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.

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.

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.

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.

Spatiotemporal organization of alpha-motoneuron activity in the human spinal cord during different gaits and gait transitions.

Here we studied the spatiotemporal organization of motoneuron (MN) activity during different human gaits. We recorded the electromyographic (EMG) activity patterns in 32 ipsilateral limb and trunk muscles from normal subjects while running and walking on a treadmill (3-12 km/h). In addition, we recorded backward walking and skipping, a distinct human gait that comprises the features of both walking and running. We mapped the recorded EMG activity patterns onto the spinal cord in approximate rostrocaudal locations of the MN pools. The activation of MNs tends to occur in bursts and be segregated by spinal segment in a gait-specific manner. In particular, sacral and cervical activation timings were clearly gait-dependent. Swing-related activity constituted an appreciable fraction (> 30%) of the total MN activity of leg muscles. Locomoting at non-preferred speeds (running and walking at 5 and 9 km/h, respectively) showed clear differences relative to preferred speeds. Running at low speeds was characterized by wider sacral activation. Walking at high non-preferred speeds was accompanied by an 'atypical' locus of activation in the upper lumbar spinal cord during late stance and by a drastically increased activation of lumbosacral segments. The latter findings suggest that the optimal speed of gait transitions may be related to an optimal intensity of the total MN activity, in addition to other factors previously described. The results overall support the idea of flexibility and adaptability of spatiotemporal activity in the spinal circuitry with constraints on the temporal functional connectivity of hypothetical pulsatile burst generators.

Asymmetric leg loading during sit-to-stand, walking and quiet standing in patients after unilateral total hip replacement surgery.

BACKGROUND: Asymmetric limb loading persists well after unilateral total hip replacement surgery and represents a risk of the development of osteoarthritis in the non-operated leg. Here we studied bilateral limb loading in hip arthroplasty patients for a variety of everyday activities. METHODS: Twenty-seven patients and 27 healthy age-matched control subjects participated in the study. They were asked to stand up from a chair, to stand quietly, to perform isometric maximal voluntary contractions and to walk along a 10 m path at a natural and fast speed. Two force platforms measured vertical forces under each foot during quiet standing and sit-to-stand maneuver. Temporal variables of gait were measured using footswitches. FINDINGS: In all tasks patients tended to preferentially load the non-operated limb, though the amount of asymmetry depended on the task being most prominent during standing up (inter-limb weight bearing difference exceeded 20%, independent of speed or visual conditions). In contrast, when performing maximal voluntary contractions, or during walking and quiet standing, the inter-limb difference in the maximal force production, stance/swing phase durations or weight bearing was typically less than 10%. INTERPRETATION: The results suggest that the amount of asymmetry might not be necessarily the same for different tasks. Asymmetric leg loading in patients can be critical during sit-to-stand maneuver in comparison with quiet standing and walking, and visual information seems to play only a minor role in the control of the weight-bearing ability. The proposed asymmetry indices might be clinically significant for development of post-surgical rehabilitation.

Interaction of involuntary post-contraction activity with locomotor movements.

Involuntary post-contraction muscle activity may occur after performing a strong long-lasting (about 30 s) isometric muscle contraction (Kohnstamm phenomenon). Here we examined how this putative excitatory state may interact with a locomotor movement. The subjects stood upright and were asked to oppose a rotational force applied to the pelvis for about 30 s either in the clockwise or in the counterclockwise direction. After that, they were asked to perform various motor tasks with the eyes closed. During quiet standing, we observed an involuntary post-contraction torsion of the trunk. During walking, the post-contraction facilitatory effect of body torsion was not overridden by the voluntary activity, but instead significantly influenced the forward locomotor program such that subjects walked along a curved trajectory in the direction of the preceding torsion. In contrast, we did not observe any rotational component when subjects were asked to step in place. We conclude that the post-contraction rotational aftereffect does not transfer to just any motor task but apparently manifests itself in those movements that incorporate the activated axial muscle synergy or rotational component. We argue that central excitability changes following the voluntary effort may contribute to the phenomenon and highlight the role of tonic influences in fine-tuning of the spinal cord.

Lack of anticipatory gaze-orienting responses in patients with right brain damage.

OBJECTIVE: To study eye movements during cervical proprioceptive stimulation by passive body rotation in darkness, with the head held stationary, in patients with right brain damage and hemineglect. BACKGROUND: At very low frequency, this stimulation is reported to produce an illusion of head turning in space and eye deviations directed opposite to trunk rotation (in the direction of the illusory head rotation). METHODS: Ten normal subjects and seven patients with unilateral cerebral lesions (five right brain-damaged patients with mild to moderate visuospatial neglect, two left brain-damaged patients without neglect) were included in the study. Subjects were seated on a rotating chair. Stimuli consisted of slow sinusoidal passive trunk rotations (+/-30 degrees, 0.01 Hz) while the head was fixed in space. RESULTS: Eye movements directed opposite to trunk rotation were typical for normal subjects and for left brain-damaged patients. In contrast, all right brain-damaged patients showed either eye movements in the direction of trunk rotation or no eye deviations at all. CONCLUSION: This result could characterize a lack of anticipatory coordinating gaze behavior in patients with right brain damage.

Muscle resistance to slow ramp weakly depends on activation level.

The mechanical response of human m. flexor pollicis longus to slow (3.2 degrees/s) linear stretch by 5.5 degrees was measured during sustained (45-60 s, 9-13.5 p.p.s.) unfused tetanus evoked by electrical stimulation. The stiffness increased during unfused tetanus. At the late phase of unfused tetanus it was 1.8 +/- 0.2 (mean +/- S.D.) times greater than at the early phase. The sensitivity of the isometric tension level to a short change in a stimulation frequency also increased. At the late phase of unfused tetanus force oscillations increased 1.2 +/- 0.2-fold during slow stretch or shortening and immediately reached a smaller amplitude after the cessation of length change. This was probably related to the friction and thixotropy in muscles. Muscle resistance to slow ramp depended only weakly on activation level. In the late phase of unfused tetanus the stiffness per unit force was 1.5 +/- 0.4 times greater at 9-13.5 p.p.s. than at 20-25 p.p.s. Thus, the relative value of muscle stiffness was greater for smaller activation levels typical for maintenance of posture. The enhancement of muscle stiffness during sustained unfused tetanus and a weak stiffness dependence on the activation level indicated a non-additivity of processes occurring in active muscle.

Integration of somatosensory and vestibular inputs in perceiving the direction of passive whole-body motion.

We investigated the contribution of somatosensory and vestibular inputs in the detection of the direction of linear whole-body displacement (1.5 m) at low levels of linear acceleration (peak acceleration 0.2 m/s2), in normal subjects. Subjects sat on a mobile robot wearing opaque goggles and headphones. They indicated the direction of motion by using a laser pointer held by the right hand at the level of the chin. Adaptation to a long-lasting static head turn (45 degrees to the right) was used to modify the perceived head orientation relative to the trunk. After about 15 min the head and trunk were perceived to be aligned with each other. After adaptation subjects pointed in the same direction as in the control condition in spite of the change in the perception of the head orientation. Because space orientated reactions to vestibular stimuli were previously shown to be coded in the perceived head reference frame, these results indicate that somatosensory cues are also integrated in the perception of linear motion. Unexpectedly, after adaptation, trunk and head perceived orientations were attracted toward the direction of the imposed motion. This suggests that the internal representation of body configuration depends also upon available cues from the extrapersonal space.

Non-specific directional adaptation to asymmetrical visual-vestibular stimulation.

Subjective estimates of passive whole-body rotations in darkness were evaluated before and after exposure to asymmetrical incoherent visual-vestibular stimulation (VVS). Two subjects who showed large capacity for adaptation to symmetrical incoherent VVS were enrolled in the study. Strikingly, after 45 min of asymmetrical left-right VVS, perception of rotation decreased equally for rotations to the right and to the left indicating that the calibration of vestibular sensory input for spatial orientation did not undergo a directional specific control.

The influence of head rotation on human upright posture during balanced bilateral vibration.

During a balanced bilateral vibration of tensor fasciae latae muscles evoking no evident postural changes in a standing human the slow head turns resulted in a pronounced lateral common gravity centre displacements to the 'occipital' side. Neck influences were most prominent at intermediate tonic background and were lacking both during very weak and strong vibratory stimulation in contrast to usual tonic vibratory reflex which becomes stronger with the increase of frequency. Body sway was induced not only by actual head turns but also by illusory ones evoked by neck muscle vibration. The neck influences on standing posture are therefore present in healthy adults, but they require a definite level of tonic readiness for their manifestation and are incorporated in the whole system of body scheme mechanisms.

Spatial, not temporal cues drive predictive orienting movements during navigation: a virtual reality study.

A fundamental property of the human brain is the ability to make predictions of future sensory and motor events. We have recently found that steering manoeuvres when walking along curvilinear trajectories are controlled by an anticipatory guidance of the direction of head (and eyes). However it is unclear whether a time-related or space-related signal triggers such anticipatory head orienting movements. By simulating navigation along a multi-legged virtual corridor we show that anticipatory orienting movements are triggered (in standing subjects) by reaching specific locations rather than by the time to the approaching corridor's bend. Similar to what happens in car driving, specific spatial features of the route rather than time to collision seem to drive steering.