Operant conditioning to increase ankle control or decrease reflex excitability improves reflex modulation and walking function in chronic spinal cord injury (original) (raw)
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Locomotor training alters the behavior of flexor reflexes during walking in human spinal cord injury
Journal of neurophysiology, 2014
In humans, a chronic spinal cord injury (SCI) impairs the excitability of pathways mediating early flexor reflexes and increases the excitability of late, long-lasting flexor reflexes. We hypothesized that in individuals with SCI, locomotor training will alter the behavior of these spinally mediated reflexes. Nine individuals who had either chronic clinically motor complete or incomplete SCI received an average of 44 locomotor training sessions. Flexor reflexes, elicited via sural nerve stimulation of the right or left leg, were recorded from the ipsilateral tibialis anterior (TA) muscle before and after body weight support (BWS)-assisted treadmill training. The modulation pattern of the ipsilateral TA responses following innocuous stimulation of the right foot was also recorded in 10 healthy subjects while they stepped at 25% BWS to investigate whether body unloading during walking affects the behavior of these responses. Healthy subjects did not receive treadmill training. We obse...
Afferent mechanisms for the reflex response to imposed ankle movement in chronic spinal cord injury
Experimental Brain Research, 2002
We have reported earlier that externally imposed ankle movements trigger ankle and hip flexion reflexes in individuals with spinal cord injury (SCI). In order to examine the afferent mechanisms underlying these movement-triggered reflexes, controlled ankle movements were imposed in 17 SCI subjects. In 13 of these subjects, reflex torques were recorded at the hip, knee and ankle in response to 5 ankle movement ranges, and 4 movement speeds. Subjects were tested using both ankle plantarflexion and dorsiflexion movements. The principal outcome measure, peak hip flexion torque of the induced reflexes, was used for comparing the effects of movement range and speed on the reflex response. We found that movement-triggered reflexes were sensitive to the angular range of ankle deflection, but insensitive to the velocity of the movement. Movement amplitudes sufficient to trigger hip and ankle flexion were routinely associated with increases in ankle passive force, suggesting that force-sensitive receptors participated in the reflex response. However, increases in angular range also corresponded to increases in muscle length, making it difficult to distinguish whether the response was triggered by a load-sensitive receptor (e.g., Golgi tendon organ or muscle free nerve ending) or a position-sensitive receptor responsive to absolute ankle angle (e.g., muscle spindle secondary afferent). The absence of velocity dependence of the reflex suggested that spindle Ia afferents were not major contributors. These results suggest movement-triggered reflexes originate in muscle receptors that are sensitive to either absolute muscle length, to muscle force or to both. Although receptors that are sensitive to absolute muscle length cannot be excluded with certainty, the finding that reflex responses require that ankle movements elicit an increase in passive force argues for a prominent role of nonspindle mechanoreceptors, such as group III/IV muscle afferents. These afferents are activated preferentially as muscles are stretched to near maximum length, and they appear to have potent reflex effects in spinal cord injury.
Reduced reciprocal inhibition during assisted stepping in human spinal cord injury
Experimental Neurology, 2011
The aim of this study was to establish the modulation pattern of the reciprocal inhibition exerted from tibialis anterior (TA) group I afferents onto soleus motoneurons during body weight support (BWS) assisted stepping in people with spinal cord injury (SCI). During assisted stepping, the soleus H-reflex was conditioned by percutaneous stimulation of the ipsilateral common peroneal nerve at one fold TA M-wave motor threshold with a single pulse delivered at a short conditioning-test interval. To counteract movement of recording and stimulating electrodes, a supramaximal stimulus at 80-100 ms after the test H-reflex was delivered. Stimuli were randomly dispersed across the step cycle which was divided into 16 equal bins. The conditioned soleus H-reflex was significantly facilitated throughout the stance phase, while during swing no significant changes on the conditioned H-reflex were observed when compared to the unconditioned soleus H-reflex recorded during stepping. Spontaneous clonic activity in triceps surae muscle occurred in multiple phases of the step cycle at a mean frequency of 7 Hz for steps with and without stimulation. This suggests that electrical excitation of TA and soleus group Ia afferents did not contribute to manifestation of ankle clonus. Absent reciprocal inhibition is likely responsible for lack of soleus H-reflex depression in swing phase observed in these patients. The pronounced reduced reciprocal inhibition in stance phase may contribute to impaired levels of co-contraction of antagonistic ankle muscles. Based on these findings, we suggest that rehabilitation should selectively target to transform reciprocal facilitation to inhibition through computer controlled reflex conditioning protocols.
Carolina Digital Repository (University of North Carolina at Chapel Hill), 2010
Spinal reflex conditioning changes reflex size, induces spinal cord plasticity, and modifies locomotion. Appropriate reflex conditioning can improve walking in rats after spinal cord injury (SCI). Reflex conditioning offers a new therapeutic strategy for restoring function in people with SCI. This approach can address the specific deficits of individuals with SCI by targeting specific reflex pathways for increased or decreased responsiveness. In addition, once clinically significant regeneration can be achieved, reflex conditioning could provide a means of re-educating the newly (and probably imperfectly) reconnected spinal cord.
Journal of Neurophysiology, 2019
Foot drop is very common among people with chronic incomplete spinal cord injury (SCI) and likely stems from SCI that disturbs the corticospinal activation of the ankle dorsiflexor tibialis anterior (TA). Thus, if one can recover or increase the corticospinal excitability reduced by SCI, motor function recovery may be facilitated. Here, we hypothesized that in people suffering from weak dorsiflexion due to chronic incomplete SCI, increasing the TA motor-evoked potential (MEP) through operant up-conditioning can improve dorsiflexion during locomotion, while in people without any injuries, it would have little impact on already normal locomotion. Before and after 24 MEP conditioning or control sessions, locomotor electromyography (EMG) and kinematics were measured. This study reports the results of these locomotor assessments. In participants without SCI, locomotor EMG activity, soleus Hoffmann reflex modulation, and joint kinematics did not change, indicating that MEP up-conditioning...
Flexion reflex modulation during stepping in human spinal cord injury
Experimental Brain Research, 2009
The Xexion reXex modulation pattern was investigated in nine people with a chronic spinal cord injury during stepping using body weight support on a treadmill and manual assistance by therapists. Body weight support was provided by an upper body harness and was adjusted for each subject to promote the best stepping pattern with the least manual assistance required by the therapists. The Xexion reXex was elicited by sural nerve stimulation with a 30 ms pulse train at 1.2-2 times the tibialis anterior reXex threshold. During stepping, stimuli were randomly dispersed across the gait cycle which was divided into 16 equal bins. A long latency (>110 ms) Xexion reXex was present in all subjects, while a short (>30 ms) and a medium latency (>70 ms) Xexion reXex were present only in three subjects. For each response, the non-stimulated EMG was subtracted from the stimulated EMG at identical time windows and bins, normalized to the maximal corresponding EMG, and signiWcant diVerences were established with a Wilcoxon rank-sum test. The long latency Xexion reXex was facilitated at late stance and during the swing-tostance transition phase. A reXex depression was present from heel strike until mid-stance and during the swing-tostance transition phase. The short and medium latency Xexion reXexes were depressed during mid-stance followed by facilitation during the stance-to-swing transition phase. Regardless of the latency, facilitatory Xexion responses during the swing phase coincided with decreased activity of ipsilateral ankle extensors. The Xexion reXex was modulated in a phase dependent manner, a behavior that was absent for the soleus H-reXex in most of these patients (Knikou et al. in Exp Brain Res 193:397-407, 2009). We propose that training should selectively target spinal reXex circuits in which extensor muscles and reXexes are involved in order to maximize sensorimotor recovery in these patients.
Journal of Neurophysiology, 2010
Knikou M. Plantar cutaneous afferents normalize the reflex modulation patterns during stepping in chronic human spinal cord injury. cutaneous afferent transmission is critical for recovery of locomotion in spinalized animals, whereas a phase-dependent reflex modulation is apparent during fictive or real locomotion. In nine people with a chronic spinal cord injury (SCI) the effects of foot sole stimulation on the soleus H-reflex and tibialis anterior (TA) flexion reflex modulation patterns during assisted stepping were established on different days. The soleus H-reflex was elicited by posterior tibial nerve stimulation followed by a supramaximal stimulus 100 ms after the test H-reflex to control for movement of recording electrodes. The flexion reflex was evoked by sural nerve stimulation with a 30-ms pulse train, recorded from the ipsilateral TA muscle, and elicited at 1.2-to twofold the reflex threshold. During assisted stepping, spinal reflexes were conditioned by percutaneous stimulation of the ipsilateral metatarsals at threefold perceptual threshold with a 20-ms pulse train delivered at 9-to 11-ms conditioning-test intervals. Stimuli were randomly dispersed across the step cycle, which was divided into 16 equal bins. The conditioned soleus H-reflex was significantly facilitated at midstance and depressed during midswing when compared with the unconditioned soleus H-reflex recorded during stepping. Foot sole stimulation induced a significant facilitation of the long-latency TA flexion reflex before, during, and after stance-to-swing transition when compared with the unconditioned long-latency TA flexion reflex during stepping. This study provides evidence that plantar cutaneous afferents remarkably influence the soleus H-reflex and TA flexion reflex modulation patterns during stepping and support that actions of plantar cutaneous afferents onto spinal interneuronal circuits engaged in locomotion are manifested in a phase-dependent manner in chronic SCI subjects.
Frontiers in Physiology, 2012
Spasticity is an important problem that complicates daily living in many individuals with spinal cord injury (SCI). While previous studies in human and animals revealed significant improvements in locomotor ability with treadmill locomotor training, it is not known to what extent locomotor training influences spasticity. In addition, it would be of considerable practical interest to know how the more ergonomically feasible cycle training compares with treadmill training as therapy to manage SCI-induced spasticity and to improve locomotor function. Thus the main objective of our present studies was to evaluate the influence of different types of locomotor training on measures of limb spasticity, gait, and reflex components that contribute to locomotion. For these studies, 30 animals received midthoracic SCI using the standard Multicenter Animal Spinal cord Injury Studies (MASCIS) protocol (10 g 2.5 cm weight drop). They were divided randomly into three equal groups: control (contused untrained), contused treadmill trained, and contused cycle trained. Treadmill and cycle training were started on post-injury day 8. Velocity-dependent ankle torque was tested across a wide range of velocities (612-49˚/s) to permit quantitation of tonic (low velocity) and dynamic (high velocity) contributions to lower limb spasticity. By post-injury weeks 4 and 6, the untrained group revealed significant velocity-dependent ankle extensor spasticity, compared to pre-surgical control values. At these post-injury time points, spasticity was not observed in either of the two training groups. Instead, a significantly milder form of velocity-dependent spasticity was detected at postcontusion weeks 8-12 in both treadmill and bicycle training groups at the four fastest ankle rotation velocities (350-612˚/s). Locomotor training using treadmill or bicycle also produced significant increase in the rate of recovery of limb placement measures (limb axis, base of support, and open field locomotor ability) and reflex rate-depression, a quantitative assessment of neurophysiological processes that regulate segmental reflex excitability, compared with those of untrained injured controls. Light microscopic qualitative studies of spared tissue revealed better preservation of myelin, axons, and collagen morphology in both locomotor trained animals. Both locomotor trained groups revealed decreased lesion volume (rostrocaudal extension) and more spared tissue at the lesion site. These improvements were accompanied by marked upregulation of BDNF, GABA/GABA b , and monoamines (e.g., norepinephrine and serotonin) which might account for these improved functions. These data are the first to indicate that the therapeutic efficacy of ergonomically practical cycle training is equal to that of the more labor-intensive treadmill training in reducing spasticity and improving locomotion following SCI in an animal model.
Spinal Cord, 2007
Study design: Spinal reflex excitability study in sensory-motor incomplete spinal cord-injured (SCI) and spinal intact subjects. Objectives: To investigate the effects of plantar cutaneous afferent excitation on the soleus H-reflex and flexion reflex in both subject groups while seated. Setting: Rehabilitation Institute of Chicago and City University of New York, USA. Methods: The flexion reflex in SCI subjects was elicited by non-nociceptive stimulation of the sural nerve. In normal subjects, it was also elicited via innocuous medial arch foot stimulation. In both cases, reflex responses were recorded from the ipsilateral tibialis anterior muscle. Soleus H-reflexes were elicited and recorded via conventional methods. Both reflexes were conditioned by plantar cutaneous afferent stimulation at conditioning test intervals ranging from 3 to 90 ms. Results: Excitation of plantar cutaneous afferents resulted in facilitation of the soleus H-reflex and late flexion reflex in SCI subjects. In normal subjects, the soleus H-reflex was depressed while the late flexion reflex was absent. The early flexion reflex was irregularly observed in SCI patients, while in normal subjects a bimodal reflex modulation pattern was observed. Conclusion: The effects of plantar cutaneous afferents change following a lesion to the spinal cord leading to exaggerated activity in both flexors and extensors. This suggests impaired modulation of the spinal inhibitory mechanisms involved in the reflex modulation. Our findings should be considered in programs aimed to restore sensorimotor function and promote recovery in these patients.
The Journal of Spinal Cord Medicine, 2001
Objective: The purpose of this study was to assess the effect of a single bout of a locomotor-training paradigm on overground walking speed and H-reflex modulation of individuals with incomplete spinal cord injury (SCI). Methods: Self-selected and maximum walking speeds and soleus H-reflexes (H/ M ratios) during standing and stance and swing phases of walking (self-selected velocity) were obtained from 4 individuals with American Spinal Injury Association impairment classification D. Data were collected immediately before and after a single bout of locomotor training with body weight support on a treadmill. The pretraining H/ M ratios of the SCI subjects were also compared with values from 4 able-bodied subjects who did not receive the intervention. Maximum H/ M ratios while standing and during midstance and midswing phases of overground walking were considerably greater in the SCI subjects than in the control subjects. Results: After the single bout of training, self-selected and maximum overground walking speeds of the subjects with SCI increased by 26% and 25%, respectively. Furthermore, H-reflexes were significantly more depressed in the SCI subjects during overground walking (28% less during stance, 34% less during swing). Conclusions: Although preliminary, these findings indicate that a single bout of locomotor training produced immediate increases in walking velocity and acute neurophysiologic changes in individuals with incomplete SCI.