Jaak Duysens

Neural control of locomotion; part 1: the central pattern generator from cats to humans

Abstract In the last years it has become possible to regain some locomotor activity in patients suffering from an incomplete spinal cord injury (SCI) through intense training on a treadmill. The ideas behind this approach owe much to insights derived from animal studies. Many studies showed that cats with complete spinal cord transection can recover locomotor function. These observations were at the basis of the concept of the central pattern generator (CPG) located at spinal level. The evidence for such a spinal CPG in cats and primates (including man) is reviewed in part 1, with special emphasis on some very recent developments which support the view that there is a human spinal CPG for locomotion.

A new method to normalize plantar pressure measurements for foot size and foot progression angle

Plantar pressure measurement provides important information about the structure and function of the foot and is a helpful tool to evaluate patients with foot complaints. In general, average and maximum plantar pressure of 6-11 areas under the foot are used to compare groups of subjects. However, masking the foot means a loss of important information about the plantar pressure distribution pattern. Therefore, the purpose of this study was to develop and test a simple method that normalizes the plantar pressure pattern for foot size, foot progression angle, and total plantar pressure. Moreover, scaling the plantar pressure to a standard foot opens the door for more sophisticated analysis techniques such as pattern recognition and machine learning. Twelve subjects walked at preferred and half of the preferred walking speed over a pressure plate. To test the method, subjects walked in a straight line and in an approaching angle of approximately 40 degrees . To calculate the normalized foot, the plantar pressure pattern was rotated over the foot progression angle and normalized for foot size. After normalization, the mean shortest distance between the contour lines of straight walking and walking at an angle had a mean of 0.22 cm (SD: 0.06 cm) for the forefoot and 0.14 cm (SD: 0.06 cm) for the heel. In addition, the contour lines of normalized feet for the various subjects were almost identical. The proposed method appeared to be successful in aligning plantar pressure of various feet without losing information.

Feasibility of measuring event Related Desynchronization with electroencephalography during walking

Brain Computer Interfaces could be useful in rehabilitation of movement, perhaps also for gait. Until recently, research on movement related brain signals has not included measuring electroencephalography (EEG) during walking, because of the potential artifacts. We investigated if it is possible to measure the event Related Desynchronization (ERD) and event related spectral perturbations (ERSP) during walking. Six subjects walked on a treadmill with a slow speed, while EEG, electromyography (EMG) of the neck muscles and step cycle were measured. A Canonical Correlation Analysis (CCA) was used to remove EMG artifacts from the EEG signals. It was shown that this method correctly deleted EMG components. A strong ERD in the mu band and a somewhat less strong ERD in the beta band were found during walking compared to a baseline period. Furthermore, lateralized ERSPs were found, depending on the phase in the step cycle. It is concluded that this is a promising method to use in BCI research on walking. These results therefore pave the way for using brain signals related to walking in a BCI context.

Proprioceptive perturbations of stability during gait

Through recent studies, the role of proprioceptors in reactions to perturbations during gait has been finally somewhat better understood. The input from spindle afferents has been investigated with tendon taps, vibration and other forms of muscle stretches, including some resembling natural perturbations (stumbling, slips, and ankle inversions). It was found that activation of spindle afferents produces short-latency response (SLR), consistent with a fast spinal pathway. These reflexes induce relatively minor activation in the stretched muscles. A central question is whether stretch reflexes can occur for stimuli that are quite remote. Thus, a new study was made to examine whether foot sole vibration is able to elicit reflex responses in upper-leg muscles, for example by conduction of vibrations throughout the whole leg. SLR responses were indeed found not only in lower- but also in upper-leg muscles. Similarly during stumbling, SLR are observed throughout the whole limb, although the primary perturbation occurs at foot level. After the SLR, much stronger activations usually occur, with latencies (85 or 120ms) well below those seen in voluntary contractions. These late responses are much more selective and presumably linked to the maintenance of stability. The role of the I(b) afferents from the Golgi tendon organs (GTO) is less clear. From animal work, it is known that these afferents are very sensitive to active muscle contraction and that they play a role in providing reinforcing feedback to extensors during the stance phase. The available evidence supports this notion in humans but lack of selective activation methods precludes more conclusive confirmation.

Botulinum Toxin-A in Children With Congenital Spastic Hemiplegia Does Not Improve Upper Extremity Motor-Related Function Over Rehabilitation Alone: A Randomized Controlled Trial

Background. Rehabilitation of the upper extremity in children with hemiplegic cerebral palsy has not been compared to the same intensity of therapy combined with injected botulinum toxin (BTX). Objective. To measure the short-term (2 weeks) and long-term (6 and 9 months) effects of a standardized functional training program versus without the addition of chemodenervation of forearm and hand muscles. Methods. Twenty children with spastic hemiplegia, aged 4 to 16 years, were matched for baseline characteristics and then randomized to standardized functional physical and occupational therapies for 6 months (PT/OT group) or to the same therapies plus multimuscle BTX-A (BTX+ group). Main outcome measures were isometric generated force, overshoot and undershoot (force production error), active and passive range of motion by goniometry (ROM), stretch restricted angle (SRA) of joints, Ashworth scores at the elbow and wrist, and the Melbourne assessment of unilateral upper limb function. All measures were performed at baseline, 2 weeks after BTX-A, 6 months (end of therapy), and then 3 months after termination of the therapy. Results. Clinical measures (muscle tone, active ROM of wrist and elbow) showed improvement in both groups. However, no significant differences emerged between groups on functional measures. Generated force decreased directly after the BTX-A injection but increased during the therapy period. The PT/OT group, however, showed a significantly higher increase in force and accuracy with therapy compared with the BTX+ therapy group. Conclusions. Functional rehabilitation therapies for the upper extremity increase manual isometric flexor force at the wrist and ROM, but BTX injections cause weakness and do not lead to better outcomes than therapy alone.

Dynamic posturography in Parkinson's disease: diagnostic utility of the "first trial effect".

Previous dynamic posturography studies demonstrated clear abnormalities in balance responses in Parkinsons disease (PD) patients compared to controls at the group level, but its clinical value in the diagnostic process and fall risk estimation in individual patients leaves for improvement. Therefore, we investigated whether a new approach, focusing on the balance responses to the very first and fully unpractised trial rather than a pooled mean response to a series of balance perturbations, could further improve the diagnostic utility of dynamic posturography. Following the first trial, subjects were exposed to repeated balance perturbations, which also permitted us to investigate the training responses. Fourteen patients with PD and 18 age-matched controls were enrolled, who received a series of multidirectional postural perturbations, induced by support surface rotations. We measured trunk and upper arm kinematics and electromyographic responses, and evaluated group differences at three levels: the postural response to the very first backward perturbation; pooled first and habituated postural responses; and habituation rates. Analysis of the first trial responses yielded similar results as evaluation of the mean response over trials: forward flexion of the trunk induced by backward perturbations was decreased in patients, accompanied by increased muscle responses present. Moreover, trunk movement and muscle activity were equally present in both groups-suggesting a preserved training response in PD patients. Early masseter activity in both groups might be indicative of a startle-like component to the balance response. In terms of diagnostic utility, focusing on the first trial response or habituation rate is no better than analysis of pooled responses to a series of perturbations. The apparently preserved training response in PD patients suggests that balance reactions in PD can be improved by repeated exposure, and this may have implications for future exercise studies. Early masseter activity warrants further studies to evaluate a potential startle component in the pathophysiology of balance disorders.

Muscle activation patterns are bilaterally linked during split-belt treadmill walking in humans

There is growing evidence that human locomotion is controlled by flexibly combining a set of basic muscle activity patterns. To explore how these patterns are modified to cope with environmental constraints, 10 healthy young adults 1st walked on a split-belt treadmill at symmetric speeds of 4 and 6 km/h for 2 min. An asymmetric condition was then performed for 10 min in which treadmill speeds for the dominant (fast) and nondominant (slow) sides were 6 and 4 km/h, respectively. This was immediately followed by a symmetric speed condition of 4 km/h for 5 min. Gait kinematics and ground reaction forces were recorded. Electromyography (EMG) was collected from 12 lower limb muscles on each side of the body. Nonnegative matrix factorization was applied to the EMG signals bilaterally and unilaterally to obtain basic activation patterns. A cross-correlation analysis was then used to quantify temporal changes in the activation patterns. During the early (1st 10 strides) and late (final 10 strides) phases of the asymmetric condition, the patterns related to ankle plantar flexor (push-off) of the fast limb and quadriceps muscle (contralateral heel contact) of the slow limb occurred earlier in the gait cycle compared with the symmetric conditions. Moreover, a bilateral temporal alignment of basic patterns between limbs was still maintained in the split-belt condition since a similar shift was observed in the unilateral patterns. The results suggest that the temporal structure of these locomotor patterns is shaped by sensory feedback and that the patterns are bilaterally linked.

SPLIT-BELT LOCOMOTION IN PARKINSON'S DISEASE WITH AND WITHOUT FREEZING OF GAIT

BACKGROUND Parkinsons disease (PD) patients have an increased gait asymmetry and variability, which is most pronounced in patients with freezing of gait (FOG). We examined if stride time variability and deficits in interlimb coordination between the upper and lower limbs would increase during split-belt locomotion in PD, and particularly so in patients with FOG. METHODS Fourteen PD patients (seven with FOG, matched for disease severity with the seven non-freezers) and 10 healthy controls walked on a treadmill with split belts at different speeds (2 versus 3km/h). Gait was recorded by means of a video motion analysis system. Outcome measures were stride length asymmetry and variability, stride time asymmetry and variability, ipsilateral and contralateral interlimb coordination, and phase coordination index. RESULTS Both PD subjects and controls were able to adapt to split-belt walking by modulating their stride length. However, freezers showed a larger increase in stride time asymmetry and stride time variability due to split-belt walking compared to non-freezers. Furthermore, contralateral interlimb coordination improved in control subjects during split-belt walking, but not in PD patients (freezers and non-freezers). Phase coordination index did not change differently across the three groups. CONCLUSIONS The ability to walk under split-belt conditions was preserved in PD. Non-freezers and controls compensated for the experimentally increased stride length asymmetry by decreasing their stride time asymmetry. This ability was lost in freezers, who in fact increased their stride time asymmetry during split-belt walking. As a result, stride time variability also increased in freezers. These findings support the hypothesis that FOG is related to gait asymmetries and to gait timing deficits.

Classification of forefoot pain based on plantar pressure measurements

BACKGROUND Plantar pressure is widely used to evaluate foot complaints. However, most plantar pressure studies focus on the symptomatic foot with foot deformities. The purposes of this study were to investigate subjects without clear foot deformities and to identify differences in plantar pressure pattern between subjects with and without forefoot pain. The second aim was to discriminate between subjects with and without forefoot pain based on plantar pressure measurements using neural networks. METHODS In total, 297 subjects without foot deformities of whom almost 50% had forefoot pain walked barefoot over a pressure plate. Foot complaints and subject characteristics were assessed with a questionnaire and a clinical evaluation. Plantar pressure was analyzed using a recently developed method, which produced pressure images of the time integral, peak pressure, mean pressure, time of activation and deactivation, and total contact time per pixel. After pre-processing the pressure images with principal component analysis, a forward selection procedure with neural networks was used to classify forefoot pain. FINDINGS The pressure-time integral and mean pressure were significantly larger under the metatarsals II and III for subjects with forefoot pain. A neural network with 14 input parameters correctly classified forefoot pain in 70.4% of the test feet. INTERPRETATION The differences in plantar pressure parameters between subjects with and without forefoot pain were small. The reasonable performance of forefoot pain classification by neural networks suggests that forefoot pain is related more to the distribution of the pressure under the foot than to the absolute values of the pressure at fixed locations.

Kinematic aiming task: measuring functional changes in hand and arm movements after botulinum toxin-A injections in children with spastic hemiplegia

Rameckers EAA, Speth LAWM, Duysens J, Vles JSH, Smits-Engelsman BCM: Kinematic aiming task: measuring functional changes in hand and arm movements after botulinum toxin-a injections in children with spastic hemiplegia. Am J Phys Med Rehabil 2007;86:538–547. Objective:To describe different aspects of a kinematic aiming task (KAT) as a quantitative way to assess changes in arm movements within 2 wks after botulinum toxin-A (BTX-A) injections in children with spastic hemiplegia. Design:Intervention study randomized clinical trial; follow-up within 4 wks after baseline measurement. Results:The KAT gave a high intraclass correlation on movement time, spread of end points (END), and index of performance effective (IP-E). After BTX-A, a significant increase of END and IP-E was shown if precision demand in the KAT was high, whereas the inverse occurred when speed was more important. These functional changes coincided with a significant decrease of the maximum voluntary contraction of the flexor muscles of the forearm. Muscle tone measured with the Ashworth scale did show a nonsignificant decrease of muscle tone, as did the stretch restricted angle and the active and passive ranges of motion of the elbow and wrist. Conclusions:Muscle force decreased immediately after BTX-A, showing the direct effect of BTX-A. The KAT is an adequate, reproducible way to quantify functional changes after BTX-A in the upper limb. BTX-A has an inverse effect in the precision task when accuracy is important, and it has a positive effect when speed prevails.