Adaptive control for backward quadrupedal walking V. Mutable activation of bifunctional thigh muscles

In this, the fifth article in a series to assess changes in posture, hindlimb dynamics, and muscle synergies associated with backward (BWD) quadrupedal walking, we compared the recruitment of three biarticular muscles of the cat's anterior thigh (anterior sartorius, SAa; medial sartorius, SAm; rectus femoris, RF) for forward (FWD) and BWD treadmill walking. Electromyography (EMG) records from these muscles, along with those of two muscles (semitendinosus, ST; anterior biceps femoris, ABF) studied previously in this series, were synchronized with kinematic data digitized from high-speed ciné film for unperturbed steps and steps in which a stumbling corrective reaction was elicited during swing. 2. During swing, the relative timing of EMG activity for the unifunctional SAm (hip and knee flexor) was similar for unperturbed steps of FWD and BWD walking. The SAm was active before paw lift off and remained active during most of swing (75%) for both forms of walking, but there was a marked decrease in EMG amplitude after paw off during BWD and not FWD swing. In contrast, the relative timing of EMG activity for the SAa and RF, two bifunctional muscles (hip flexors, knee extensors), was different for FWD and BWD swing. During FWD swing, the SAa and the RF (to a lesser extent) were coactive with the SAm; however, during BWD swing, the SAa and RF were active just before paw lift off and then inactive for the rest of swing until just before paw contact (see 3). Thus the swing-phase activity of the SAa and RF was markedly shorter for BWD than FWD swing. 3. Activity in SAa and RF was also different during FWD and BWD stance. The RF was consistently active from mid-to-late stance of FWD walking, and the SAa was also active during this period in some FWD steps. During the stance phase of BWD walking, however, the onset of activity in both muscles consistently shifted to early stance as both muscles became active just before paw contact (the E1 phase). Activity in RF consistently persisted through most of BWD stance. The duration of SAa recruitment during BWD stance was more variable across cats with offsets ranging from mid- to late stance. 4. The activation patterns of the biarticular anterior thigh muscles during stumbling corrective reactions were, in general, similar to their different activations during FWD and BWD swing. The initial response to a mechanical stimulus applied to the dorsum of the paw that obstructed FWD swing was an augmentation of knee flexion and increased activity in ST and SAm. A mechanical stimulus applied to the ventral surface of the paw to obstruct BWD swing resulted in an initial conversion of hip extension to flexion and a slowing of knee flexion. There was a corresponding recruitment of SAa and RF and an enhancement of background activity in SAm. 5. The two forms of walking are differentiated by posture and limb dynamics, yet muscles participating in the basic flexor and extensor synergies are unchanged. Although central pattern generating (CPG) circuits determine the basic timing of these synergies, changes in the duration and waveform of muscle activity may depend on unique interactions among the CPG, supraspinal inputs that set posture and the animal's goal (to walk BWD or FWD) and motion-related feedback from the hindlimb. Output mutability to each muscle may depend on the balance of this tripartite input; muscles with immutable patterns may rely heavily on input from CPG circuits, whereas muscles with mutable patterns may rely more on form-specific proprioceptive and supraspinal inputs.