Activity of bifunctional motoneurons during fictive locomotion: A computational modeling study

More than 90 years ago, Graham Brown demonstrated that the cat spinal cord can generate a locomotor rhythm in the absence of input from higher brain centers and afferent feedback, and proposed a general schematic for the spinal central pattern generator (CPG) generating rhythmic alternating activity of flexor and extensor motoneurons during locomotion, the "half-center" model. Since that time, the half-center concept has been used as the basis in many CPG models. Despite many advantages, classical half-center models of the locomotor CPG have been so far unable to reproduce and explain the generation of more complex activity patterns expressed during locomotion by some bifunctional motoneurons actuating muscles controlling more than one joint, such as posterior biceps and semitendinosus (PBSt) and rectus femoris (RF), which were found to be active within a portion of one phase or generated activity during both phases. During normal locomotion, the activity patterns of PBSt and RF are modulated by supra-spinal inputs and afferent feedback and vary with gate and locomotor conditions. However, even during fictive locomotion in the absence of afferent feedback and patterned supra-spinal inputs, PBSt and RF demonstrate a variety of complex activity patterns, similar to those observed in real locomotion under different conditions. This suggests that the complex patterns of bifunctionals are defined by the intrinsic spinal CPG organization. The non-trivial activity profiles expressed by bifunctional motoneurons have been considered as a strong argument against a bipartite half-center organization of the spinal locomotor CPG. The challenging task of this study was to find and propose a neural organization of the spinal locomotor CPG that is able to reproduce the full repertoire of PBSt and RF activities observed during fictive locomotion within the framework of the bipartite organization of the locomotor CPG, implement it in a computational model, and validate the model by reproducing the behavior of bifunctional motoneurons during various types of deletions occurring during fictive locomotion. This study represents a significant step towards understanding the organization of the mammalian spinal locomotor CPG, shaping complex patterns of bifunctional motoneurons, and offers a mechanism for their control by afferent feedback.