromechanical model with muscle actuators,proprioceptive feedback, sensory phase-switching rules, anda CPG. Interestingly, sequences of stable locomotion were alwaysassociated with phase durations that conformed to an extensor-dominatedphase-duration characteristic (where extension durations varymore than flexion durations). This is the characteristic seenin normal animals, but not necessarily in fictive locomotion,where movement and associated sensory input are absent. Thissuggests that to produce the biomechanical events required forstability, an extensor-dominated phase-duration characteristicis required. In the model, when the preset CPG phase durationswere well matched to coincide the biomechanical requirements,CPG-mediated phase switching produced stable cycles. When CPGphase durations were too short, phases switched prematurelyand 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 fromhigher centers continually adjusts the operating point of theCPG on the preset phase-duration characteristic according toanticipated biomechanical requirements. When the predictionsare good, CPG-generated phase durations closely match thoserequired by the kinetics and kinematics, and little or no sensoryadjustment occurs. We propose the term "neuromechanical tuning"to describe this process of matching the CPG to the biomechanicalrequirements.