Somatosensory control of balance during locomotion in decerebrated cat.

Postmammillary decerebrated cats can generate stepping on a moving treadmill belt when the brain stem or spinal cord is stimulated tonically and the hindquarters are supported both vertically and laterally. While adequate propulsion seems to be generated by the hindlimbs under these conditions, the ability to sustain equilibrium during locomotion has not been examined extensively. We found that tonic epidural spinal cord stimulation (5 Hz at L5) of decerebrated cats initiated and sustained unrestrained weight-bearing hindlimb stepping for extended periods. Detailed analyses of the relationships among hindlimb muscle EMG activity and trunk and limb kinematics and kinetics indicated that the motor circuitries in decerebrated cats actively maintain equilibrium during walking, similar to that observed in intact animals. Because of the suppression of vestibular, visual, and head-neck-trunk sensory input, balance-related adjustments relied entirely on the integration of somatosensory information arising from the moving hindquarters. In addition to dynamic balance control during unperturbed locomotion, sustained stepping could be reestablished rapidly after a collapse or stumble when the hindquarters switched from a restrained to an unrestrained condition. Deflecting the body by pulling the tail laterally induced adaptive modulations in the EMG activity, step cycle features, and left-right ground reaction forces that were sufficient to maintain lateral stability. Thus the brain stem-spinal cord circuitry of decerebrated cats in response to tonic spinal cord stimulation can control dynamic balance during locomotion using only somatosensory input.

Novel and direct access to the human locomotor spinal circuitry.

The degree of automaticity of locomotion in primates compared with other mammals remains unclear. Here, we examine the possibility for activation of the spinal locomotor circuitry in noninjured humans by spinal electromagnetic stimulation (SEMS). SEMS (3 Hz and 1.3-1.82 tesla) at the T11-T12 vertebrae induced involuntary bilateral locomotor-like movements in the legs of individuals placed in a gravity-neutral position. The formation of locomotor-like activity during SEMS started with a latency of 0.68 +/- 0.1 s after delivering the first stimulus, unlike continuous vibration of muscles, which requires several seconds. The first EMG burst in response to SEMS was observed most often in a proximal flexor muscle. We speculate that SEMS directly activates the circuitry intrinsic to the spinal cord, as suggested by the immediate response and the electrophysiological observations demonstrating an absence of strictly time-linked responses within the EMG burst associated with individual stimuli during SEMS. SEMS in the presence of vibration of the leg muscles was more effective in facilitating locomotor-like activity than SEMS alone. The present results suggest that SEMS could be an effective noninvasive clinical tool to determine the potential of an individual to recover locomotion after a spinal cord injury, as well as being an effective rehabilitation tool itself.

Propriospinal bypass of the serotonergic system that can facilitate stepping.

The neurotransmitter systems mediating spinal locomotion in response to epidural spinal cord stimulation (ES) have not been identified. Here, we examine the role of the serotonergic system in regulating locomotor behavior of decerebrated cats during ES at L4-L5. ES elicited coordinated, weight-bearing, hindlimb stepping with plantar foot placement on a moving treadmill belt. Ketanserin [a 5-hydroxytryptamine (serotonin) (5-HT)(2/7) receptor antagonist] depressed this locomotor activity: only weak rhythmic movements without plantar foot placement and depressed EMG activity were observed. Cyproheptadine, a nonselective 5-HT blocker, prevented facilitation of stepping by epidural stimulation. These data demonstrate an important role of the serotonergic system in facilitating locomotion in the presence of epidural stimulation. In the presence of ketanserin, passive movements of one forelimb in a step-like manner immediately induced stepping of both hindlimbs with EMG patterns similar to those observed with ES without ketanserin. Thus, a non-5-HT-dependent spinal circuitry projecting from the cervical to the lumbar region of the spinal cord can facilitate stepping. The specific neurotransmitters responsible for this forelimb-facilitated stepping of the hindlimbs are unknown. These data suggest that a 5-HT(2/7) receptor-dependent pathway that processes hindlimb locomotor-like proprioception to facilitate hindlimb stepping can be complemented with proprioceptive afferents from the forelimbs via a non-5-HT(2/7) receptor neurotransmitter system. Thus, different neurotransmitter receptor systems can be used to mediate the same type of sensory event, i.e., locomotor-like proprioception to facilitate the same motor task, i.e., hindlimb stepping.