Sensory perturbations from hindlimb cutaneous afferents generate coordinated functional responses in all four limbs during locomotion in intact cats.

Coordinating the four limbs is an important feature of terrestrial mammalian locomotion. When the foot dorsum contacts an obstacle, cutaneous mechanoreceptors send afferent signals to the spinal cord to elicit coordinated reflex responses in the four limbs to ensure dynamic balance and forward progression. To determine how the locomotor pattern of all four limbs changes in response to a sensory perturbation evoked by activating cutaneous afferents from one hindlimb, we electrically stimulated the superficial peroneal nerve with a relatively long train at four different phases (mid-stance, stance-to-swing transition, mid-swing, and swing-to-stance transition) of the hindlimb cycle in seven adult cats. The largest functional effects of the stimulation were found at mid-swing and at the stance-to-swing transition with several changes in the ipsilateral hindlimb, such as increased activity in muscles that flex the knee and hip joints, increased joint flexion and toe height, increased stride/step lengths and increased swing duration. We also observed several changes in support periods to shift support from the stimulated hindlimb to the other three limbs. The same stimulation applied at mid-stance and the swing-to-stance transition produced more subtle changes in the pattern. We observed no changes in stride and step lengths in the ipsilateral hindlimb with stimulation in these phases. We did observe some slightly greater flexions at the knee and ankle joints with stimulation at mid-stance and a reduction in double support periods and increase in triple support. Our results show that correcting or preventing stumbling involves functional contributions from all four limbs. Significance Statement The skin contains mechanoreceptors that, when activated, send afferent signals to the spinal cord, signaling a perturbation. For example, when the foot dorsum hits an obstacle during the swing phase, cutaneous inputs trigger a functional reflex response in all four limbs to rapidly move the leg away from and over the stimulus or obstacle to ensure dynamic balance and forward progression. Here, we investigate the locomotor pattern of all four limbs after cutaneous nerve stimulation of one hindpaw at four different phases of the step cycle during quadrupedal treadmill locomotion. Functionally, stimulating cutaneous afferents innervating the foot dorsum generates functional responses involving the whole-body. These responses are phase-dependent and serve to correct or prevent stumbling.