Neuromotor and musculoskeletal responses to locomotor training for an individual with chronic motor complete AIS-B spinal cord injury.

BACKGROUND/OBJECTIVE: To determine the effects of locomotor training (LT) using body weight support (BWS), treadmill, and manual assistance on muscle activation, bone mineral density (BMD), and body composition changes for an individual with motor complete spinal cord injury (AIS B), 1 year after injury. METHODS: A man with chronic C6 AIS B (motor complete and sensory incomplete) spinal cord injury (SCI), 1 year after injury, completed 2 blocks of LT over a 9-month training period (35-session block followed by 8.6 weeks of no training and then a 62-session block). RESULTS: Before training, muscle activation was minimal for any muscle examined, whereas after the 2 blocks of LT (97 sessions), hip and knee muscle activation patterns for the bilateral rectus femoris, biceps femoris, and gastrocnemius were in phase with the kinematics. Mean EMG amplitude increased for all bilateral muscles and burst duration increased for rectus femoris and gastrocnemius muscles, whereas burst duration decreased for the biceps femoris after 62 LT sessions. Before LT, left biceps femoris had a pattern that reflected muscle stretch, whereas after training, muscle stretch of the left biceps femoris could not totally account for mean EMG amplitude or burst duration. After the 62 training sessions, total BMD decreased (1.54%), and regional BMD decreased (legs: 6.72%). Total weight increased, lean mass decreased (6.6%), and fat mass increased (7.4%) in the arms, whereas fat mass decreased (3.5%) and lean mass increased (4%) in the legs. CONCLUSIONS: LT can induce positive neural and body composition changes in a nonambulatory person with chronic SCI, indicating that neuromuscular plasticity can be induced by repetitive locomotor training after a motor complete SCI.

Validity of the walking scale for spinal cord injury and other domains of function in a multicenter clinical trial.

OBJECTIVE: To demonstrate criterion (concurrent and predictive) and construct validity of the Walking Index for Spinal Cord Injury (WISCI) scale and other walking measures in the Spinal Cord Injury Locomotor Trial (SCILT). DESIGN: Prospective multicenter clinical trial of a walking intervention for patients with acute traumatic spinal cord injury (SCI). PARTICIPANTS/ METHODS: Body weight-supported treadmill training was compared to overground mobility training in 146 patients with incomplete SCI (C4 to L3) enrolled within 8 weeks of onset and treated for 12 weeks. Primary outcome measures were the Functional Independence Measure (FIM), 50-foot walking speed (50FW-S), and 6-minute walking distance (6MW-D), tested 3, 6, and 12 months after entry. Secondary measures were the Lower Extremity Motor Score (LEMS), Berg Balance Scale (BBS), WISCI, and FIM locomotor score (LFIM), assessed at 6 centers by blinded observers. Data for the 2 arms were combined since no significant differences in outcomes had been found. RESULTS: Correlations with WISCI at 6 months were significant with BBS (r = .90), LEMS (r = .85), LFIM (r = .89), FIM (r = .77), 50FW-S (r = .85), and 6MW-D ( r = .79); similar correlations occurred at 3 and 12 months. Correlations of change scores from baseline WISCI were significant for change scores from baseline of LEMS/BBS/LFIM. Correlation of baseline LEMS and WISCI at 12 months were most significant (r = .73). The R(2) of baseline LEMS explained 57% of variability of WISCI levels at 3 months. CONCLUSION: Concurrent validity of the WISCI scale was supported by significant correlations with all measures at 3, 6, and 12 months. Correlation of change scores supports predictive validity. The LEMS at baseline was the best predictor of the WISCI score at 12 months and explained most of the variance, which supported both predictive and construct validity. The combination of the LEMS, BBS, WISCI, 50FW-S, and LFIM appears to encompass adequate descriptors for outcomes of walking trials for incomplete SCI.

Physical determinants, emerging concepts, and training approaches in gait of individuals with spinal cord injury.

The aim of this review is to examine the physical determinants for functional walking as well as the efficacy of gait rehabilitation after spinal cord injury (SCI) in humans. The results indicate several important physical determinants in gait. Examples are provided of different interventions that produce beneficial effects on outcome measures of gait such as gait speed, stride length, walking endurance, motor recovery, and gait quality. These findings need to be considered in current SCI rehabilitation practices, but the efficacy of certain interventions remains unclear. Well-designed clinical trials are needed to provide evidence of the role of physical determinants in the development of new concepts and principles in locomotor recovery after SCI. This review focuses on relevant literature, and informs rehabilitation specialists and basic scientists about the physical determinants and factors to consider for optimization of gait training in individuals with incomplete SCI.

Postural adaptation to walking on inclined surfaces: II. Strategies following spinal cord injury.

OBJECTIVE: To investigate the postural adaptations to inclined walking in spinal cord injured (SCI) subjects. METHODS: Eight subjects with an incomplete spinal cord injury and eight age- and sex-matched healthy control subjects walked on a treadmill at five different grades (from -10 to 10%) without any assistance. The movements of the trunk and pelvis were recorded with four high-resolution cameras. RESULTS: The SCI subjects walked with greater forward tilt of both trunk and pelvic segments during level or inclined walking and could not adapt their body orientation to the inclination of the support surface as observed in healthy control subjects. Trunk and pelvic rotations as well as lateral excursions were maintained constant during inclined walking in both groups of subjects but total excursions were always greater in the SCI subjects. CONCLUSIONS: We argue that the forward bending posture observed in SCI subjects at any treadmill grade is adopted to compensate for a certain degree of instability due to lower-limb deficits and is a postural adaptation to the daily use of ambulatory assistive devices. SIGNIFICANCE: The bent posture adopted by SCI subjects is not adequate when performing level or downhill walking and can lead to a loss of balance or a fall in these subjects.

Speed and temporal-distance adaptations during treadmill and overground walking following stroke.

OBJECTIVE: To compare the maximum gait speed of stroke subjects attained during treadmill and overground in stroke subjects and to identify the temporal-distance determinants of the maximal gait speed. METHODS: Ten individuals with hemiparetic gait deficits and whose walking speeds ranged between 0.24 m/s and 0.82 m/s participated. Five healthy age-matched controls were also tested to provide comparative data for the gait speed transfer between the 2 modes of locomotion. Following a brief habituation process to walking on the treadmill, subjects were tested while walking at comfortable and maximal speeds on the treadmill and overground, in a random order. Main Outcome Measure. Self-selected comfortable and maximum gait speed and temporal-distance factors were acquired using a 6-camera Vicontrade mark motion analysis system and compared between treadmill and overground walking at a similar speed. RESULTS: Overground walking resulted in higher maximal speeds (P < 0.001), greater stride lengths (P < 0.001), and a lower cadence (P < 0.02), as compared to tread-mill. The comfortable gait speed and the maximum stride length proved to be strong determinants for the maximal speed on both modes of locomotion (P < 0.01), but the maximum cadence was correlated to maximum speed only for overground locomotion (P < 0.05). CONCLUSIONS: Stroke subjects walked slower on the treadmill as compared to overground. They also used a different strategy to increase gait speed, relying mostly on increasing the stride length during treadmill ambulation.

Timing of cortical excitability changes during the reaction time of movements superimposed on tonic motor activity.

Seated subjects were instructed to react to an auditory cue by simultaneously contracting the tibialis anterior (TA) muscle of each ankle isometrically. Focal transcranial magnetic stimulation of the leg area of the motor cortex (MCx) was used to determine the time course of changes in motor-evoked potential amplitude (MEP) during the reaction time (RT). In one condition the voluntary contraction was superimposed on tonic EMG activity maintained at 10% of maximal voluntary contraction. In the other condition the voluntary contraction was made starting from rest. MEPs in the TA contralateral to the stimulation coil were evoked at various times during the RT in each condition. These were compared to the control MEPs evoked during tonic voluntary activity or with the subject at rest. The RT was measured trial by trial from the EMG activity of the TA ipsilateral to the magnetic stimulus, taking into account the nearly constant time difference between the two sides. The MEPs became far greater than control MEPs during the RT (mean = 332%, SD = 44 %, of control MEPs, P < 0.001) without any measurable change in the background level of EMG activity. The onset of this facilitation occurred on average 12.80 ms (SD = 7.55 ms) before the RT. There was no difference in the onset of facilitation between the two conditions. Because MEPs were facilitated without a change in the background EMG activity, it is concluded that this facilitation is specifically due to an increase of MCx excitability just before voluntary muscle activation. This conclusion is further reinforced by the observation that MEPs evoked by near-threshold anodal stimuli to the MCx were not facilitated during the RT, in contrast to those evoked by near-threshold transcranial magnetic stimulation. However, several observations in the present and previous studies indicate that MEP amplitude may be more sensitive to alpha-motoneuron activity than to motor cortical neuron activity, an idea that has important methodological implications.

Kinematic adaptations of spinal cord-injured subjects during obstructed walking.

STUDY DESIGN: A case-control study of walking over obstacles. OBJECTIVE: To characterize and compare the kinematic, anticipatory locomotor adjustments used by people with incomplete spinal cord injuries (SCIs). METHODS: The angular and linear kinematics of the lower limb when going over obstacles of low height (0.005 and 0.030 m) were compared between SCI subjects (n = 6) and able-bodied participants (n = 5). RESULTS: The results of this study show that even though SCI participants could adapt their kinematic patterns to go over obstacles, none of the participants used kinematic strategies similar to those of able-bodied participants. CONCLUSIONS: This difference could be explained in part by the absence in the SCI participants of increased hip flexion when going over the obstacles. Other confounding factors are discussed.

Methods for a randomized trial of weight-supported treadmill training versus conventional training for walking during inpatient rehabilitation after incomplete traumatic spinal cord injury.

The authors describe the rationale and methodology for the first prospective, multicenter, randomized clinical trial (RCT) of a task-oriented walking intervention for subjects during early rehabilitation for an acute traumatic spinal cord injury (SCI). The experimental strategy, body weight-supported treadmill training (BWSTT), allows physical therapists to systematically train patients to walk on a treadmill at increasing speeds typical of community ambulation with increasing weight hearing. The therapists provide verbal and tactile cues to facilitate the kinematic, kinetic, and temporal features of walking. Subjects were randomly assigned to a conventional therapy program for mobility versus the same intensity and duration of a combination of BWSTT and over-ground locomotor retraining. Subjects had an incomplete SCI (American Spinal Injury Association grades B, C, and D) from C-4 to T-10 (upper motoneuron group) or from T-11 to L-3 (lower motoneuron group). Within 8 weeks of a SCI, 146 subjects were entered for 12 weeks of intervention. The 2 single-blinded primary outcome measures are the level of independence for ambulation and, for those who are able to walk, the maximal speed for walking 50 feet, tested 6 and 12 months after randomization. The trial's methodology offers a model for the feasibility of translating neuroscientific experiments into a RCT to develop evidence-based rehabilitation practices.

The effects of long-term FES-assisted walking on intrinsic and reflex dynamic stiffness in spastic spinal-cord-injured subjects.

The effects of long-term functional electrical stimulation (FES)-assisted walking on ankle dynamic stiffness were examined in spinal cord-injured (SCI) subjects with incomplete motor function loss. A parallel-cascade system identification method was used to identify intrinsic and reflex contributions to dynamic ankle stiffness at different ankle positions while subjects remained relaxed. Intrinsic stiffness dynamics were well modeled by a linear second-order model relating intrinsic torque to joint position. Reflex stiffness dynamics were accurately described by a linear third-order model relating halfwave rectified velocity to reflex torque. We examined four SCI subjects before and after long-term FES-assisted walking (> 16 mo). Another SCI subject, who used FES for only five months was examined 12 mo latter to serve as a non-FES, SCI control. Reflex stiffness decreased in FES subjects by an average of 53% following FES-assisted walking, intrinsic stiffness also dropped by 45%. In contrast, both reflex and intrinsic stiffness increased in the non-FES, SCI control. These findings suggest that FES-assisted walking may have therapeutic effects, helping to reduce abnormal joint stiffness.

Postural adaptation to walking on inclined surfaces: I. Normal strategies.

This study investigated the postural strategies to adapt to uphill and downhill treadmill inclination (0, 5 and 10%) during walking and standing in eight healthy subjects. Increasing the treadmill grade from 0 to 10% induced an increasingly flexed posture of the hip, knee and ankle at initial foot contact as well as a progressive forward tilt of pelvis and trunk. These postural changes were accompanied by a progressive decrease in pelvic lateral drop toward the swinging limb and a gradual increase in stride length as the uphill slope became steeper. Decreasing the treadmill grade from 0 to -10% lead to a decreasingly flexed posture of the hip at initial foot contact as well as an increase in knee flexion during weight acceptance and late stance. These changes were accompanied by a gradual decrease in stride length, a progressive backward tilt of trunk and pelvis and an increase in pelvic lateral drop toward the swinging limb as downhill slope became steeper. Changes in trunk and pelvic postural alignment in the sagittal plane might be used to facilitate power generation or absorption in adapting to slope changes during walking. During quiet standing, however, the trunk and pelvis remained aligned with respect to earth's vertical at any surface inclination. These results showed that postural adaptations are task-specific and the control requirements are different between standing and walking on an inclined surface.

Evidence-based therapy for recovery of function after spinal cord injury.

Physical rehabilitation for individuals coping with neurological deficits is evolving in response to a paradigm shift in thinking about the injured nervous system and using evidence as a basis for clinical decisions. Functional recovery from paralysis was generally believed to be nearly impossible, based on traditional expert opinion, and the priority was to develop compensation strategies to achieve functional goals in the home and community. Research, which began in animal models of neurological insult and is currently being translated to the clinic, has challenged these assumptions. The nervous system, whether intact or injured, has enormous potential for adaptation and modification, which can be harnessed to facilitate recovery. In this chapter we will briefly outline the history of physical rehabilitation as it concerns the development of strategies aimed at compensation, rather than functional recovery. Then we will discuss how new activity-based therapies are being developed, based on evidence from basic science and clinical evidence. One of these activity-based therapies is locomotor training, a program which relies on the intrinsic, automatic, control of locomotion by "lower" neural centers. A brief description of the program, including the four foundational principles, will be followed by an introduction to the use of robotics in these programs. Finally, we will discuss a second activity-based therapy, functional electrical stimulation (FES), and the future of physical rehabilitation for spinal cord injury and other neurological disorders.

Arm and leg coordination during treadmill walking in individuals with motor incomplete spinal cord injury: a preliminary study.

Arm and leg coordination naturally emerges during walking, but can be affected by stroke or Parkinson's disease. The purpose of this preliminary study was to characterize arm and leg coordination during treadmill walking at self-selected comfortable walking speeds (CWSs) in individuals using arm swing with motor incomplete spinal cord injury (iSCI). Hip and shoulder angle cycle durations and amplitudes, strength of peak correlations between contralateral hip and shoulder joint angle time series, the time shifts at which these peak correlations occur, and associated variability were quantified. Outcomes in individuals with iSCI selecting fast CWSs (range, 1.0-1.3m/s) and speed-matched individuals without neurological injuries are similar. Differences, however, are detected in individuals with iSCI selecting slow CWSs (range, 0.25-0.65 m/s) and may represent compensatory strategies to improve walking balance or forward propulsion. These individuals elicit a 1:1, arm:leg frequency ratio versus the 2:1 ratio observed in non-injured individuals. Shoulder and hip movement patterns, however, are highly reproducible (coordinated) in participants with iSCI, regardless of CWS. This high degree of inter-extremity coordination could reflect an inability to modify a single movement pattern post-iSCI. Combined, these data suggest inter-extremity walking coordination may be altered, but is present after iSCI, and therefore may be regulated, in part, by neural control.

Chapter 16--spinal plasticity in the recovery of locomotion.

Locomotion is a very robust motor pattern which can be optimized after different types of lesions to the central and/or peripheral nervous system. This implies that several plastic mechanisms are at play to re-express locomotion after such lesions. Here, we review some of the key observations that helped identify some of these plastic mechanisms. At the core of this plasticity is the existence of a spinal central pattern generator (CPG) which is responsible for hindlimb locomotion as observed after a complete spinal cord section. However, normally, the CPG pattern is adapted by sensory inputs to take the environment into account and by supraspinal inputs in the context of goal-directed locomotion. We therefore also review some of the sensory and supraspinal mechanisms involved in the recovery of locomotion after partial spinal injury. We particularly stress a recent development using a dual spinal lesion paradigm in which a first partial spinal lesion is made which is then followed, some weeks later, by a complete spinalization. The results show that the spinal cord below the spinalization has been changed by the initial partial lesion suggesting that, in the recovery of locomotion after partial spinal lesion, plastic mechanisms within the spinal cord itself are very important.

Optimal outcomes obtained with body-weight support combined with treadmill training in stroke subjects.

OBJECTIVES: To identify stroke patients who are most likely to benefit from locomotor training with body-weight support (BWS), to determine the extent of carryover from treadmill training to overground locomotion, and to determine the variables that are most likely to influence the recovery of locomotion. DESIGN: A randomized clinical trial. SETTING: Inpatient rehabilitation hospital. PARTICIPANTS: Of 100 stroke subjects, 50 were randomized to receive locomotor training with BWS (BWS group), and 50 were randomized to receive locomotor training with full weight bearing (no-BWS group). The subjects were stratified according to their initial overground walking speed and endurance, initial treadmill speed and endurance, functional balance, motor recovery, side of the lesion, and age. INTERVENTION: Fifty subjects were trained to walk on a treadmill with up to 40% of their body weight supported by a BWS system with an overhead harness (BWS group), and 50 subjects were trained to walk while bearing their full weight (no-BWS group). MAIN OUTCOME MEASURES: Clinical outcome measures included overground walking speed and endurance, functional balance, and motor recovery. The effect of confounding variables such as age, comorbidity, and depression on locomotor outcome was also investigated. RESULTS: After 6 weeks of locomotor training, the BWS group scored significantly higher in all clinical outcomes. When the subjects were stratified according to their initial overground walking speed, endurance, balance, and motor recovery, a significant statistical difference in gait and balance dysfunction of all outcomes occurred in the more severely impaired subjects. An important transfer from treadmill speed to overground walking speed was observed in subjects in the BWS group. Finally, a significantly greater effect was observed in older subjects (65-85y) in the BWS group. CONCLUSIONS: Retraining gait in severely impaired stroke subjects with a percentage of their body weight supported resulted in better walking and postural abilities than did gait training in patients bearing their full weight. It appears that subjects with greater gait impairments benefited the most from training with BWS, as did the older patients with stroke. There is evidence of transfer from treadmill training to overground locomotion.

The effect of locomotor training combined with functional electrical stimulation in chronic spinal cord injured subjects: walking and reflex studies.

With the new developments in traumatology medicine, the majority of spinal cord injuries sustained are clinically incomplete and the proportion is likely to continue to rise. Thus, it is necessary to continue to develop new treatment and rehabilitation strategies and understand the factors that can enhance recovery of walking following spinal cord injury (SCI). One new development is the use of functional electrical stimulation (FES) device to assist locomotion. The objective of this review is to present findings from some recent studies on the effect of long-term locomotor training with FES in subjects with SCI. Promising results are shown in all outcome measures of walking, such as functional mobility, speed, spatio-temporal parameters, and the physiological cost of walking. Furthermore, the change in the walking behavior could be associated with plasticity in the CNS organization, as seen by the modification of the stretch reflex and changes in the corticospinal projection to muscles of the lower leg. In conclusion, recovery of walking is an increasing possibility for a large number of people with SCI. New modalities of treatment have become available for this population but most still need to be evaluated for their efficacy. This review has focused on FES assisted walking as a therapeutic modality in subjects with chronic SCI, but it is envisaged that the care and recovery of SCI in the early phase of recovery could also be improved.

Effects of intrathecal glutamatergic drugs on locomotion. II. NMDA and AP-5 in intact and late spinal cats.

In a previous article, we have shown that, in cats, intrathecal injections of N-methyl-D-aspartate (NMDA) in the first few days after spinalization at T13 do not induce locomotion as in many other spinal preparations. This is in contrast to alpha-2 noradrenergic receptor stimulation, which can trigger locomotion at this early stage. However, it is known that spinal cats do recover spontaneous locomotion in the absence of descending noradrenergic pathways and that the spinal pattern generator must then depend on other neurotransmitters still present in the cord such as excitatory amino acids. In the present paper, therefore we look at the effects of intrathecal NMDA, a glutamatergic agonist, and 2-amino-5-phosphonovaleric acid (AP-5), an NMDA receptor blocker, in both intact and late spinal cats. Low doses of NMDA had no major effect on the locomotor pattern in both intact and late spinal cats. Larger doses of NMDA in the chronic spinal cat initially produced an increase in the general excitability followed by more regular locomotion. AP-5 in intact cats caused a decrease in the amplitude of the flexion reflex and induced a bilateral foot drag as well as some decrease in weight support but it did not prevent locomotion. However, in late spinal cats, the same dose of AP-5 blocked locomotion completely. These results indicate that NMDA receptors may be critical for the spontaneous expression of spinal locomotion. It is proposed that the basic locomotor rhythmicity in cats is NMDA-dependent and that normally this glutamatergic mechanism is modulated by other neurotransmitters, such as 5-HT and NA.

Effects of intrathecal glutamatergic drugs on locomotion I. NMDA in short-term spinal cats.

Excitatory amino acids (EAA) have been reported to induce fictive locomotion in different in vitro and in vivo preparations in a variety of species through their actions on both N-methyl-D-aspartate (NMDA), and non-NMDA receptors. NMDA-induced intrinsic membrane properties such as intrinsic motoneuronal membrane oscillations and plateau potentials have been suggested to play a role in the generation of locomotion. There is, however, no information on the ability of NMDA in triggering spinal locomotion in awake behaving animals. Because most of the previous work on the induction of locomotion has concentrated on monoaminergic drugs, mainly noradrenergic drugs, the aim of this study is to examine the potential of NMDA in initiating locomotion in chronic spinal cats within the first week after spinalization. Five cats chronically implanted with an intrathecal cannula and electromyographic (EMG) electrodes were used. EMG activity synchronized to video images of the hindlimbs were recorded. The results show that during the early posttransection period (within the 1st week postspinalization), NMDA did not trigger robust locomotion as did noradrenergic drugs. The predominant effects of NMDA were a general hyperexcitability reflected by fast tremor, toe fanning, and an increase in small alternating hindlimb movements with no foot placement nor weight support. During the intermediate phase posttransection (6-8 days), when the cats were able to make some rudimentary steps with foot placement, NMDA significantly enhanced the locomotor performance, which lasted for 24-72 h postinjection. NMDA was also found to increase the excitability of the cutaneous reflex transmission only in early spinal cats. One possible hypothesis for the ineffectiveness of NMDA in triggering locomotion in early spinal cats could be attributed to the widespread activation of NMDA receptors on various neuronal elements involved in the transmission of afferent pathways that in turn may interfere with the expression of locomotion. The marked effects of NMDA in intermediate-spinal cats suggest that NMDA receptors play an important role in locomotion perhaps through its role on intrinsic membrane properties of neurons in shaping and amplifying spinal neuronal transmission or by augmenting the sensory afferent inputs. The long-term effects mediated by NMDA receptors have been reported in the literature and may involve mechanisms such as induction of long-term potentiation or interactions with neuropeptides. The effects of NMDA injection in intact cats and long-term chronic spinal cats will be addressed in a forthcoming companion paper.