Brain-spinal cord interactions stabilize the locomotor rhythm to an external perturbation

Motor networks within the spinal cord of vertebrates are capable of generating rhythmic locomotor output even in the absence of phasic sensory input. In an intact animal these spinal pattern generators are affected by descending inputs from the brain and by sensory inputs. The role of the feedforward-feedback (FF-FB) loops between the brain and the spinal cord in the control of locomotion are not well understood. We hypothesized that the dynamic interaction between the brain and the spinal cord would affect the response of the neural system to external perturbation. We investigated this hypothesis in an in-vitro brain-spinal cord fictive locomotion preparation of a primitive vertebrate, lamprey. In tandem, we analyzed the behavior of a neural network model representing the brain and multiple segments of the spinal cord. Our experimental results indicate that with intact FF-FB loops, phase locked entrainment of the spinal motor activity can be obtained on direct stimulation of the spinal cord. However, the effect is localized with minimal influence on distal spinal segments. The intersegmental coupling strength is strong as indicated by a fast recovery of the perturbed rhythm to the natural frequency on termination of the perturbation. With the FF-FB loop interrupted, the perturbation was capable of altering the motor activity from multiple sites in the spinal cord. Also, upon termination of the perturbation there was a prolonged period before recovery of the original natural frequency. Model analyses support our interpretation of the experimental results. In the neural network model with the brain-spinal cord loops closed there was a localized effect on the oscillatory rhythm and strong intersegmental coupling. Also, the analysis indicated the presence of a smaller entrainment range and many more periodic orbits than with the loops open. The results suggest that the increased variability in the locomotor rhythm and decreased sensitivity to perturbation observed in the presence of intact brain spinal cord connections may be a reflection of a higher dimensional system with many periodic orbits. The higher dimension could allow the system to collectively remain within the attractor space of one of these periodic orbits and thus remain resilient to perturbation.