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Walking in natural environments requires visually guided modifications, which can be more challenging when involving sideway steps rather than longer steps. This exploratory study investigated whether these two types of modifications involve different changes in the central drive to spinal motor neurons of leg muscles. Fifteen adults [age:36 ± 6 (SD years)] walked on a treadmill (4 km/h) while observing a screen displaying real-time position of their toes. At the beginning of the swing phase, a visual target appeared in front (forward) or medial-lateral (sideway) of the ground contact in random step cycles (approximately every 3rd step). We measured 3D kinematics and electromyographic activity from leg muscles bilaterally. Intermuscular coherence was calculated in the alpha (5-15 Hz), beta (15-30 Hz), and gamma bands (30-45 Hz) approximately 230 ms prior and post ground contact in control and target steps. Results showed that adjustments towards sideway targets were associated with significantly higher error, lower foot lift, and higher co-contraction between antagonist ankle muscles. Movements towards sideway targets were associated with larger beta-band SOL: MG coherence and a more narrow and larger peak of synchronization in the cumulant density before ground contact. In contrast, movements towards forward targets showed no significant differences in coherence or synchronization compared to control steps. Larger SOL: MG beta-band coherence and short-term synchronization were observed during sideway, but not forward, gait modifications. This suggests that visually guided gait modifications may involve differences in the central drive to spinal ankle motor neurons dependent on the level of task difficulty.

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Spastic movement disorder is characterized by reduced ability to selectively activate muscles with significant co-activation of antagonist muscles. It has traditionally been thought that hyperexcitable stretch reflexes have a central role in the pathophysiology and the clinical manifestations of the disorder. Here we argue that the main functional challenges for persons with spastic movement disorder are related to contractures, paresis, weak muscles and inappropriate central motor commands, whereas hyperexcitable reflexes play no or only an insignificant functional role. Co-activation of antagonist muscles and stiff posture and gait may rather be adaptations that aim to ensure joint and postural stability due to insufficient muscle strength. Aberrant (involuntary) muscle activity is likely related to an inadequate prediction of the sensory consequences of movement and a resulting impairment of muscle coordination. We argue that improvement of functional muscle strength and muscle coordination following central motor lesions may be achieved by optimizing integration of somatosensory information into central feedforward motor programs, whereas anti-spastic therapy that aims to reduce reflex activity may be less efficient. This opens for novel investigations into new treatment strategies that may improve functional control of movement and prevent reduced joint mobility in people with brain lesions.

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BACKGROUND: Human walking involves a rapid and powerful contraction of ankle plantar flexors during push-off in late stance. OBJECTIVE: Here we investigated whether impaired push-off force contributes to gait problems in children with cerebral palsy (CP) and whether it may be improved by intensive gait training. METHODS: Sixteen children with CP (6-15 years) and fourteen typically developing (TD) children (4-15 years) were recruited. Foot pressure was measured by insoles and gait kinematics were recorded by 3-dimensional video analysis during treadmill and overground walking. The peak derivative of ground reaction force at push off (dPF) was calculated from the foot pressure measurements. Maximal voluntary plantar flexion (MVC) was measured while seated. Measurements were performed before and after a control period and after 4 weeks of 30 minutes daily inclined treadmill training. RESULTS: dPF and MVC were significantly lower in children with CP on the most affected (MA) as compared to TD children (p < .001). dPF was lower on the MA leg as compared to the less affected (LA) leg in children with CP (p < .05). Following gait training, increases in dPF (p < .001) and MVC (p < .01) were observed for the MA leg. Following gait training children with CP showed similar timing of dPF and similar stance phase duration on both legs indicating improved symmetry of gait. These effects were also shown during overground walking. CONCLUSION: Impaired ability to voluntarily activate ankle plantar flexors and produce a rapid and powerful push-off during late stance are of importance for impaired gait function in children with CP. Intensive treadmill training may facilitate the drive to ankle plantar flexors and reduce gait asymmetry during both treadmill and overground walking.

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Voluntary toe walking in adults is characterized by feedforward control of ankle muscles in order to ensure optimal stability of the ankle joint at ground impact. Toe walking is frequently observed in children with cerebral palsy, but the mechanisms involved have not been clarified. Here, we investigated maturation of voluntary toe walking in typically-developing children and typically-developed adults and compared it to involuntary toe walking in children with cerebral palsy. Twenty-eight children with cerebral palsy (age 3-14 years), 24 typically-developing children (age 2-14 years) and 15 adults (mean age 30.7 years) participated in the study. EMG activity was measured from the tibialis anterior and soleus muscles together with knee and ankle joint position during treadmill walking. In typically-developed adults, low step-to-step variability of the drop of the heel after ground impact was correlated with low tibialis anterior and high soleus EMG with no significant coupling between the antagonist muscle EMGs. Typically-developing children showed a significant age-related decline in EMG amplitude reaching an adult level at 10-12 years of age. The youngest typically-developing children showed a broad peak EMG-EMG synchronization (>100 ms) associated with large 5-15 Hz coherence between antagonist muscle activities. EMG coherence declined with age and at the age of 10-12 years no correlation was observed similar to adults. This reduction in coherence was closely related to improved step-to-step stability of the ankle joint position. Children with cerebral palsy generally showed lower EMG levels than typically-developing children and larger step-to-step variability in ankle joint position. In contrast to typically-developing children, children with cerebral palsy showed no age-related decline in tibialis anterior EMG amplitude. Motor unit synchronization and 5-15 Hz coherence between antagonist EMGs was observed more frequently in children with cerebral palsy when compared to typically-developing children and in contrast to typically-developing participants there was no age-related decline. We conclude that typically-developing children develop mature feedforward control of ankle muscle activity as they age, such that at age 10-12 years there is little agonist-antagonist muscle co-contraction around the time of foot-ground contact during toe walking. Children with cerebral palsy, in contrast, continue to co-contract agonist and antagonist ankle muscles when toe walking. We speculate that children with cerebral palsy maintain a co-contraction activation pattern when toe walking due to weak muscles and insufficient motor and sensory signalling necessary for optimization of feedforward motor programs. These findings are important for understanding of the pathophysiology and treatment of toe walking.

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KEY POINTS: Activation of ankle muscles at ground contact during toe walking is unaltered when sensory feedback is blocked or the ground is suddenly dropped. Responses in the soleus muscle to transcranial magnetic stimulation, but not peripheral nerve stimulation, are facilitated at ground contact during toe walking. We argue that toe walking is supported by feedforward control at ground contact. ABSTRACT: Toe walking requires careful control of the ankle muscles in order to absorb the impact of ground contact and maintain a stable position of the joint. The present study aimed to clarify the peripheral and central neural mechanisms involved. Fifteen healthy adults walked on a treadmill (3.0 km h-1 ). Tibialis anterior (TA) and soleus (Sol) EMG, knee and ankle joint angles, and gastrocnemius-soleus muscle fascicle lengths were recorded. Peripheral and central contributions to the EMG activity were assessed by afferent blockade, H-reflex testing, transcranial magnetic brain stimulation (TMS) and sudden unloading of the planter flexor muscle-tendon complex. Sol EMG activity started prior to ground contact and remained high throughout stance. TA EMG activity, which is normally seen around ground contact during heel strike walking, was absent. Although stretch of the Achilles tendon-muscle complex was observed after ground contact, this was not associated with lengthening of the ankle plantar flexor muscle fascicles. Sol EMG around ground contact was not affected by ischaemic blockade of large-diameter sensory afferents, or the sudden removal of ground support shortly after toe contact. Soleus motor-evoked potentials elicited by TMS were facilitated immediately after ground contact, whereas Sol H-reflexes were not. These findings indicate that at the crucial time of ankle stabilization following ground contact, toe walking is governed by centrally mediated motor drive rather than sensory driven reflex mechanisms. These findings have implications for our understanding of the control of human gait during voluntary toe walking.

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KEY POINTS: The early postnatal development of functional corticospinal connections in human infants is not fully clarified. Corticospinal drive to upper and lower limb muscle shows developmental changes with an increased functional coupling in infants between 9 and 25 weeks in the beta frequency band. The changes in functional coupling coincide with the developmental period where fidgety movements are present in healthy infants. Data support a possible sensitive period where functional connections between corticospinal tract fibres and spinal motoneurones undergo activity-dependent reorganization. ABSTRACT: The early postnatal development of functional corticospinal connections in human infants is not fully clarified. We used EEG and EMG to investigate the development of corticomuscular and intramuscular coherence as indicators of functional corticospinal connectivity in healthy infants aged 1-66 weeks. EEG was recorded over leg and hand area of motor cortex. EMG recordings were made from right ankle dorsiflexor and right wrist extensor muscles. Quantification of the amount of corticomuscular coherence in the 20-40 Hz frequency band showed a significantly larger coherence for infants aged 9-25 weeks compared to younger and older infants. Coherence between paired EMG recordings from tibialis anterior muscle in the 20-40 Hz frequency band was also significantly larger for the 9-25 week age group. A low-amplitude, broad-duration (40-50 ms) central peak of EMG-EMG synchronization was observed for infants younger than 9 weeks, whereas a short-lasting (10-20 ms) central peak was observed for EMG-EMG synchronization in older infants. This peak was largest for infants aged 9-25 weeks. These data suggest that the corticospinal drive to lower and upper limb muscles shows significant developmental changes with an increase in functional coupling in infants aged 9-25 weeks, a period which coincides partly with the developmental period of normal fidgety movements. We propose that these neurophysiological findings may reflect the existence of a sensitive period where the functional connections between corticospinal tract fibres and spinal motoneurones undergo activity-dependent reorganization. This may be relevant for the timing of early therapy interventions in infants with pre- and perinatal brain injury.

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Foot drop and toe walking are frequent concerns in children with cerebral palsy. The main underlying cause of these problems is early damage and lack of maturation of the corticospinal tract. In the present study we investigated whether 4 weeks of daily treadmill training with an incline may facilitate corticospinal transmission and improve the control of the ankle joint in children with cerebral palsy. Sixteen children with cerebral palsy (Gross Motor Classification System I:6, II:6, III:4) aged 5-14 years old, were recruited for the study. Evaluation of gait ability and intramuscular coherence was made twice before and twice after training with an interval of 1 month. Gait kinematics were recorded by 3D video analysis during treadmill walking with a velocity chosen by the child at the first evaluation. Foot pressure was measured by force sensitive foot soles during treadmill and over ground walking. EMG-EMG coherence was calculated from two separate electrode recordings placed over the tibialis anterior muscle. Training involved 30 min of walking daily on a treadmill with an incline for 30 days. Gait training was accompanied by significant increases in gait speed, incline on the treadmill, the maximal voluntary dorsiflexion torque, the number and amplitude of toe lifts late in the swing phase during gait and the weight exerted on the heel during the early stance phase of the gait cycle. EMG-EMG coherence in the beta and gamma frequency bands recorded from tibialis anterior muscle increased significantly when compared to coherence before training. The largest changes in coherence with training were observed for children <10 years of age. Importantly, in contrast to training-induced EMG increases, the increase in coherence was maintained at the follow-up measurement 1 month after training. Changes in the strength of coherence in the beta and gamma band were positively correlated with improvements in the subjects' ability to lift the toes in the swing phase. These data show that daily intensive gait training increases beta and gamma oscillatory drive to ankle dorsiflexor motor neurons and that it improves toe lift and heel strike in children with cerebral palsy. We propose that intensive gait training may produce plastic changes in the corticospinal tract, which are responsible for improvements in gait function.

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