Mechanical and metabolic requirements for active lateral stabilization in human walking

Walking appears to be passively unstable in the lateral direction, requiring active feedback control for stability. The central nervous system may control stability by adjusting medio-lateral foot placement, but potentially with a metabolic cost. This cost increases with narrow steps and may affect the preferred step width. We hypothesized that external stabilization of the body would reduce the active control needed, thereby decreasing metabolic cost and preferred step width. To test these hypotheses, we provided external lateral stabilization, using springs pulling bilaterally from the waist, to human subjects walking on a force treadmill at 1.25 m/s. Ten subjects walked, with and without stabilization, at a prescribed step width of zero and also at their preferred step width. We measured metabolic cost using indirect calorimetry, and step width from force treadmill data. We found that at the prescribed zero step width, external stabilization resulted in a 33% decrease in step width variability (root-mean-square) and a 9.2% decrease in metabolic cost. In the preferred step width conditions, external stabilization caused subjects to prefer a 47% narrower step width, with a 32% decrease in step width variability and a 5.7% decrease in metabolic cost. These results suggest that (a). human walking requires active lateral stabilization, (b). body lateral motion is partially stabilized via medio-lateral foot placement, (c). active stabilization exacts a modest metabolic cost, and (d). humans avoid narrow step widths because they are less stable.     

The effects of step width and arm swing on energetic cost and lateral balance during running

In walking, humans prefer a moderate step width that minimizes energetic cost and vary step width from step-to-step to maintain lateral balance. Arm swing also reduces energetic cost and improves lateral balance. In running, humans prefer a narrow step width that may present a challenge for maintaining lateral balance. However, arm swing in running may improve lateral balance and help reduce energetic cost. To understand the roles of step width and arm swing, we hypothesized that net metabolic power would be greater at step widths greater or less than preferred and when running without arm swing. We further hypothesized that step width variability (indicator of lateral balance) would be greater at step widths greater or less than preferred and when running without arm swing. Ten subjects ran (3m/s) at four target step widths (0%, 15%, 20%, and 25% leg length (LL)) with arm swing, at their preferred step width with arm swing, and at their preferred step width without arm swing. We measured metabolic power, step width, and step width variability. When subjects ran at target step widths less (0% LL) or greater (15%, 20%, and 25% LL) than preferred, both net metabolic power demand (by 3%, 9%, 12%, and 15%) and step width variability (by 7%, 33%, 46%, and 69%) increased. When running without arm swing, both net metabolic power demand (by 8%) and step width variability (by 9%) increased compared to running with arm swing. It appears that humans prefer to run with a narrow step width and swing their arms so as to minimize energetic cost and improve lateral balance.     

Running perturbations reveal general strategies for step frequency selection

Recent research has suggested that energy minimization in human walking involves both a fast preprogrammed process and a slow optimization process. Here, we studied human running to test whether these two processes represent control mechanisms specific to walking or a more general strategy for minimizing energetic cost in human locomotion. To accomplish this, we used free response experiments to enforce step frequency with a metronome at values above and below preferred step frequency and then determined the response times for the return to preferred steady-state step frequency when the auditory constraint was suddenly removed. In forced response experiments, we applied rapid changes in treadmill speed and examined response times for the processes involved in the consequent adjustments to step frequency. We then compared the dynamics of step frequency adjustments resulting from the two different perturbations to each other and to previous results found in walking. Despite the distinct perturbations applied in the two experiments, both responses were dominated by a fast process with a response time of 1.47 ± 0.05 s with fine-tuning provided by a slow process with a response time of 34.33 ± 0.50 s. The dynamics of the processes underlying step frequency adjustments in running match those found previously in walking, both in magnitude and relative importance. Our results suggest that the underlying mechanisms are fundamental strategies for minimizing energetic cost in human locomotion.     

Distinct fast and slow processes contribute to the selection of preferred step frequency during human walking

Humans spontaneously select a step frequency that minimizes the energy expenditure of walking. This selection might be embedded within the neural circuits that generate gait so that the optimum is pre-programmed for a given walking speed. Or perhaps step frequency is directly optimized, based on sensed feedback of energy expenditure. Direct optimization is expected to be slow due to the compounded effect of delays and iteration, whereas a pre-programmed mechanism presumably allows for faster step frequency selection, albeit dependent on prior experience. To test for both pre-programmed selection and direct optimization, we applied perturbations to treadmill walking to elicit transient changes in step frequency. We found that human step frequency adjustments (n = 7) occurred with two components, the first dominating the response (66 ± 10% of total amplitude change; mean ± SD) and occurring quite quickly (1.44 ± 1.14 s to complete 95% of total change). The other component was of smaller amplitude (35 ± 10% of total change) and took tens of seconds (27.56 ± 16.18 s for 95% completion). The fast process appeared to be too fast for direct optimization and more indicative of a pre-programmed response. It also persisted even with unusual closed-loop perturbations that conflicted with prior experience and rendered the response energetically suboptimal. The slow process was more consistent with the timing expected for direct optimization. Our interpretation of these results is that humans may rely heavily on pre-programmed gaits to rapidly select their preferred step frequency and then gradually fine-tune that selection with direct optimization.     

The cost of walking downhill: Is the preferred gait energetically optimal?

Humans tend to prefer walking patterns that minimize energetic cost, but must also maintain stability to avoid falling over. The relative importance of these two goals in determining the preferred gait pattern is not currently clear. We investigated the relationship between energetic cost and stability during downhill walking, a context in which gravitational energy will assist propulsion but may also reduce stability. We hypothesized that humans will not minimize energetic cost when walking downhill, but will instead prefer a gait pattern that increases stability. Simulations of a dynamic walking model were used to determine whether stable downhill gaits could be achieved using a simple control strategy. Experimentally, twelve healthy subjects walked downhill at 1.25 m/s (0, 0.05, 0.10, and 0.15 gradients). For each slope, subjects performed normal and relaxed trials, in which they were instructed to reduce muscle activity and allow gravity to maximally assist their gait. We quantified energetic cost, stride timing, and leg muscle activity. In our model simulations, increase in slope reduced the required actuation but also decreased stability. Experimental subjects behaved more like the model when using the relaxed rather than the normal walking strategy; the relaxed strategy decreased energetic cost at the steeper slopes but increased stride period variability, an indicator of instability. These results indicate that subjects do not take optimal advantage of the propulsion provided by gravity to decrease energetic cost, but instead prefer a more stable and more costly gait pattern.     

Mechanical and metabolic determinants of the preferred step width in human walking

We studied the selection of preferred step width in human walking by measuring mechanical and metabolic costs as a function of experimentally manipulated step width (0.00-0.45L, as a fraction of leg length L). We estimated mechanical costs from individual limb external mechanical work and metabolic costs using open circuit respirometry. The mechanical and metabolic costs both increased substantially (54 and 45%, respectively) for widths greater than the preferred value (0.15-0.45L) and with step width squared (R(2) = 0.91 and 0.83, respectively). As predicted by a three-dimensional model of walking mechanics, the increases in these costs appear to be a result of the mechanical work required for redirecting the centre of mass velocity during the transition between single stance phases (step-to-step transition costs). The metabolic cost for steps narrower than preferred (0.10-0.00L) increased by 8%, which was probably as a result of the added cost of moving the swing leg laterally in order to avoid the stance leg (lateral limb swing cost). Trade-offs between the step-to-step transition and lateral limb swing costs resulted in a minimum metabolic cost at a step width of 0.12L, which is not significantly different from foot width (0.11L) or the preferred step width (0.13L). Humans appear to prefer a step width that minimizes metabolic cost.     

Energy cost of balance control during walking decreases with external stabilizer stiffness independent of walking speed

Human walking requires active neuromuscular control to ensure stability in the lateral direction, which inflicts a certain metabolic load. The magnitude of this metabolic load has previously been investigated by means of passive external lateral stabilization via spring-like cords. In the present study, we applied this method to test two hypotheses: (1) the effect of external stabilization on energy cost depends on the stiffness of the stabilizing springs, and (2) the energy cost for balance control, and consequently the effect of external stabilization on energy cost, depends on walking speed. Fourteen healthy young adults walked on a motor driven treadmill without stabilization and with stabilization with four different spring stiffnesses (between 760 and 1820 N m⁻¹) at three walking speeds (70%, 100%, and 130% of preferred speed). Energy cost was calculated from breath-by-breath oxygen consumption. Gait parameters (mean and variability of step width and stride length, and variability of trunk accelerations) were calculated from kinematic data. On average external stabilization led to a decrease in energy cost of 6% (p<0.005) as well as a decrease in step width (24%; p<0.001), step width variability (41%; p<0.001) and variability of medio-lateral trunk acceleration (12.5%; p<0.005). Increasing stabilizer stiffness increased the effects on both energy cost and medio-lateral gait parameters up to a stiffness of 1260 N m⁻¹. Contrary to expectations, the effect of stabilization was independent of walking speed (p=0.111). These results show that active lateral stabilization during walking involves an energetic cost, which is independent of walking speed.     

Lateral stabilization improves walking in people with myelomeningocele

Muscle weakness and sensory deficits in people with myelomeningocele (MMC) make their walking control a greater challenge. We know little about how people with MMC optimize their walking balance. Recently, researchers have argued that medial-lateral control of gait requires more active neural input than the anterior-posterior direction, which is more passive. Our goal was to investigate the effect of providing external lateral stabilization (ELS) on walking patterns in people with MMC. We examined 12 people with MMC who could perform at least 4-6 independent steps. We found that the normalized step width (SW) was decreased 20% from without stabilizer to with stabilizer, where as the normalized step length (SL) was increased 4.17% from without stabilizer to with stabilizer. The ELS resulted in 25.10% reduction in centre of mass (COM) ranges of motions in the medial-lateral direction and 13.43% reduction in pelvic range of motions in the frontal plane. Our results suggested that by decreasing the medial-lateral control demands in people with MMC, we could improve gait with smaller SW, longer SL as well as reduced COM and pelvic ranges of motion in the frontal plane. In addition, ELS decreased energy cost and muscle co-activation of soleus and vastus lateralis that may help in diminishing the chances of pain and fatigue in people with MMC. Exploring the effect of the ELS provided us information that might be used to increase mobility safety and to develop a superior rehabilitation intervention for people with MMC.     

The energetic cost of maintaining lateral balance during human running

To quantify the energetic cost of maintaining lateral balance during human running, we provided external lateral stabilization (LS) while running with and without arm swing and measured changes in energetic cost and step width variability (indicator of lateral balance). We hypothesized that external LS would reduce energetic cost and step width variability of running (3.0 m/s), both with and without arm swing. We further hypothesized that the reduction in energetic cost and step width variability would be greater when running without arm swing compared with running with arm swing. We controlled for step width by having subjects run along a single line (zero target step width), which eliminated any interaction effects of step width and arm swing. We implemented a repeated-measures ANOVA with two within-subjects fixed factors (external LS and arm swing) to evaluate main and interaction effects. When provided with external LS (main effect), subjects reduced net metabolic power by 2.0% (P = 0.032) and step width variability by 12.3% (P = 0.005). Eliminating arm swing (main effect) increased net metabolic power by 7.6% (P < 0.001) but did not change step width variability (P = 0.975). We did not detect a significant interaction effect between external LS and arm swing. Thus, when comparing conditions of running with or without arm swing, external LS resulted in a similar reduction in net metabolic power and step width variability. We infer that the 2% reduction in the net energetic cost of running with external LS reflects the energetic cost of maintaining lateral balance. Furthermore, while eliminating arm swing increased the energetic cost of running overall, arm swing does not appear to assist with lateral balance. Our data suggest that humans use step width adjustments as the primary mechanism to maintain lateral balance during running.     

Sideways walking: preferred is slow,slow is optimal,and optimal is expensive

When humans wish to move sideways, they almost never walk sideways, except for a step or two; they usually turn and walk facing forward. Here, we show that the experimental metabolic cost of walking sideways, per unit distance, is over three times that of forward walking. We explain this high metabolic cost with a simple mathematical model; sideways walking is expensive because it involves repeated starting and stopping. When walking sideways, our subjects preferred a low natural speed, averaging 0.575 m s⁻¹ (0.123 s.d.). Even with no prior practice, this preferred sideways walking speed is close to the metabolically optimal speed, averaging 0.610 m s⁻¹ (0.064 s.d.). Subjects were within 2.4% of their optimal metabolic cost per distance. Thus, we argue that sideways walking is avoided because it is expensive and slow, and it is slow because the optimal speed is low, not because humans cannot move sideways fast.     

Energetics of walking and running: insights from simulated reduced-gravity experiments.

On Earth, a person uses about one-half as much energy to walk a mile as to run a mile. On another planet with lower gravity, would walking still be more economical than running? When people carry weights while they walk or run, energetic cost increases in proportion to the added load. It would seem to follow that if gravity were reduced, energetic cost would decrease in proportion to body weight in both gaits. However, we find that under simulated reduced gravity, the rate of energy consumption decreases in proportion to body weight during running but not during walking. When gravity is reduced by 75%, the rate of energy consumption is reduced by 72% during running but only by 33% during walking. Because reducing gravity decreases the energetic cost much more for running than for walking, walking is not the cheapest way to travel a mile at low levels of gravity. These results suggest that the link between the mechanics of locomotion and energetic cost is fundamentally different for walking and for running.     

Bioenergetics and the origin of hominid bipedalism

Compared to most quadrupedal mammals, humans are energetically inefficient when running at high speeds. This fact can be taken to mean that human bipedalism evolved for reasons other than to reduce relative energy cost during locomotion. Recalculation of the energy expended during human walking at normal speeds shows that (1) human bipedalism is at least as efficient as typical mammalian quadrupedalism and (2) human gait is much more efficient than bipedal or quadrupedal locomotion in the chimpanzee. We conclude that bipedalism bestowed an energetic advantage on the Miocene hominoid ancestors of the Hominidae.     

Energy cost of walking and gait instability in healthy 65- and 80-yr-olds.

This study tested whether the lower economy of walking in healthy elderly subjects is due to greater gait instability. We compared the energy cost of walking and gait instability (assessed by stride to stride changes in the stride time) in octogenarians (G80, n = 10), 65-yr-olds (G65, n = 10), and young controls (G25, n = 10) walking on a treadmill at six different speeds. The energy cost of walking was higher for G80 than for G25 across the different walking speeds (P < 0.05). Stride time variability at preferred walking speed was significantly greater in G80 (2.31 +/- 0.68%) and G65 (1.93 +/- 0.39%) compared with G25 (1.40 +/- 0.30%; P < 0.05). There was no significant correlation between gait instability and energy cost of walking at preferred walking speed. These findings demonstrated greater energy expenditure in healthy elderly subjects while walking and increased gait instability. However, no relationship was noted between these two variables. The increase in energy cost is probably multifactorial, and our results suggest that gait instability is probably not the main contributing factor in this population. We thus concluded that other mechanisms, such as the energy expenditure associated with walking movements and related to mechanical work, or neuromuscular factors, are more likely involved in the higher cost of walking in elderly people.     

Bionic ankle-foot prosthesis normalizes walking gait for persons with leg amputation

Over time, leg prostheses have improved in design, but have been incapable of actively adapting to different walking velocities in a manner comparable to a biological limb. People with a leg amputation using such commercially available passive-elastic prostheses require significantly more metabolic energy to walk at the same velocities, prefer to walk slower and have abnormal biomechanics compared with non-amputees. A bionic prosthesis has been developed that emulates the function of a biological ankle during level-ground walking, specifically providing the net positive work required for a range of walking velocities. We compared metabolic energy costs, preferred velocities and biomechanical patterns of seven people with a unilateral transtibial amputation using the bionic prosthesis and using their own passive-elastic prosthesis to those of seven non-amputees during level-ground walking. Compared with using a passive-elastic prosthesis, using the bionic prosthesis decreased metabolic cost by 8 per cent, increased trailing prosthetic leg mechanical work by 57 per cent and decreased the leading biological leg mechanical work by 10 per cent, on average, across walking velocities of 0.75-1.75 m s(-1) and increased preferred walking velocity by 23 per cent. Using the bionic prosthesis resulted in metabolic energy costs, preferred walking velocities and biomechanical patterns that were not significantly different from people without an amputation.     

Limitations imposed by wearing armour on Medieval soldiers' locomotor performance

In Medieval Europe, soldiers wore steel plate armour for protection during warfare. Armour design reflected a trade-off between protection and mobility it offered the wearer. By the fifteenth century, a typical suit of field armour weighed between 30 and 50 kg and was distributed over the entire body. How much wearing armour affected Medieval soldiers' locomotor energetics and biomechanics is unknown. We investigated the mechanics and the energetic cost of locomotion in armour, and determined the effects on physical performance. We found that the net cost of locomotion (C(met)) during armoured walking and running is much more energetically expensive than unloaded locomotion. C(met) for locomotion in armour was 2.1-2.3 times higher for walking, and 1.9 times higher for running when compared with C(met) for unloaded locomotion at the same speed. An important component of the increased energy use results from the extra force that must be generated to support the additional mass. However, the energetic cost of locomotion in armour was also much higher than equivalent trunk loading. This additional cost is mostly explained by the increased energy required to swing the limbs and impaired breathing. Our findings can predict age-associated decline in Medieval soldiers' physical performance, and have potential implications in understanding the outcomes of past European military battles.     

Do Humans Optimally Exploit Redundancy to Control Step Variability in Walking?

It is widely accepted that humans and animals minimize energetic cost while walking. While such principles predict average behavior, they do not explain the variability observed in walking. For robust performance, walking movements must adapt at each step, not just on average. Here, we propose an analytical framework that reconciles issues of optimality, redundancy, and stochasticity. For human treadmill walking, we defined a goal function to formulate a precise mathematical definition of one possible control strategy: maintain constant speed at each stride. We recorded stride times and stride lengths from healthy subjects walking at five speeds. The specified goal function yielded a decomposition of stride-to-stride variations into new gait variables explicitly related to achieving the hypothesized strategy. Subjects exhibited greatly decreased variability for goal-relevant gait fluctuations directly related to achieving this strategy, but far greater variability for goal-irrelevant fluctuations. More importantly, humans immediately corrected goal-relevant deviations at each successive stride, while allowing goal-irrelevant deviations to persist across multiple strides. To demonstrate that this was not the only strategy people could have used to successfully accomplish the task, we created three surrogate data sets. Each tested a specific alternative hypothesis that subjects used a different strategy that made no reference to the hypothesized goal function. Humans did not adopt any of these viable alternative strategies. Finally, we developed a sequence of stochastic control models of stride-to-stride variability for walking, based on the Minimum Intervention Principle. We demonstrate that healthy humans are not precisely “optimal,” but instead consistently slightly over-correct small deviations in walking speed at each stride. Our results reveal a new governing principle for regulating stride-to-stride fluctuations in human walking that acts independently of, but in parallel with, minimizing energetic cost. Thus, humans exploit task redundancies to achieve robust control while minimizing effort and allowing potentially beneficial motor variability.     

Energetic Consequences of Human Sociality: Walking Speed Choices among Friendly Dyads

Research has shown that individuals have an optimal walking speed–a speed which minimizes energy expenditure for a given distance. Because the optimal walking speed varies with mass and lower limb length, it also varies with sex, with males in any given population tending to have faster optimal walking speeds. This potentially creates an energetic dilemma for mixed-sex walking groups. Here we examine speed choices made by individuals of varying stature, mass, and sex walking together. Individuals (N = 22) walked around a track alone, with a significant other (with and without holding hands), and with friends of the same and opposite sex while their speeds were recorded every 100 m. Our findings show that males walk at a significantly slower pace to match the females’ paces (p = 0.009), when the female is their romantic partner. The paces of friends of either same or mixed sex walking together did not significantly change (p>0.05). Thus significant pace adjustment appears to be limited to romantic partners. These findings have implications for both mobility and reproductive strategies of groups. Because the male carries the energetic burden by adjusting his pace (slowing down 7%), the female is spared the potentially increased caloric cost required to walk together. In energetically demanding environments, we will expect to find gender segregation in group composition, particularly when travelling longer distances.     

Muscle mechanical work requirements during normal walking: the energetic cost of raising the body's center-of-mass is significant

Inverted pendulum models of walking predict that little muscle work is required for the exchange of body potential and kinetic energy in single-limb support. External power during walking (product of the measured ground reaction force and body center-of-mass (COM) velocity) is often analyzed to deduce net work output or mechanical energetic cost by muscles. Based on external power analyses and inverted pendulum theory, it has been suggested that a primary mechanical energetic cost may be associated with the mechanical work required to redirect the COM motion at the step-to-step transition. However, these models do not capture the multi-muscle, multi-segmental properties of walking, co-excitation of muscles to coordinate segmental energetic flow, and simultaneous production of positive and negative muscle work. In this study, a muscle-actuated forward dynamic simulation of walking was used to assess whether: (1). potential and kinetic energy of the body are exchanged with little muscle work; (2). external mechanical power can estimate the mechanical energetic cost for muscles; and (3.) the net work output and the mechanical energetic cost for muscles occurs mostly in double support. We found that the net work output by muscles cannot be estimated from external power and was the highest when the COM moved upward in early single-limb support even though kinetic and potential energy were exchanged, and muscle mechanical (and most likely metabolic) energetic cost is dominated not only by the need to redirect the COM in double support but also by the need to raise the COM in single support.     

The metabolic cost of changing walking speeds is significant,implies lower optimal speeds for shorter distances,and increases daily energy estimates

Humans do not generally walk at constant speed, except perhaps on a treadmill. Normal walking involves starting, stopping and changing speeds, in addition to roughly steady locomotion. Here, we measure the metabolic energy cost of walking when changing speed. Subjects (healthy adults) walked with oscillating speeds on a constant-speed treadmill, alternating between walking slower and faster than the treadmill belt, moving back and forth in the laboratory frame. The metabolic rate for oscillating-speed walking was significantly higher than that for constant-speed walking (6–20% cost increase for ±0.13–0.27 m s⁻¹ speed fluctuations). The metabolic rate increase was correlated with two models: a model based on kinetic energy fluctuations and an inverted pendulum walking model, optimized for oscillating-speed constraints. The cost of changing speeds may have behavioural implications: we predicted that the energy-optimal walking speed is lower for shorter distances. We measured preferred human walking speeds for different walking distances and found people preferred lower walking speeds for shorter distances as predicted. Further, analysing published daily walking-bout distributions, we estimate that the cost of changing speeds is 4–8% of daily walking energy budget.     

Increasing step width reduces the requirements for subtalar joint moments and powers

The subtalar joint (STJ) contributes to the absorption and generation of mechanical energy (and power) during walking to maintain frontal plane stability. Previous observational studies have suggested that there may be a relationship between step width and STJ supination moment. This study directly tests the hypothesis that walking with a step width greater than preferred would reduce STJ moments, energy absorption, and power generation requirements, while increasing energy absorption at the hip during initial contact. Participants (n = 12, 7 females) were asked to walk on an instrumented treadmill at a constant velocity and cadence at a range of fixed step widths ranging from 0.1 to 0.4 times leg length (L). Walking at step widths greater than preferred (0.149 ± 0.04 L) reduced peak STJ moments at initial contact and propulsion which subsequently reduced the negative and positive work performed at the STJ. There was a 43% reduction in energy absorption (negative work) and approximately 30% decrease in positive work at the STJ as step width increased from 0.1 L to 0.4 L. An increase in energy absorption at the knee and hip was evident with an increase in step width during initial contact, although minimal mechanical changes were observed at the proximal joints during propulsion. These results suggest an increase in step width reduces the forces generated by muscles at the STJ across stance and is therefore likely to be beneficial in the prevention and treatment of their injuries. In terms of rehabilitation, the increase in mechanical costs occurring due to an increase in energy absorption by the hip and knee is of minimal concern.