Non-patterned electrical stimulation of the posterior structures of the lumbar spinal cord in subjects with complete, long-standing spinal cord injury, can induce patterned, locomotor-like activity. We show that epidural spinal cord stimulation can elicit step-like EMG activity and locomotor synergies in paraplegic subjects. An electrical train of stimuli applied over the second lumbar segment with a frequency of 25 to 60 Hz and an amplitude of 5-9 V was effective in inducing rhythmic, alternating stance and swing phases of the lower limbs. This finding suggests that spinal circuitry in humans has the capability of generating locomotor-like activity even when isolated from brain control, and that externally controlled sustained electrical stimulation of the spinal cord can replace the tonic drive generated by the brain.
Motor responses evoked by stimulating the spinal cord percutaneously between the T11 and T12 spinous processes were studied in eight human subjects during walking and running. Stimulation elicited responses bilaterally in the biceps femoris, vastus lateralis, rectus femoris, medial gastrocnemius, soleus, tibialis anterior, extensor digitorum brevis and flexor digitorum brevis. The evoked responses were consistent with activation of Ia afferent fibres through monosynaptic neural circuits since they were inhibited when a prior stimulus was given and during tendon vibration. Furthermore, the soleus motor responses were inhibited during the swing phase of walking as observed for the soleus H-reflex elicited by tibial nerve stimulation. Due to the anatomical site and the fibre composition of the peripheral nerves it is difficult to elicit H-reflex in leg muscles other than the soleus, especially during movement. In turn, the multisegmental monosynaptic responses (MMR) technique provides the opportunity to study modulation of monosynaptic reflexes for multiple muscles simultaneously. Phase-dependent modulation of the MMR amplitude throughout the duration of the gait cycle period was observed in all muscles studied. The MMR amplitude was large when the muscle was activated whereas it was generally reduced, or even suppressed, when the muscle was quiescent. However, during running, there was a systematic anticipatory increase in the amplitude of the MMR at the end of swing in all proximal and distal extensor muscles. The present findings therefore suggest that there is a general control scheme by which the transmission in the monosynaptic neural circuits is modulated in all leg muscles during stepping so as to meet the requirement of the motor task.
An increasing number of studies supports the view that transcutaneous electrical stimulation of the spinal cord (TESS) promotes functional recovery in humans with spinal cord injury (SCI). However, the neural mechanisms contributing to these effects remain poorly understood. Here we examined motor-evoked potentials in arm muscles elicited by cortical and subcortical stimulation of corticospinal axons before and after 20 min of TESS (30 Hz pulses with a 5 kHz carrier frequency) and sham-TESS applied between C5 and C6 spinous processes in males and females with and without chronic incomplete cervical SCI. The amplitude of subcortical, but not cortical, motorevoked potentials increased in proximal and distal arm muscles for 75 min after TESS, but not sham-TESS, in control subjects and SCI participants, suggesting a subcortical origin for these effects. Intracortical inhibition, elicited by paired stimuli, increased after TESS in both groups. When TESS was applied without the 5 kHz carrier frequency both subcortical and cortical motor-evoked potentials were facilitated without changing intracortical inhibition, suggesting that the 5 kHz carrier frequency contributed to the cortical inhibitory effects. Hand and arm function improved largely when TESS was used with, compared with without, the 5 kHz carrier frequency. These novel observations demonstrate that TESS influences cortical and spinal networks, having an excitatory effect at the spinal level and an inhibitory effect at the cortical level. We hypothesized that these parallel effects contribute to further the recovery of limb function following SCI.
We investigated the role of afferent information during recovery of coordinated rhythmic activity of the hindlimbs in rats with a complete spinal cord section (approximately T8) and unilateral deafferentation (T12-S2) to answer the following questions: (1) Can bilateral stepping be generated with only afferent projections intact on one side? (2) Can the sensory input from the non-deafferented side compensate for the loss of the afferent input from the deafferented side through the crossed connections within the lumbosacral spinal cord? (3) Which afferent projections to the spinal cord from the non-deafferented side predominantly mediate the effect of epidural stimulation to facilitate stepping? Recovery of stepping ability was tested under the facilitating influence of epidural stimulation at the S1 spinal segment, or epidural stimulation plus quipazine, a 5-HT agonist. All chronic spinal rats were able to generate stepping-like patterns on a moving treadmill on the non-deafferented, but not deafferented, side from 3 to 7 weeks after surgery when facilitated by epidural stimulation. Adaptation to the loss of unilateral afferent input was evident at 7 weeks after surgery, when some movements occurred on the deafferented side. Spinal-cord-evoked potentials were observed on both sides, although middle (monosynaptic) and late (long latency) responses were more prominent on the non-deafferented side. The afferent information arising from the non-deafferented side, however, eventually could mediate limited restoration of hindlimb movements on the deafferented side. These data suggest that facilitation of stepping with epidural stimulation is mediated primarily through ipsilateral afferents that project to the locomotor networks.
A new method for the activation of spinal locomotor networks (SLN) in humans by transcutane ous electrical spinal cord stimulation (tESCS) has been described. The tESCS applied in the region of the T11-T12 vertebrae with a frequency of 5-40 Hz elicited involuntary step like movements in healthy subjects with their legs suspended in a gravity neutral position. The amplitude of evoked step like movements increased with increasing tESCS frequency. The frequency of evoked step like movements did not depend on the frequency of tESCS. It was shown that the hip, knee, and ankle joints were involved in the evoked move ments. It has been suggested that tESCS activates the SPG (SLN) through in part, via the dorsal roots that enter the spinal cord. tESCS can be used as a noninvasive method in rehabilitation of spinal pathology.
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.
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