Postural control in the elephant.

As the largest extant legged animals, elephants arguably face the most extreme challenge for stable standing. In this study, we investigated the displacement of the centre of pressure of 12 elephants during quiet standing. We found that the average amplitude of the oscillations in the lateral and fore-aft directions was less than 1.5 cm. Such amplitudes for postural oscillation are comparable with those of dogs and other species, suggesting that some aspects of sensorimotor postural control do not scale with size.

Neuromechanical adjustments when walking with an aiding or hindering horizontal force.

PURPOSE: Walking against a constant horizontal traction force which either hinders or aids the motion of the centre of mass of the body (COM) will create a discrepancy between the positive and negative work being done by the muscles and may thus affect the mechanics and energetics of walking. We aimed at investigating how this imbalance affects the exchange between potential and kinetic energy of the COM and how its dynamics is related to specific spatiotemporal organisation of motor pool activity in the spinal cord. To understand if and how the spinal cord activation may be associated with COM dynamics, we also compared the neuromechanical adjustments brought on by a horizontal force with published data about those brought on by a slope. METHODS: Ten subjects walked on a treadmill at different speeds with different traction forces. We recorded kinetics, kinematics, and electromyographic activity of 16 lower-limb muscles and assessed the spinal locomotor output by mapping them onto the rostrocaudal location of the motoneuron pools. RESULTS: When walking with a hindering force, the major part of the exchange between potential and kinetic energy of the COM occurs during the first part of stance, whereas with an aiding force exchanges increase during the second part of stance. Those changes occur since limb and trunk orientations remain aligned with the average orientation of the ground reaction force vector. Our results also show the sacral motor pools decreased their activity with an aiding force and increased with a hindering one, whereas the lumbar motor pools increased their engagement both with an aiding and a hindering force. CONCLUSION: Our findings suggest that applying a constant horizontal force results in similar modifications of COM dynamics and spinal motor output to those observed when walking on slopes, consistent with common principles of motor pool functioning and biomechanics of locomotion.

Differential activation of lumbar and sacral motor pools during walking at different speeds and slopes.

Organization of spinal motor output has become of interest for investigating differential activation of lumbar and sacral motor pools during locomotor tasks. Motor pools are associated with functional grouping of motoneurons of the lower limb muscles. Here we examined how the spatiotemporal organization of lumbar and sacral motor pool activity during walking is orchestrated with slope of terrain and speed of progression. Ten subjects walked on an instrumented treadmill at different slopes and imposed speeds. Kinetics, kinematics, and electromyography of 16 lower limb muscles were recorded. The spinal locomotor output was assessed by decomposing the coordinated muscle activation profiles into a small set of common factors and by mapping them onto the rostrocaudal location of the motoneuron pools. Our results show that lumbar and sacral motor pool activity depend on slope and speed. Compared with level walking, sacral motor pools decrease their activity at negative slopes and increase at positive slopes, whereas lumbar motor pools increase their engagement when both positive and negative slope increase. These findings are consistent with a differential involvement of the lumbar and the sacral motor pools in relation to changes in positive and negative center of body mass mechanical power production due to slope and speed.NEW & NOTEWORTHY In this study, the spatiotemporal maps of motoneuron activity in the spinal cord were assessed during walking at different slopes and speeds. We found differential involvement of lumbar and sacral motor pools in relation to changes in positive and negative center of body mass power production due to slope and speed. The results are consistent with recent findings about the specialization of neuronal networks located at different segments of the spinal cord for performing specific locomotor tasks.

Planar covariance of upper and lower limb elevation angles during hand-foot crawling in healthy young adults.

Habitual quadrupeds have been shown to display a planar covariance of segment elevation angle waveforms in the fore and hind limbs during many forms of locomotion. The purpose of the current study was to determine if humans generate similar patterns in the upper and lower limbs during hand-foot crawling. Nine healthy young adults performed hand-foot crawling on a treadmill at speeds of 1, 2, and 3 km/h. A principal component analysis (PCA) was applied to the segment elevation angle waveforms for the upper (upper arm, lower arm, and hand) and lower (thigh, shank, and foot) limbs separately. The planarity of the elevation angle waveforms was determined using the sum of the variance explained by the first two PCs and the orientation of the covariance plane was quantified using the direction cosines of the eigenvector orthogonal to the plane, projected upon each of the segmental semi-axes. Results showed that planarity of segment elevation angles was maintained in the upper and lower limbs (explained variance >97%), although a slight decrease was present in the upper limb when crawling at 3 km/h. The orientation of the covariance plane was highly limb-specific, consistent with animal studies and possibly related to the functional neural control differences between the upper and lower limbs. These results may suggest that the motor patterns stored in the central nervous system for quadrupedal locomotion may be retained through evolution and may still be exploited when humans perform such tasks.

Neuromuscular adjustments of gait associated with unstable conditions.

A compact description of coordinated muscle activity is provided by the factorization of electromyographic (EMG) signals. With the use of this approach, it has consistently been shown that multimuscle activity during human locomotion can be accounted for by four to five modules, each one comprised of a basic pattern timed at a different phase of gait cycle and the weighting coefficients of synergistic muscle activations. These modules are flexible, in so far as the timing of patterns and the amplitude of weightings can change as a function of gait speed and mode. Here we consider the adjustments of the locomotor modules related to unstable walking conditions. We compared three different conditions, i.e., locomotion of healthy subjects on slippery ground (SL) and on narrow beam (NB) and of cerebellar ataxic (CA) patients on normal ground. Motor modules were computed from the EMG signals of 12 muscles of the right lower limb using non-negative matrix factorization. The unstable gait of SL, NB, and CA showed significant changes compared with controls in the stride length, stride width, range of angular motion, and trunk oscillations. In most subjects of all three unstable conditions, >70% of the overall variation of EMG waveforms was accounted for by four modules that were characterized by a widening of muscle activity patterns. This suggests that the nervous system adopts the strategy of prolonging the duration of basic muscle activity patterns to cope with unstable conditions resulting from either slippery ground, reduced support surface, or pathology.

Locomotor patterns in cerebellar ataxia.

Several studies have demonstrated how cerebellar ataxia (CA) affects gait, resulting in deficits in multijoint coordination and stability. Nevertheless, how lesions of cerebellum influence the locomotor muscle pattern generation is still unclear. To better understand the effects of CA on locomotor output, here we investigated the idiosyncratic features of the spatiotemporal structure of leg muscle activity and impairments in the biomechanics of CA gait. To this end, we recorded the electromyographic (EMG) activity of 12 unilateral lower limb muscles and analyzed kinematic and kinetic parameters of 19 ataxic patients and 20 age-matched healthy subjects during overground walking. Neuromuscular control of gait in CA was characterized by a considerable widening of EMG bursts and significant temporal shifts in the center of activity due to overall enhanced muscle activation between late swing and mid-stance. Patients also demonstrated significant changes in the intersegmental coordination, an abnormal transient in the vertical ground reaction force and instability of limb loading at heel strike. The observed abnormalities in EMG patterns and foot loading correlated with the severity of pathology [International Cooperative Ataxia Rating Scale (ICARS), a clinical ataxia scale] and the changes in the biomechanical output. The findings provide new insights into the physiological role of cerebellum in optimizing the duration of muscle activity bursts and the control of appropriate foot loading during locomotion.

Effects of transcranial magnetic stimulation during voluntary and non-voluntary stepping movements in humans.

Here, we compared motor evoked potentials (MEP) in response to transcranial magnetic stimulation of the motor cortex and the H-reflex during voluntary and vibration-induced air-stepping movements in humans. Both the MEPs (in mm biceps femoris, rectus femoris and tibialis anterior) and H-reflex (in m soleus) were significantly smaller during vibration-induced cyclic leg movements at matched amplitudes of angular motion and muscle activity. These findings highlight differences between voluntary and non-voluntary activation of the spinal pattern generator circuitry in humans, presumably due to an extra facilitatory effect of voluntary control/triggering of stepping on spinal motoneurons and interneurons. The results support the idea of active engagement of supraspinal motor areas in developing central pattern generator-modulating therapies.

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.

Are effects of the symmetric and asymmetric tonic neck reflexes still visible in healthy adults?

When a cat's head is rotated in a transverse plane to one side, the legs on that side of the body extend, while on the other side, they flex (asymmetric tonic neck reflexes ATNR). On the contrary, when the head is rotated in a sagittal plane both legs flex when the head flexes, and extend when the head extends (symmetric tonic neck reflexes STNR). These reflexes have also been found in newborn babies and are thought to be a motor primitive, which is suppressed later in life. Still, using a test in which children sit on hand and knees, the ATNR and STNR can be found in children up to 9 years of age. This may suggest that these reflexes may still be involved in motor control in these children. Whether this is also the case in full-grown adults has thus far only been studied using coarse methods. Thus, for the current study, we set out to measure in detail whether the ATNR/STNR can still be evoked in healthy adult subjects. We measured 10 subjects who were asked to sit on their hands and knees while (1) their head was rotated left and right by an experimenter, (2) their head was flexed and extended by an experimenter. Kinematics was registered using a Vicon system. Elbow and head angles were detrended, and a regression analysis was performed, to investigate the effects of head angle on elbow angle. Results clearly showed the existence of the ATNR and STNR in adult subjects. A next step will be to assess the effects of the ATNR and STNR during everyday motor control tasks, such as making head rotations while driving a bike.

Plasticity and modular control of locomotor patterns in neurological disorders with motor deficits.

Human locomotor movements exhibit considerable variability and are highly complex in terms of both neural activation and biomechanical output. The building blocks with which the central nervous system constructs these motor patterns can be preserved in patients with various sensory-motor disorders. In particular, several studies highlighted a modular burst-like organization of the muscle activity. Here we review and discuss this issue with a particular emphasis on the various examples of adaptation of locomotor patterns in patients (with large fiber neuropathy, amputees, stroke and spinal cord injury). The results highlight plasticity and different solutions to reorganize muscle patterns in both peripheral and central nervous system lesions. The findings are discussed in a general context of compensatory gait mechanisms, spatiotemporal architecture and modularity of the locomotor program.

Trunk orientation, stability, and quadrupedalism.

Interesting cases of human quadrupedalism described by Tan and Colleagues (2005-2012) have attracted the attention of geneticists, neurologists, and anthropologists. Since his first publications in 2005, the main attention has focused on the genetic aspects of disorders that lead to quadrupedalism within an evolutionary framework. In recent years this area has undergone a convincing critique (Downey, 2010) and ended with a call "… to move in a different direction … away from thinking solely in terms of genetic abnormality and evolutionary atavism." We consider quadrupedalism as a "natural experiment" that may contribute to our knowledge of the physiological mechanisms underlying our balance system and our tendency toward normal (upright) posture. Bipedalism necessitates a number of characteristics that distinguish us from our ancestors and present-day mammals, including: size and shape of the bones of the foot, structure of the axial and proximal musculature, and the orientation of the human body and head. In this review we address the results of experimental studies on the mechanisms that stabilize the body in healthy people, as well as how these mechanisms may be disturbed in various forms of clinical pathology. These disturbances are related primarily to automatic rather than voluntary control of posture and suggest that human quadrupedalism is a behavior that can result from adaptive processes triggered by disorders in postural tone and environmental cues. These results will serve as a starting point for comparing and contrasting bi- and quadrupedalism.

Lack of non-voluntary stepping responses in Parkinson's disease.

The majority of research and therapeutic actions in Parkinson's disease (PD) focus on the encephalic areas, however, the potential involvement of the spinal cord in its genesis has received little attention. Here we examined spinal locomotor circuitry activation in patients with PD using various types of central and peripheral tonic stimulation and compared results to those of age-matched controls. Subjects lay on their sides with both legs suspended, allowing low-friction horizontal rotation of the limb joints. Air-stepping can be used as a unique and important model for investigating human rhythmogenesis since its manifestation is largely facilitated by the absence of external resistance. In contrast to the frequent occurrence of non-voluntary stepping responses in healthy subjects, both peripheral (muscle vibration) and central (Jendrassik maneuver, mental task, Kohnstamm phenomenon) tonic influences had little if any effect on rhythmic leg responses in PD. On the other hand, a remarkable feature of voluntary air-stepping movements in patients was a significantly higher frequency of leg oscillations than in age-matched controls. A lack of non-voluntary stepping responses was also observed after dopaminergic treatment despite the presence of prominent shortening reactions (SRs) to passive movements. We argue that the state and the rhythmogenesis capacity of the spinal circuitry are impaired in patients with PD. In particular, the results suggest impaired central pattern generator (CPG) access by sensory and central activations.

Coupling of upper and lower limb pattern generators during human crawling at different arm/leg speed combinations.

A crawling paradigm was performed by healthy adults to examine inter-limb coupling patterns and to understand how central pattern generators (CPGs) for the upper and lower limbs are coordinated. Ten participants performed hands-and-feet crawling on two separate treadmills, one for the upper limbs and another one for the lower limbs, the speed of each of them being changed independently. A 1:1 frequency relationship was often maintained even when the treadmill speed was not matched between the upper and lower limbs. However, relative stance durations in the upper limbs were only affected by changes of the upper limb treadmill speed, suggesting that although absolute times are adjusted, the relative proportions of stances and swing do not adapt to changes in lower limb treadmill speeds. With large differences between treadmill speeds, changes in upper and lower limb coupling ratio tended to occur when the upper limbs stepped at slower speeds than the lower limbs, but more rarely the other way around. These findings are in sharp contrast with those in the cat, where forelimbs always follow the rhythm of the faster moving hindlimbs. However, the fact that an integer frequency ratio is often maintained between the upper and lower limbs supports evidence of coupled CPG control. We speculate that the preference for the upper limb to decrease step frequency at lower speeds in humans may be due to weaker ascending propriospinal connections and/or a larger influence of cortical control on the upper limbs which allows for an overriding of spinal CPG control.

Foot anatomy specialization for postural sensation and control.

Anthropological and biomechanical research suggests that the human foot evolved a unique design for propulsion and support. In theory, the arch and toes must play an important role, however, many postural studies tend to focus on the simple hinge action of the ankle joint. To investigate further the role of foot anatomy and sensorimotor control of posture, we quantified the deformation of the foot arch and studied the effects of local perturbations applied to the toes (TOE) or 1st/2nd metatarsals (MT) while standing. In sitting position, loading and lifting a 10-kg weight on the knee respectively lowered and raised the foot arch between 1 and 1.5 mm. Less than 50% of this change could be accounted for by plantar surface skin compression. During quiet standing, the foot arch probe and shin sway revealed a significant correlation, which shows that as the tibia tilts forward, the foot arch flattens and vice versa. During TOE and MT perturbations (a 2- to 6-mm upward shift of an appropriate part of the foot at 2.5 mm/s), electromyogram (EMG) measures of the tibialis anterior and gastrocnemius revealed notable changes, and the root-mean-square (RMS) variability of shin sway increased significantly, these increments being greater in the MT condition. The slow return of RMS to baseline level (>30 s) suggested that a very small perturbation changes the surface reference frame, which then takes time to reestablish. These findings show that rather than serving as a rigid base of support, the foot is compliant, in an active state, and sensitive to minute deformations. In conclusion, the architecture and physiology of the foot appear to contribute to the task of bipedal postural control with great sensitivity.

Features of hand-foot crawling behavior in human adults.

Interlimb coordination of crawling kinematics in humans shares features with other primates and nonprimate quadrupeds, and it has been suggested that this is due to a similar organization of the locomotor pattern generators (CPGs). To extend the previous findings and to further explore the neural control of bipedal vs. quadrupedal locomotion, we used a crawling paradigm in which healthy adults crawled on their hands and feet at different speeds and at different surface inclinations (13°, 27°, and 35°). Ground reaction forces, limb kinematics, and electromyographic (EMG) activity from 26 upper and lower limb muscles on the right side of the body were collected. The EMG activity was mapped onto the spinal cord in approximate rostrocaudal locations of the motoneuron pools to characterize the general features of cervical and lumbosacral spinal cord activation. The spatiotemporal pattern of spinal cord activity significantly differed between quadrupedal and bipedal gaits. In addition, participants exhibited a large range of kinematic coordination styles (diagonal vs. lateral patterns), which is in contrast to the stereotypical kinematics of upright bipedal walking, suggesting flexible coupling of cervical and lumbosacral pattern generators. Results showed strikingly dissimilar directional horizontal forces for the arms and legs, considerably retracted average leg orientation, and substantially smaller sacral vs. lumbar motoneuron activity compared with quadrupedal gait in animals. A gradual transition to a more vertical body orientation (increasing the inclination of the treadmill) led to the appearance of more prominent sacral activity (related to activation of ankle plantar flexors), typical of bipedal walking. The findings highlight the reorganization and adaptation of CPG networks involved in the control of quadrupedal human locomotion and a high specialization of the musculoskeletal apparatus to specific gaits.

Idiosyncratic control of the center of mass in expert climbers.

Here, we studied posture and movement coordination adopted by expert climbers. The investigation of such expertise might be of particular interest to gain understanding about the mechanisms underlying the biomechanical control of vertical quadrupedal locomotion. A novel custom setup was developed to analyze the motion of the center-of-mass (COM) and complementary information about the dynamic distribution of vertical reaction forces under the feet during climbing in nine elite climbers (EC) and nine control subjects. Two adaptive features were found in EC. First, unexpectedly they tended to maintain larger COM distances from the wall relative to controls, during both the static and dynamic phases of vertical motion (by ∼5 cm in both cases). Second, while the control subjects tended to restrain the lateral motion of the COM, all EC demonstrated systematic COM oscillations (∼1.3 times larger) associated with a significant alternating dynamic redistribution of the body weight between the limbs during the double support phase. The latter phenomenon likely reflects an adopted basic climbing strategy in experts. Furthermore, a convergence of the optimal solution towards a more diagonal climbing strategy in EC may shed light on the origin of the diagonal gait in primates and early hominids habituated to quadrupedal vertical locomotion.

Assisted leg displacements and progressive loading by a tilt table combined with FES promote gait recovery in acute stroke.

OBJECTIVE: Here we developed and tested a novel system for early motor rehabilitation in acute stroke when patients are unable to stand and walk without assistance. Stepping performance may be largely facilitated by providing treatment in the supine position on a tilt table using step-synchronized functional electrical stimulation (FES) with assisted leg movements and progressive limb loading. METHODS: Sixty-one individuals with acute stroke were randomly assigned to two groups, experimental and control. The first group received both a conventional therapy and FES-therapy combined with progressive limb loading, whereas the control group received a conventional therapy only. Changes after treatment were assessed using clinical scores and neurophysiological measurements of movement performance. RESULTS: After treatment, there was an improvement of the clinical scores, muscle forces and everyday life activity performance in both groups, however, significantly higher in the experimental group. Active rhythmic movements of the non paretic leg often provoked muscle activity in the paretic leg as well as there was a reduction of the contralateral leg muscle contraction during paretic leg movements. CONCLUSION: The developed FES and leg displacement-assisted therapy facilitates a smooth transition to walking in the vertical position and increases the patient's functional abilities and the effectiveness of rehabilitation.

Locomotor body scheme.

The concept of body schema has been introduced and widely discussed in the literature to explain various clinical observations and distortions in the body and space representation. Here we address the role of body schema related information in multi-joint limb motion. The processing of proprioceptive information may differ significantly in static and dynamic conditions since in the latter case the control system may employ specific dynamic rules and constraints. Accordingly, the perception of movement, e.g., estimation of step length and walking distance, may rely on a priori knowledge about intrinsic dynamics of limb segment motion and inherent relationships between gait parameters and body proportions. The findings are discussed in the general framework of space and body movement representation and suggest the existence of a dynamic locomotor body schema used for controlling step length and path estimation.

A novel approach to mechanical foot stimulation during human locomotion under body weight support.

Input from the foot plays an essential part in perceiving support surfaces and determining kinematic events in human walking. To simulate adequate tactile pressure inputs under body weight support (BWS) conditions that represent an effective form of locomotion training, we here developed a new method of phasic mechanical foot stimulation using light-weight pneumatic insoles placed inside the shoes (under the heel and metatarsus). To test the system, we asked healthy participants to walk on a treadmill with different levels of BWS. The pressure under the stimulated areas of the feet and subjective sensations were higher at high levels of BWS and when applied to the ball and toes rather than heels. Foot stimulation did not disturb significantly the normal motor pattern, and in all participants we evoked a reliable step-synchronized triggering of stimuli for each leg separately. This approach has been performed in a general framework looking for "afferent templates" of human locomotion that could be used for functional sensory stimulation. The proposed technique can be used to imitate or partially restore surrogate contact forces under body weight support conditions.

Tonic central and sensory stimuli facilitate involuntary air-stepping in humans.

Air-stepping can be used as a model for investigating rhythmogenesis and its interaction with sensory input. Here we show that it is possible to entrain involuntary rhythmic movement patterns in healthy humans by using different kinds of stimulation techniques. The subjects lay on their sides with one or both legs suspended, allowing low-friction horizontal rotation of the limb joints. To evoke involuntary stepping of the suspended leg, either we used continuous muscle vibration, electrical stimulation of the superficial peroneal or sural nerves, the Jendrassik maneuver, or we exploited the postcontraction state of neuronal networks (Kohnstamm phenomenon). The common feature across all stimulations was that they were tonic. Air-stepping could be elicited by most techniques in about 50% of subjects and involved prominent movements at the hip and the knee joint (approximately 40-70 degrees). Typically, however, the ankle joint was not involved. Minimal loading forces (4-25 N) applied constantly to the sole (using a long elastic cord) induced noticeable (approximately 5-20 degrees) ankle-joint-angle movements. The aftereffect of a voluntary long-lasting (30-s) contraction in the leg muscles featured alternating rhythmic leg movements that lasted for about 20-40 s, corresponding roughly to a typical duration of the postcontraction activity in static conditions. The Jendrassik maneuver per se did not evoke air-stepping. Nevertheless, it significantly prolonged rhythmic leg movements initiated manually by an experimenter or by a short (5-s) period of muscle vibration. Air-stepping of one leg could be evoked in both forward and backward directions with frequent spontaneous transitions, whereas involuntary alternating two-legged movements were more stable (no transitions). The hypothetical role of tonic influences, contact forces, and bilateral coordination in rhythmogenesis is discussed. The results overall demonstrated that nonspecific tonic drive may cause air-stepping and the characteristics and stability of the evoked pattern depended on the sensory input.