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Results of previous studies raise the question of how timing neuromuscular functional electrical stimulation (FES) to limb movements during stepping might alter neuromuscular control differently than patterned stimulation alone. We have developed a prototype FES system for a rodent model of spinal cord injury (SCI) that times FES to robotic treadmill training (RTT). In this study, one group of rats (n = 6) was trained with our FES+RTT system and received stimulation of the ankle flexor (tibialis anterior [TA]) muscle timed according to robot-controlled hind-limb position (FES+RTT group); a second group (n = 5) received a similarly patterned stimulation, randomly timed with respect to the rats' hind-limb movements, while they were in their cages (randomly timed stimulation [RS] group). After 4 wk of training, we tested treadmill stepping ability and compared kinematic measures of hind-limb movement and electromyography (EMG) activity in the TA. The FES+RTT group stepped faster and exhibited TA EMG profiles that better matched the applied stimulation profile during training than the RS group. The shape of the EMG profile was assessed by "gamma," a measure that quantified the concentration of EMG activity during the early swing phase of the gait cycle. This gamma measure was 112% higher for the FES+RTT group than for the RS group. The FES+RTT group exhibited burst-to-step latencies that were 41% shorter and correspondingly exhibited a greater tendency to perform ankle flexion movements during stepping than the RS group, as measured by the percentage of time the hind limb was either dragging or in withdrawal. The results from this study support the hypothesis that locomotor training consisting of FES timed to hind-limb movement improves the activation of hind-limb muscle more so than RS alone. Our rodent FES+RTT system can serve as a tool to help further develop this combined therapy to target appropriate neurophysiological changes for locomotor control.

The effect of timing electrical stimulation to robotic-assisted stepping on neuromuscular activity and associated kinematics