Muscle Activity during Passive and Active Movements in Preterm and Full-Term Infants.

Manifestation of muscle reactions at an early developmental stage may reflect the processes underlying the generation of appropriate muscle tone, which is also an integral part of all movements. In preterm infants, some aspects of muscular development may occur differently than in infants born at term. Here we evaluated early manifestations of muscle tone by measuring muscle responses to passive stretching (StR) and shortening (ShR) in both upper and lower limbs in preterm infants (at the corrected age from 0 weeks to 12 months), and compared them to those reported in our previous study on full-term infants. In a subgroup of participants, we also assessed spontaneous muscle activity during episodes of relatively large limb movements. The results showed very frequent StR and ShR, and also responses in muscles not being primarily stretched/shortened, in both preterm and full-term infants. A reduction of sensorimotor responses to muscle lengthening and shortening with age suggests a reduction in excitability and/or the acquisition of functionally appropriate muscle tone during the first year of life. The alterations of responses during passive and active movements in preterm infants were primarily seen in the early months, perhaps reflecting temporal changes in the excitability of the sensorimotor networks.

Complexity of modular neuromuscular control increases and variability decreases during human locomotor development.

When does modular control of locomotion emerge during human development? One view is that modularity is not innate, being learnt over several months of experience. Alternatively, the basic motor modules are present at birth, but are subsequently reconfigured due to changing brain-body-environment interactions. One problem in identifying modular structures in stepping infants is the presence of noise. Here, using both simulated and experimental muscle activity data from stepping neonates, infants, preschoolers, and adults, we dissect the influence of noise, and identify modular structures in all individuals, including neonates. Complexity of modularity increases from the neonatal stage to adulthood at multiple levels of the motor infrastructure, from the intrinsic rhythmicity measured at the level of individual muscles activities, to the level of muscle synergies and of bilateral intermuscular network connectivity. Low complexity and high variability of neuromuscular signals attest neonatal immaturity, but they also involve potential benefits for learning locomotor tasks.

Higher Responsiveness of Pattern Generation Circuitry to Sensory Stimulation in Healthy Humans Is Associated with a Larger Hoffmann Reflex.

The state and excitability of pattern generators are attracting the increasing interest of neurophysiologists and clinicians for understanding the mechanisms of the rhythmogenesis and neuromodulation of the human spinal cord. It has been previously shown that tonic sensory stimulation can elicit non-voluntary stepping-like movements in non-injured subjects when their limbs were placed in a gravity-neutral unloading apparatus. However, large individual differences in responsiveness to such stimuli were observed, so that the effects of sensory neuromodulation manifest only in some of the subjects. Given that spinal reflexes are an integral part of the neuronal circuitry, here we investigated the extent to which spinal pattern generation excitability in response to the vibrostimulation of muscle proprioceptors can be related to the H-reflex magnitude, in both the lower and upper limbs. For the H-reflex measurements, three conditions were used: stationary limbs, voluntary limb movement and passive limb movement. The results showed that the H-reflex was considerably higher in the group of participants who demonstrated non-voluntary rhythmic responses than it was in the participants who did not demonstrate them. Our findings are consistent with the idea that spinal reflex measurements play important roles in assessing the rhythmogenesis of the spinal cord.

Maturation of the Locomotor Circuitry in Children With Cerebral Palsy.

The first years of life represent an important phase of maturation of the central nervous system, processing of sensory information, posture control and acquisition of the locomotor function. Cerebral palsy (CP) is the most common group of motor disorders in childhood attributed to disturbances in the fetal or infant brain, frequently resulting in impaired gait. Here we will consider various findings about functional maturation of the locomotor output in early infancy, and how much the dysfunction of gait in children with CP can be related to spinal neuronal networks vs. supraspinal dysfunction. A better knowledge about pattern generation circuitries in infancy may improve our understanding of developmental motor disorders, highlighting the necessity for regulating the functional properties of abnormally developed neuronal locomotor networks as a target for early sensorimotor rehabilitation. Various clinical approaches and advances in biotechnology are also considered that might promote acquisition of the locomotor function in infants at risk for locomotor delays.

Distinct locomotor precursors in newborn babies.

Mature locomotion involves modular spinal drives generating a set of fundamental patterns of motoneuron activation, each timed at a specific phase of locomotor cycles and associated with a stable muscle synergy. How locomotor modules develop and to what extent they depend on prior experience or intrinsic programs remains unclear. To address these issues, we herein leverage the presence at birth of two types of locomotor-like movements, spontaneous kicking and weight-bearing stepping. The former is expressed thousands of times in utero and postnatally, whereas the latter is elicited de novo by placing the newborn on the ground for the first time. We found that the neuromuscular modules of stepping and kicking differ substantially. Neonates kicked with an adult-like number of temporal activation patterns, which lacked a stable association with systematic muscle synergies across movements. However, on the ground neonates stepped with fewer temporal patterns but all structured in stable synergies. Since kicking and ground-stepping coexist at birth, switching between the two behaviors may depend on a dynamic reconfiguration of the underlying neural circuits as a function of sensory feedback from surface contact. We tracked the development of ground-stepping in 4- to 48-mo-old infants and found that, after the age of 6 mo, the number of temporal patterns increased progressively, reaching adult-like conformation only after independent walking was established. We surmise that mature locomotor modules may derive by combining the multiple patterns of repeated kicking, on the one hand, with synergies resulting from fractionation of those revealed by sporadic weight-bearing stepping, on the other hand.

Muscle Responses to Passive Joint Movements in Infants During the First Year of Life.

Muscle tone represents one of the important concepts for characterizing changes in the state of the developing nervous system. It can be manifested in the level of activity of flexors and extensors and in muscle reactions to its passive stretching (StR) or shortening (ShR). Here we investigated such reactions in a cohort of healthy infants aged from 2 weeks to 12 months. We examined the presence and the characteristics of StR and ShR during slow passive cyclic flexion/extension movements (T~3 s) in the hip, knee, ankle, and elbow joints while awake infants were in the supine position. The results showed that most infants demonstrated prominent ShRs in response to passive joint rotations, although the StR was observed more frequently, suggesting that the ShR is an important component of adaptive motor behavior already at an early developmental stage. Interestingly, the occurrence of both StR and ShR in most muscles significantly decreased throughout the first year of life. Passive cyclic flexion/extension movements could also evoke rhythmic muscle responses in other joints or in the contralateral limb, however, such responses were predominantly observed in younger infants (<6 months). A noticeable manifestation of muscle reactions at an early developmental stage, along with spontaneous motor activity in this period of life, may reflect the processes underlying a formation of appropriate muscle tone and the self-organization of neural circuits. A substantial reduction of ipsilateral and contralateral muscle responses to passive movements with age is consistent with the idea of a functional reorganization of the motor circuitry during early development.

Tonic and Rhythmic Spinal Activity Underlying Locomotion.

In recent years, many researches put significant efforts into understanding and assessing the functional state of the spinal locomotor circuits in humans. Various techniques have been developed to stimulate the spinal cord circuitries, which may include both diffuse and quite specific tuning effects. Overall, the findings indicate that tonic and rhythmic spinal activity control are not separate phenomena but are closely integrated to properly initiate and sustain stepping. The spinal cord does not simply transmit information to and from the brain. Its physiologic state determines reflex, postural and locomotor control and, therefore, may affect the recovery of the locomotor function in individuals with spinal cord and brain injuries. This review summarizes studies that examine the rhythmogenesis capacity of cervical and lumbosacral neuronal circuitries in humans and its importance in developing central pattern generator-modulating therapies.

Rhythmic wrist movements facilitate the soleus H-reflex and non-voluntary air-stepping in humans.

Neural coupling between the upper and lower limbs during human walking is supported by modulation of cross-limb reflexes and the presence of rhythmic activity in the proximal arm muscles. Nevertheless, the involvement of distal arm muscles in cyclic movements and sensorimotor neuromodulation is also suggested given their step-synchronized activation in many locomotor-related tasks (e.g., swimming, skiing, climbing, cycling, crawling, etc.). Here we investigated the effect of rhythmic wrist movements, separately and in conjunction with arm swinging, on the characteristics of non-voluntary cyclic leg movements evoked by muscle vibration in a gravity neutral position and on the soleus H-reflex of the stationary legs. For the H-reflex modulation, five conditions were compared: stationary arms, voluntary alternating upper limb swinging, combined upper limb and wrist motion, wrist movements only and motion of the upper limbs with addition of load. Rhythmic wrist movements significantly facilitated the amplitude of non-voluntary leg oscillations, including ankle joint oscillations, and the H-reflex. The latter effect was related to rhythmicity of wrist motion rather than to a simple extra tension in the upper limb muscles (a kind of the Jendrassik manoeuvre) since adding resistance to arm oscillations (without flexion-extension in the wrist joint) had an opposite inhibitory effect on the H-reflex. Our results further support the existence of connections between the distal parts of the upper and lower extremities at the neural level, suggesting that wrist joint movements can be an important component of motor neurorehabilitation.

Tapping into rhythm generation circuitry in humans during simulated weightlessness conditions.

An ability to produce rhythmic activity is ubiquitous for locomotor pattern generation and modulation. The role that the rhythmogenesis capacity of the spinal cord plays in injured populations has become an area of interest and systematic investigation among researchers in recent years, despite its importance being long recognized by neurophysiologists and clinicians. Given that each individual interneuron, as a rule, receives a broad convergence of various supraspinal and sensory inputs and may contribute to a vast repertoire of motor actions, the importance of assessing the functional state of the spinal locomotor circuits becomes increasingly evident. Air-stepping can be used as a unique and important model for investigating human rhythmogenesis since its manifestation is largely facilitated by a reduction of external resistance. This article aims to provide a review on current issues related to the "locomotor" state and interactions between spinal and supraspinal influences on the central pattern generator (CPG) circuitry in humans, which may be important for developing gait rehabilitation strategies in individuals with spinal cord and brain injuries.

Interhemispheric motor cortex influence during bimanual unloading.

Using the transcranial magnetic stimulation (TMS) of motor cortex we examined changes in the motor evoked potential (MEP) during natural bimanual unloading, during lifting of an equivalent weight by the contralateral arm while the ipsilateral forearm was held stationary (CONTRA) and during practice of unnatural unloading. During natural unloading, MEP amplitude decreased proportionally to the muscle activity. In CONTRA task MEP amplitude decreased, but the muscle activity was not changed. It suggests that the motor cortex activity related to the "postural" arm was inhibited by the contralateral motor cortex related to the "lifting" arm. This inhibition was diminished during the unloading task. When learning the unnatural unloading, the muscle activity decreased significantly with insignificant changes of MEP amplitude. Active role of the motor cortex during learning of the new task might be related to the reduction of the contralateral inhibition. This suggestion is supported by the observation that MEP amplitude decreased stronger than muscle activity in the first learning session similar to that in CONTRA task. MEP amplitude and background activity of the muscle proportionally decreased in the last learning trial. The results show that motor cortex activity in natural and unnatural unloading task might be related to the reduction of the interhemispheric inhibition.