Inhibition and Facilitation of the Spinal Locomotor Central Pattern Generator and Reflex Circuits by Somatosensory Feedback From the Lumbar and Perineal Regions After Spinal Cord Injury

Somatosensory feedback from peripheral receptors dynamically interacts with networks located in the spinal cord and brain to control mammalian locomotion. Although somatosensory feedback from the limbs plays a major role in regulating locomotor output, those from other regions, such as lumbar and perineal areas also shape locomotor activity. In mammals with a complete spinal cord injury, inputs from the lumbar region powerfully inhibit hindlimb locomotion, while those from the perineal region facilitate it. Our recent work in cats with a complete spinal cord injury shows that they also have opposite effects on cutaneous reflexes from the foot. Lumbar inputs increase the gain of reflexes while those from the perineal region decrease it. The purpose of this review is to discuss how somatosensory feedback from the lumbar and perineal regions modulate the spinal locomotor central pattern generator and reflex circuits after spinal cord injury and the possible mechanisms involved. We also discuss how spinal cord injury can lead to a loss of functional specificity through the abnormal activation of functions by somatosensory feedback, such as the concurrent activation of locomotion and micturition. Lastly, we discuss the potential functions of somatosensory feedback from the lumbar and perineal regions and their potential for promoting motor recovery after spinal cord injury.

Compression socks enhance sensory feedback to improve standing balance reactions and reflex control of walking

Background Compression garments are generally used for their potential benefits in exercise performance and post-exercise recovery. Previous studies show that compression sleeves worn at the elbow change neuromuscular control and improve performance during reaching movement. Cutaneous stimulation of the foot skin produces location-specific reflexes in the lower limb that guide foot placement during locomotion. However, it is not clear whether enhancement of sensory feedback with compression socks can alter the neuromuscular excitability of muscles in the leg and amplify balance performance and walking. The current project aimed to determine whether enhanced sensory input from wearing compression socks could affect: 1) spinal cord excitability (as measured by cutaneous reflexes from stimulation at the top or bottom of the foot during locomotion); 2) static balance performance; and, 3) dynamic balance performance following virtual perturbations. Methods Twelve participants completed walking and balance tasks wearing four types of garments: 1) non-compression (control) socks; 2) ankle compression socks; 3) calf-compression socks; and, 4) customized ankle sleeves. During walking, electrical stimulations were delivered to three discrete locations on the dorsal (ankle crease, forefoot medial) and plantar (forefoot medial) surfaces of the foot in separate trials with each garment. Electromyography of ankle dorsiflexor tibialis anterior, plantarflexor medial gastrocnemius and evertor peroneus longus were measured bilaterally along with kinematic data from knee and ankle and kinetics under the right (stimulated) foot. Results Compared to control socks, altered cutaneous reflexes and biomechanical responses were observed in all the conditions during walking. In dynamic balance tests, time and integrated EMG for recovering from virtual perturbation were significantly reduced when wearing calf compression socks and the ankle sleeve. Conclusions Our findings suggest sensory enhancement from compression garments modifies spinal cord excitability during walking and improves performance in balance recovery after virtual perturbation.

Indirect Vibration of the Upper Limbs Alters Transmission Along Spinal but Not Corticospinal Pathways

The use of upper limb vibration (ULV) during exercise and rehabilitation continues to gain popularity as a modality to improve function and performance. Currently, a lack of knowledge of the pathways being altered during ULV limits its effective implementation. Therefore, the aim of this study was to investigate whether indirect ULV modulates transmission along spinal and corticospinal pathways that control the human forearm. All measures were assessed under CONTROL (no vibration) and ULV (30 Hz; 0.4 mm displacement) conditions while participants maintained a small contraction of the right flexor carpi radialis (FCR) muscle. To assess spinal pathways, Hoffmann reflexes (H-reflexes) elicited by stimulation of the median nerve were recorded from FCR with motor response (M-wave) amplitudes matched between conditions. An H-reflex conditioning paradigm was also used to assess changes in presynaptic inhibition by stimulating the superficial radial (SR) nerve (5 pulses at 300Hz) 37 ms prior to median nerve stimulation. Cutaneous reflexes in FCR elicited by stimulation of the SR nerve at the wrist were also recorded. To assess corticospinal pathways, motor evoked potentials (MEPs) elicited by transcranial magnetic stimulation of the contralateral motor cortex were recorded from the right FCR and biceps brachii (BB). ULV significantly reduced H-reflex amplitude by 15.7% for both conditioned and unconditioned reflexes (24.0 ± 15.7 vs. 18.4 ± 11.2% Mmax; p < 0.05). Middle latency cutaneous reflexes were also significantly reduced by 20.0% from CONTROL (−1.50 ± 2.1% Mmax) to ULV (−1.73 ± 2.2% Mmax; p < 0.05). There was no significant effect of ULV on MEP amplitude (p > 0.05). Therefore, ULV inhibits cutaneous and H-reflex transmission without influencing corticospinal excitability of the forearm flexors suggesting increased presynaptic inhibition of afferent transmission as a likely mechanism. A general increase in inhibition of spinal pathways with ULV may have important implications for improving rehabilitation for individuals with spasticity (SCI, stroke, MS, etc.).

Indirect Vibration of the Upper Limbs Alters Transmission Along Spinal but not Corticospinal Pathways

The aim of this study was to investigate whether indirect upper limb vibration (ULV) modulates transmission along spinal and corticospinal pathways that control the human forearm. All measures were assessed under CONTROL (no vibration) and ULV (30 Hz; 0.4 mm displacement) conditions while participants maintained a small contraction of the right flexor carpi radialis (FCR) muscle. To assess spinal pathways, Hoffmann reflexes (H-reflexes) elicited by stimulation of the median nerve were recorded from FCR with motor response (M-wave) amplitudes matched between conditions. An H-reflex conditioning paradigm was also used to assess changes in presynaptic inhibition by stimulating the superficial radial (SR) nerve (5 pulses at 300Hz) 37 ms prior to median nerve stimulation. Cutaneous reflexes in FCR elicited by stimulation of the SR nerve at the wrist were also recorded. To assess corticospinal pathways, motor evoked potentials (MEPs) elicited by transcranial magnetic stimulation of the contralateral motor cortex were recorded from the right FCR and biceps brachii (BB). ULV significantly reduced H-reflex amplitude by 15.7% for both conditioned and unconditioned reflexes (24.0±15.7 vs 18.4±11.2 % Mmax; p<0.05). Middle latency cutaneous reflexes were also significantly reduced by 20.0% from CONTROL (−1.50 ± 2.1 % Mmax) to ULV (−1.73 ± 2.2 % Mmax; p<0.05). There was no significant effect of ULV on MEP amplitude (p>0.05). Therefore, ULV inhibits cutaneous and H-reflex transmission without influencing corticospinal excitability of the forearm flexors suggesting increased presynaptic inhibition of afferent transmission as a likely mechanism. A general increase in inhibition of spinal pathways with ULV may have important implications for improving rehabilitation for individuals with spasticity (SCI, stroke, MS, etc).

Cutaneous inputs from perineal region facilitates and modulates spinal locomotor activity and reduces cutaneous reflexes from the foot in spinal cats

It is well known that mechanically stimulating the perineal region potently facilitates hindlimb locomotion and weight support in mammals with a spinal transection (spinal mammals). However, how perineal stimulation mediates this excitatory effect is poorly understood. We evaluated the effect of mechanically stimulating (vibration or pinch) the perineal region on ipsilateral (9-14 ms onset) and contralateral (14-18 ms onset) short-latency cutaneous reflex responses evoked by electrically stimulating the superficial peroneal or distal tibial nerve in seven adult spinal cats where hindlimb movement was restrained. Cutaneous reflexes were evoked before, during, and after mechanical stimulation of the perineal region. We found that vibration or pinch of the perineal region effectively triggered rhythmic activity, unilateral and bilateral to nerve stimulation. When electrically stimulating nerves, adding perineal stimulation modulated rhythmic activity by decreasing cycle and burst durations and by increasing the amplitude of flexors and extensors. Perineal stimulation also disrupted the timing of the ipsilateral rhythm, which had been entrained by nerve stimulation. Mechanically stimulating the perineal region decreased ipsilateral and contralateral short-latency reflex responses evoked by cutaneous inputs, a phenomenon we observed in muscles crossing different joints and located in different limbs. The results suggest that the excitatory effect of perineal stimulation on locomotion and weight support is not mediated by increasing cutaneous reflex gain and instead points to an excitation of central pattern-generating circuitry. Our results are consistent with a state-dependent modulation of reflexes by spinal interneuronal circuits.Significance StatementMechanically stimulating the skin of the perineal region strongly facilitates hindlimb locomotion in mammals following a complete spinal cord injury (SCI). Despite its remarkable effectiveness in promoting hindlimb locomotion in spinal cord-injured mammals, we do not know how this is mediated. The present study provides data on how inputs from the perineal region interact with neuronal circuits that generate locomotor-like activity and reflexes from the foot. A better understanding of how inputs from the perineal region interact with neuronal circuits of the spinal cord could lead to non-invasive approaches to restore walking in people with SCI.

Plantarflexion force is amplified with sensory stimulation during ramping submaximal isometric contractions

Stimulating cutaneous nerves, causing tactile sensations, reduces the perceived heaviness of an object, suggesting that either descending commands are facilitated or the perception of effort is reduced when tactile sensation is enhanced. Sensory stimulation can also mitigate decrements in motor output and spinal cord excitability that occur with fatigue. The effects of sensory stimulation applied with coincident timing of voluntary force output, however, are yet to be examined. Therefore, the purpose of this study was to examine effects of sensory enhancement to nerves innervating opposed skin areas of the foot (top or bottom) on force production during voluntary plantarflexion or dorsiflexion contractions. Stimulation trains were applied for 2 s at either a uniform 150 Hz or a modulated frequency that increased linearly from 50 to 150 Hz and were delivered at the initiation of the contraction. Participants were instructed to perform a ramp contraction [~10% maximal voluntary contraction (MVC)/s] to ~20% MVC and then to hold ~20% MVC for 2 s while receiving real-time visual feedback. Cutaneous reflexes were evoked 75 ms after initiating the hold (75 ms after sensory enhancement ended). Force output was greater for all sensory-enhanced conditions compared with control during plantarflexion; however, force output was not amplified during dorsiflexion. Cutaneous reflexes evoked after sensory enhancement were unaltered. These results indicate that sensory enhancement can amplify plantarflexion but not dorsiflexion, likely as a result of differences in neuroanatomical projections to the flexor and extensor motor pools. Further work is required to elucidate the mechanisms of enhanced force during cutaneous stimulation. NEW & NOTEWORTHY The efficacy of behaviorally timed sensory stimulation to enhance sensations and amplify force output has not been examined. Here we show cutaneous nerve sensory stimulation can amplify plantarflexion force output. This amplification in force occurs irrespective of whether the cutaneous field that is stimulated resides on the surface that is producing the force or the opposing surface. This information may provide insights for the development of technologies to improve performance and/or rehabilitation training.