biomechanics sideways walking: preferred is slow, slow is ...€¦ · similar to point-mass models...

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rsbl.royalsocietypublishing.org Research Cite this article: Handford ML, Srinivasan M. 2014 Sideways walking: preferred is slow, slow is optimal, and optimal is expensive. Biol. Lett. 10: 20131006. http://dx.doi.org/10.1098/rsbl.2013.1006 Received: 27 November 2013 Accepted: 19 December 2013 Subject Areas: biomechanics, behaviour Keywords: legged locomotion, walking, metabolic energy cost, optimality, minimization, mathematical model Author for correspondence: Manoj Srinivasan e-mail: [email protected] Electronic supplementary material is available at http://dx.doi.org/10.1098/rsbl.2013.1006 or via http://rsbl.royalsocietypublishing.org. Biomechanics Sideways walking: preferred is slow, slow is optimal, and optimal is expensive Matthew L. Handford and Manoj Srinivasan Mechanical and Aerospace Engineering, The Ohio State University, Columbus, OH 43210, USA 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 21 (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 21 (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. 1. Introduction Humans walk and run in a manner that approximately minimizes metabolic energy expenditure [1–4]. However, most evidence for metabolic energy optimality has been for natural gaits, such as walking and running. Here, we examine optimality in an unnatural movement: a sideways walking gait (figure 1a). With human subject experiments, we show that the sideways walk- ing speeds which humans prefer are close to minimizing the metabolic cost per distance. Both experiment and mathematical models suggest that the metabolic cost of sideways walking is significantly higher than normal walking. This high cost suggests why people rarely walk sideways even when they wish to move sideways. 2. Material and methods (a) Experimental protocol The protocol was approved by the Ohio State University’s Institutional Review Board. Subjects gave informed consent. The subjects were 10 healthy adults (50% males : females), with mean age 27.5 years (12.5 s.d., range 19–52), mean height 173.8 cm (8.0 s.d.) and mean mass 73.2 kg (13.5 s.d.). First, before extensive practice in walking sideways, the subjects were asked to walk sideways for 61 m in a hallway at a speed they found comfortable. They reversed direction mid-way (30.5 m), switching their leading leg. The ‘pre-treadmill’ preferred speed was estimated by timing and averaging four such trials. Next, the subjects walked sideways on a treadmill, with their preferred leg lead- ing. We used seven to nine treadmill trials (80 trials across 10 subjects), with speeds 0.1 – 1.0 m s 21 , the top speed adapted to the subject’s comfort level. Metabolic rates were estimated with a metabolic measurement system (Oxycon Mobile, mass 1 kg), which measures respiratory oxygen and carbon dioxide flux. We approximate the metabolic rate per unit mass in W kg 21 by _ E ¼ 16:58 _ V O2 þ4:51 _ V CO2 ; where _ V is in ml s 21 kg 21 [5]. Each treadmill trial lasted 6 min: 3 min to reach a steady state and 3 min to estimate an average steady state metabolic rate. Resting metabolic rate was measured while sitting before the treadmill trials. & 2014 The Author(s) Published by the Royal Society. All rights reserved. on January 20, 2014 rsbl.royalsocietypublishing.org Downloaded from

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Page 1: Biomechanics Sideways walking: preferred is slow, slow is ...€¦ · similar to point-mass models used for forward walking [6,7]. This biped has the upper body mass m centred at

rsbl.royalsocietypublishing.org

ResearchCite this article: Handford ML, Srinivasan M.2014 Sideways walking: preferred is slow, slowis optimal, and optimal is expensive. Biol. Lett.10: 20131006.http://dx.doi.org/10.1098/rsbl.2013.1006

Received: 27 November 2013Accepted: 19 December 2013

Subject Areas:biomechanics, behaviour

Keywords:legged locomotion, walking, metabolic energycost, optimality, minimization,mathematical model

Author for correspondence:Manoj Srinivasane-mail: [email protected]

Electronic supplementary material is availableat http://dx.doi.org/10.1098/rsbl.2013.1006 orvia http://rsbl.royalsocietypublishing.org.

Biomechanics

Sideways walking: preferred is slow, slowis optimal, and optimal is expensiveMatthew L. Handford and Manoj Srinivasan

Mechanical and Aerospace Engineering, The Ohio State University, Columbus, OH 43210, USA

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, perunit distance, is over three times that of forward walking. We explain thishigh metabolic cost with a simple mathematical model; sideways walkingis expensive because it involves repeated starting and stopping. Whenwalking sideways, our subjects preferred a low natural speed, averaging0.575 m s21 (0.123 s.d.). Even with no prior practice, this preferred sidewayswalking speed is close to the metabolically optimal speed, averaging0.610 m s21 (0.064 s.d.). Subjects were within 2.4% of their optimal metaboliccost per distance. Thus, we argue that sideways walking is avoided becauseit is expensive and slow, and it is slow because the optimal speed is low, notbecause humans cannot move sideways fast.

1. IntroductionHumans walk and run in a manner that approximately minimizes metabolicenergy expenditure [1–4]. However, most evidence for metabolic energyoptimality has been for natural gaits, such as walking and running. Here, weexamine optimality in an unnatural movement: a sideways walking gait(figure 1a). With human subject experiments, we show that the sideways walk-ing speeds which humans prefer are close to minimizing the metabolic cost perdistance. Both experiment and mathematical models suggest that the metaboliccost of sideways walking is significantly higher than normal walking. Thishigh cost suggests why people rarely walk sideways even when they wish tomove sideways.

2. Material and methods(a) Experimental protocolThe protocol was approved by the Ohio State University’s Institutional ReviewBoard. Subjects gave informed consent. The subjects were 10 healthy adults (50%males : females), with mean age 27.5 years (12.5 s.d., range 19–52), mean height173.8 cm (8.0 s.d.) and mean mass 73.2 kg (13.5 s.d.).

First, before extensive practice in walking sideways, the subjects were asked towalk sideways for 61 m in a hallway at a speed they found comfortable. Theyreversed direction mid-way (30.5 m), switching their leading leg. The ‘pre-treadmill’preferred speed was estimated by timing and averaging four such trials.

Next, the subjects walked sideways on a treadmill, with their preferred leg lead-ing. We used seven to nine treadmill trials (80 trials across 10 subjects), with speeds0.1–1.0 m s21, the top speed adapted to the subject’s comfort level. Metabolic rateswere estimated with a metabolic measurement system (Oxycon Mobile, mass 1 kg),which measures respiratory oxygen and carbon dioxide flux. We approximate themetabolic rate per unit mass in W kg21 by _E ¼ 16:58 _VO2 þ4:51 _VCO2 ; where _V isin ml s21 kg21 [5]. Each treadmill trial lasted 6 min: 3 min to reach a steady stateand 3 min to estimate an average steady state metabolic rate. Resting metabolicrate was measured while sitting before the treadmill trials.

& 2014 The Author(s) Published by the Royal Society. All rights reserved.

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After the treadmill trials, the preferred speeds weremeasured again in the hallway. During the hallway trials, thesubjects wore the metabolic equipment, but no metabolicmeasurements were made. We do not discuss the post-treadmillpreferred speeds because subjects had different cool-down proto-cols after the treadmill trials.

(b) Mathematical modelWe consider a simple mathematical model of a biped (figure 2a),similar to point-mass models used for forward walking [6,7].This biped has the upper body mass m centred at the hip, withhigh moment of inertia, so that the hip muscles can torque theleg forward by reacting against this upper body. During single

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Figure 1. Sideways walking experiment and energetics. (a) Sideways walking gait. Subjects faced perpendicular to their travel direction, never crossed their feet andalways had at least one foot on the ground. (b) Mass-normalized metabolic rate for all subjects (different markers) and a quadratic speed-dependence fit to thepooled data from all subjects (red curve). Metabolic rate for normal (forward) walking [2] is also shown. (c) Mass-normalized metabolic cost per unit distance forsideways walking. The best fit curves for sideways walking (red line) and normal walking (blue line [2]) are shown. The dark green vertical line indicates the optimalspeed (0.612 m s21) from the pooled data. The light green band (0.531 – 0.705 m s21) is the range of speeds with less than a 1% increase over the optimalmetabolic cost per distance. Displayed below the graph are the subjects’ optimal speeds, post-treadmill preferred speeds and pre-treadmill preferred speeds.

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Figure 2. Sideways walking model. (a) An idealized biped with the upper body mass centred at the hip, performing idealized sideways walking. The sequence ofhip lowering, foot-strike and push-off impulses, hip raising and vertical rest phases is shown. (b) The metabolic rates of sideways and forward walking obtained fromthe simple mathematical models with foot-strike preceding push-off and vice versa for fixed step length dstep ¼ ‘/2 and ‘ ¼ 1 m; no leg-swing or resting cost.(c) Sideways walking metabolic cost per distance from experiment and model (two versions) with leg-swing cost and unconstrained (optimally chosen) step lengths.The optimal speeds from experiment and model are shown.

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stance, ignoring the swing leg, the biped is an inverted pendu-lum with a clockwise hip torque t, described by the equations:m‘2 €uþmg‘ sin u ¼ t; with leg angle u measured clockwise fromthe vertical (u ¼ 0), acceleration due to gravity g and leg length ‘.

For this biped model, an idealized sideways walking gait isdescribed in figure 2a (see also the electronic supplementarymaterial, animation). This gait starts and returns every stride toa vertical position with angular rate _u ¼ 0: Starting at the verticalposition, finite positive work is performed by a hip-torqueimpulse, taking the angular rate _u from zero to some finitequantity instantaneously. The inverted pendulum then coastspassively, lowering the hip, until a foot-strike and push-offimpulse achieve a step-to-step transition. The inverted pendulumcoasts passively, raising the hip until the leg is vertical again,when a hip-torque impulse decelerates _u back to zero.

Consider walking with average forward speed v, step lengthdstep and step period Tstep ¼ dstep/v. For lowering the hip, theinitial leg angle at t ¼ 0 is u(0) ¼ 0. We solve for the initialangular rate _uð0þÞ just after the accelerating torque impulse, sothat the passive inverted pendulum motion reaches the step-to-step transition leg angle uðTstep/2Þ ¼ a ¼ sin%1ðdstep/2‘Þ in halfthe step period, Tstep/2. The hip speed at this time isv% ¼ ‘ _uðTstep/2Þ:

The initial kinetic energy 12 m‘2 _uð0þÞ2 is the positive

work performed by the hip-torque impulse. The foot-strike andpush-off impulses perform negative and positive work of equalmagnitude: 1

2 mjv%j2(1% cos22a/cos2a) when foot-strike precedespush-off and 1

2 m jv%j2 tan2a when push-off precedes foot-strike.Raising the hip is the reverse of lowering the hip, switching posi-tive and negative work. Metabolic cost is modelled as a weightedsum of positive and negative work, scaled by their respectiveefficiency reciprocals, b1 ¼ 4 and b2 ¼ 1 [7]. In addition to thismetabolic cost, for some comparisons, we added a leg-swingcost and a constant metabolic rate, equal to erest or a0, to themodel (otherwise, model has zero metabolic rate at zerospeed); for these comparisons, we found the optimal steplength and metabolic cost at every speed (see electronicsupplementary material, S3).

We performed analogous calculations for forward walking,one model with foot-strike (usually called heel-strike [7–9])before push-off and another with the impulse sequence reversed[7,9]. Forward walking models differ from sideways walkingmodels only in that they do not have a vertical rest position ateach step. See the electronic supplementary material for adetailed derivation, methods and computer programs.

3. ResultsThe resting metabolic rate per unit mass, erest, averaged1.542 W kg21 (s.d. 0.222). The sideways walking metabolicrate increased monotonically with speed v (figure 1b). Similarto normal walking [2,4,10], the total sideways walking meta-bolic rate per unit mass, _E (including the resting cost), isapproximated well, using least squares, by: _E ¼ a0 þ a2v2:

For metabolic rate data pooled over the subjectpopulation (figure 1b), a0 ¼ 2.742 W kg21 and a2 ¼7.313 W (m s21)22 kg21. Fitting the data from individual sub-jects separately and then averaging the coefficients gives:"a0 ¼ 2:746 W kg%1 and "a2 ¼ 7:306 W (m s%1Þ%2 kg%1. See theelectronic supplementary material, S4 for these coefficients’error estimates. Note that zero-speed cost a0 . erest, as alsofound for forward walking ([2,4]; electronic supplementarymaterial, S5).

The total metabolic cost per unit distance per unit massis given by E0 ¼ _E/v ¼ a0/vþ a2v (see [10]), shown in figure1c. The speed that minimizes E0 is given by

vopt ¼ffiffiffiffiffiffiffiffiffiffiffia0/a2p

¼ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi2:742/7:313p

¼ 0:612 m s%1 (s.d. 0.027; 95%CI 0.495–0.754 m s21).

By subtracting resting cost, we get the net metabolicrate _Enet ¼ _E% erest: The net metabolic cost per unit distanceE0net ¼ _Enet /v is minimized at speed vopt;net ¼ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiða0 % erestÞ/a2

p¼ 0:405 m s%1. Not subtracting the resting

cost gives the ‘maximum range speed’, the speed whichmaximizes distance for given energy [10]. For forward walk-ing, vopt (about 1.3–1.4 m s21) is much closer to the preferredwalking speeds than vopt,net (about 0.7–0.9 m s21); see [10]for a review of these issues. Here, we use vopt as the predictedoptimal speed.

The subject-specific optimal speeds, obtained from indivi-dual fits, averaged 0.610 m s21 (s.d. 0.064). Preferred hallwaywalking speeds before and after the treadmill trials aver-aged 0.575 m s21 (s.d. 0.123) and 0.649 m s21 (s.d. 0.111),respectively. These speeds are shown in figure 1c.

The metabolically optimal speeds and the pre-treadmillpreferred speeds have similar means, differing only by0.035 m s21. The subjects’ individual optimal speeds differedfrom their pre-treadmill speeds by a mean absolute differenceof 0.12 m s21, corresponding to an increase of 2.4% in E0 overoptimal. Furthermore, out of the 10 subjects, five chose aspeed with an E0 within 1% of the optimal (the green bandin figure 1c). Thus, the subjects are not far from optimal.

From prior research, forward walking has a0 & 2.1 W kg21

and a2 & 121.5 W (m s21)22 kg21 [2,4]. For matched speedsbelow 1 m s21, the net metabolic rate _Enet of sideways walkingis three to five times that of forward walking. The optimal side-ways walking speed (0.612 m s21) is only half as fast as theoptimal forward walking speed (1.25–1.35 m s21 [2,10]). Attheir respective optimal speeds, the optimal sideways meta-bolic cost per distance E0 (8.95 J m21 kg21) is about threetimes the optimal forward E0 (3.2 J m21 kg21).

Our mathematical model of sideways walking also has amuch higher cost than similar inverted pendulum models offorward walking, thus qualitatively explaining the vast differ-ence in measured costs (figure 2b, ignoring leg-swing cost). Inthese models, compared with optimal inverted pendulumforward walking [7,9], the metabolic rate of sideways walkingis about 3–10 times higher at 1 m s21 depending on whetherfoot-strike or push-off is assumed to occur first for both gaits;the costs are similar at infinitesimal speeds. While the modelwith leg-swing cost still underestimates the metabolic cost(figure 2c), it predicts an optimal speed of 0.5319 m s21

when erest is added and 0.6420 m s21 when a0 is added (seethe electronic supplementary material, S3).

4. DiscussionHumans likely prefer a slow sideways walk because of thelow optimal speed. While subjects stayed within 1–2% ofoptimal metabolic cost at their preferred speeds, their pre-ferred speeds were highly variable. This variability isperhaps inevitable given the insensitivity of E0 to speed,near the optimal speed (low curvature). Such insensitivity,if typical, might make predicting human coordination frommetabolic optimality inaccurate [7], even if humans wereclose to optimal. However, this speed variability maydecrease with sufficient practice.

Slow speeds in humans with mobility issues is sometimesimplicitly attributed to an inability to walk faster (e.g. [11]).

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However, as argued here for sideways walking, humans walkclose to their (slow) metabolically optimal speeds even whileusing prostheses and crutches [2].

Sideways walking has a high metabolic cost e.g. at 1 m s21,it has the same gross metabolic rate as running at 2.3 m s21

(see the electronic supplementary material, S1, for othercomparisons). Nevertheless, humans often use one or twosideways steps when they wish to move sideways a short dis-tance e.g. while working at a kitchen counter or self-organizingfor a group photograph. But when humans wish to move side-ways for longer distances, they simply turn and walk facingforward. Here, the one-time turning cost is compensated bythe substantial cost reduction by walking forward. Measuringthe turning cost will let us predict the distance under whichhumans step sideways as opposed to turn and walk forward.

In our mathematical model, we used a work-based meta-bolic cost, found appropriate also for forward humanwalking [8,12], neglecting force-related terms [12,13], whichmay explain the model’s underestimation. The model’swork estimates are an approximate lower bound for the

leg work and will require a corresponding metabolic cost,assuming negligible elastic recovery mechanisms.

Sideways walking involves no knee flexion and the anklepronation–supination is much smaller than the plantarflex-ion–dorsiflexion in forward walking. Given such kinematicsimplicity, sideways walking may serve as a simpler taskfor studying locomotion energetics, perhaps requiring sim-pler muscle-driven human models than necessary forforward walking. Inverted pendulum-like walking modelsmay also be better suited to sideways walking than forwardwalking. Studying such simplified tasks might bridge thegap between studying isolated limb movements such as legswing and studying normal walking.

Acknowledgements. We are grateful for the treadmill facilities providedby Emily Martini and Carmen Swain, and to Geoff Brown for initialassistance.Funding statement. This article was partly supported by NSF grant nos.CMMI-1254842 and CMMI-1300655.

References

1. Hogberg P. 1952 How do stride length and stridefrequency influence the energy-output duringrunning? Arbeitsphysiologie 14, 437 – 441.

2. Ralston HJ. 1958 Energy – speed relation andoptimal speed during level walking. Eur. J. Appl.Physiol. 17, 277 – 283. (doi:10.1007/BF00698754)

3. Alexander RM. 2003 Principles of animal locomotion.Princeton, NJ: Princeton University Press.

4. Long LL, Srinivasan M. 2013 Walking, running, andresting under time, distance, and average speedconstraints: optimality of walk-run-rest mixtures.J. R. Soc. Interface 10, 20120980. (doi:10.1098/rsif.2012.0980)

5. Brockway JM. 1987 Derivation of formulae used tocalculate energy expenditure in man. Hum. Nutr.Clin. Nutr. 41C, 463 – 471.

6. Srinivasan M, Ruina A. 2006 Computer optimizationof a minimal biped model discovers walking andrunning. Nature 439, 72 – 75. (doi:10.1038/nature04113)

7. Srinivasan M. 2011 Fifteen observations on thestructure of energy minimizing gaits in manysimple biped models. J. R. Soc. Interface 8, 74 – 98.(doi:10.1098/rsif.2009.0544)

8. Donelan JM, Kram R, Kuo AD. 2002 Mechanicalwork for step-to-step transitions is a majordeterminant of the metabolic cost of humanwalking. J. Exp. Biol. 205, 3717 – 3727.

9. Ruina A, Bertram JE, Srinivasan M. 2005 Acollisional model of the energetic cost of supportwork qualitatively explains leg-sequencing inwalking and galloping, pseudo-elastic leg behavior

in running and the walk-to-run transition. J. Theor.Biol. 14, 170 – 192. (doi:10.1016/j.jtbi.2005.04.004)

10. Srinivasan M. 2009 Optimal speeds for walking andrunning, and walking on a moving walkway. CHAOS19, 026112. (doi:10.1063/1.3141428)

11. Bendall MJ, Bassey EJ, Pearson MB. 1989 Factorsaffecting walking speed of elderly people. AgeAgeing 18, 327 – 332. (doi:10.1093/ageing/18.5.327)

12. Griffin TM, Roberts TJ, Kram R. 2003 Metabolic costof generating muscular force in human walking:insights from load-carrying and speed experiments.J. Appl. Physiol. 95, 172 – 183.

13. Doke J, Donelan MJ, Kuo AD. 2005 Mechanics andenergetics of swinging the human leg. J. Exp. Biol.208, 439 – 445. (doi:10.1242/jeb.01408)

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Supplementary Information Appendix for the article:

Sideways walking: preferred is slow, slow is optimal,

and optimal is expensive

Matthew L. Handford and Manoj Srinivasan⇤

Mechanical and Aerospace Engineering,The Ohio State University, Columbus OH 43210, USA

The Supplementary Information has four components: (1) a Supplementary Information Ap-pendix (namely, this document). (2) Experimental data, as a text file. (3) Video animation ofthe inverted pendulum walking, forward and sideways. (4) Computer programs which perform themodel predictions, described below in greater detail.

(1) Supplementary Information Appendix (this document). This appendix has five sec-tions S1 to S5 and four figures S1 to S4. The sections S1 to S5 respectively describe:

• Section S1. Comparison of other activities to sideways walking costs.

• Section S2. Mathematical models for walking metabolic costs.

• Section S3. Adding a leg swing cost and obtaining model-based optimal speeds.

• Section S4. Covariances and error estimates for the metabolic rate fits.

• Section S5. Metabolic cost of walking at zero speed versus cost of resting.

(2) Experimental data. Text file containing all (de-identified) human subject data used in thisarticle.

(3) Video animation. Two video animations: one shows the simplest model of forward walking,namely inverted pendulum walking and the second shows our simple model of sideways walking.For sideways walking, the momentary rest phase when the legs are vertical is exaggerated in thesideways walking animation so as to make its presence more clear; in the model, this phase is ofinfinitesimal duration. The leg swing shown corresponds to a simple pendular motion, not includedin the simulated equations of motion.

(4) Computer programs. A text file containing MATLAB programs. These are used to simulatethe mathematical models for sideways walking and compute its cost. One sub-folder containscalculations of metabolic cost with fixed step length and no leg swing cost and another sub-foldercontains calculations with leg swing cost, without step length constraints.

⇤Author for correspondence: Manoj Srinivasan, [email protected], http://movement.osu.edu

1

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velocity just after push-off

Velocity change due topush-off impulse along trailing leg

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velocity just before heel-strike

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b) Push-off entirely before heel-strike

Figure S1: Impulsive step-to-step transition. a) Heel-strike entirely before push-o↵. b) Push-o↵entirely before heel-strike. The transition from an inverted pendulum motion about one leg to an invertedpendulum motion about the next leg is accomplished by two impulses in sequence: a heel-strike impulsefrom the leading length and a push-o↵ impulse from the trailing leg. These impulses re-direct the center ofmass velocity from downward (

�!OA) to upward (

�!OC). The panels on the right show a zoomed-in version of

the step-to-step transitions. The velocity changes due to heel-strike are shown in light red (�!AB and

�!EC),

velocity changes due to push-o↵ are shown in light blue (�!BC and

�!AE), the horizontal velocity between the

two impulses is shown in light green (�!OB and

�!OE), the direction of the two legs are shown as dashed lines.

S1 Comparisons of other activities to sideways walking costs

Forward walking and running. At low speeds, the sideways walking cost is much higher thanthe forward walking cost: in particular, the gross sideways cost (including resting cost, per distanceor per time) is about twice forward walking cost at 0.6 m/s. Also, we find that walking sidewaysat 1 m/s has the same gross metabolic rate as running forward at about 2.3 m/s (using [1]).

Carrying a load. Forward walking costs can also be increased by carrying a load. Up to carryingan extra load of about 75% body weight, gross metabolic rate has been shown to increase roughlyproportional to total mass at a given speed [2]. Extrapolating this cost increase, one might haveto carry about 100% body weight while walking forward to have the same gross metabolic cost assideways walking at 0.6 m/s.

2

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Small animals. Per unit mass and for a given absolute speed, small animals have a much highermetabolic rate than larger animals. The allometric scaling of net metabolic cost per distance perunit mass with the animals’ body mass M

animal

is roughly like M�0.3animal

[3]. Net sideways walkingmetabolic cost per distance is three to five times (say, four) higher than forward walking. So, ananimal that is roughly 4(1/0.3) ⇡ 100 times less massive than a human, that is, about a kilogram(in order of magnitude), might be expected to have the same cost per distance per unit mass. Notethat the M�0.3

animal

cost-dependence power law was constructed with mostly running data [3], so theabove estimate may change slightly when re-done with walking allometric data.

Robots. Finally, despite the high metabolic cost of sideways walking compared to normal humanwalking, many state-of-the-art legged walking robots are much worse than even sideways walking;for instance, the two legged Asimo robot is about ten times more expensive than normal humanwalking (e.g., as estimated by [4]).

S2 Mathematical models for walking metabolic costs.

Work-based metabolic cost. In this article, for simplicity, we only use a work-based metaboliccost. That is, if Wp was the total positive work and Wn was the total negative work over a singlestep, we model the metabolic cost over the step by b

1

Wp + b2

Wn. Here, b1

= 4 and b2

= 1 are the(approximate) reciprocals of muscle e�ciencies for positive and negative work respectively [5, 6].If T

step

is the duration of a single step, the metabolic rate is computed as (b1

Wp + b2

Wn) /Tstep

.

Stance cost. The metabolic cost of the step-to-step transition and the cost of starting andstopping at mid-stance together form the stance cost E

stance

. This is the metabolic cost due thework performed by the stance leg (the leg in contact with the ground) [7]; this cost is sometimesdubbed as being due to “center of mass work” and is similar to the so-called “external work” [8].In particular, this cost ignores the swinging the leg about the upper body.

For the sideways walking model in the main manuscript and for the forward inverted pendulumwalking models, the step-to-step transition is accomplished using an impulsive push-o↵ from thetrailing leg and an impulsive heel-strike from the leading leg. As shown in Figure S1, these twoimpulses change of the direction of the hip velocity from downward at the end of one invertedpendular phase to upward at the beginning of the next pendular phase. The work done by the twoimpulses depend on the order in which the impulses occur and more generally, on the amount ofoverlap they have. Work expressions for arbitrary overlap are derived in [5], with simplificationsfor the limit of small leg angles during walking. In this section, for completeness, we derive theformulas for the positive and negative work performed by the impulses, without the small angleapproximation, adapted from [9].

Heel-strike entirely before push-o↵. In Figure S1a,�!OA is the velocity just before heel-strike

at the end of the step.�!OC is the velocity at the beginning of the next step, after both heel-strike

and push-o↵ are complete. A heel-strike impulse along the leading leg produces a velocity change�!AB along the leading leg, resulting in a horizontal post-heel-strike velocity

�!OB. Then, the trailing

leg pushes o↵, resulting in a velocity change�!BC along the trailing leg, thereby changing the center

of mass velocity from�!OB to

�!OC.

By symmetry, the negative work done by the heel-strike is equal to the positive work done bythe push-o↵. Because the sign of the work is fixed for each impulse (entirely positive or entirely

3

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negative), the work can be calculated as the change in kinetic energy between�!OA or

�!OC and

�!OB.

|Work| =12m|�!OA|2 � 1

2m|�!OB|2 =

12m|�!OC|2 � 1

2m|�!OB|2. (1)

Here,�!OB =

�!OD � �!BD, where |�!OD| = |�!OA| cos ↵ and |�!BD| = |�!AD| tan↵ = |�!OA| sin ↵ · tan↵.

Therefore,

|�!OB| = |�!OA| (cos ↵� sin ↵ · tan↵) = |�!OA|cos 2↵

cos ↵.

Thus,

|Work| =12m|�!OA|2

✓1� cos2 2↵

cos2 ↵

◆, (2)

as noted in the main manuscript, where we use the notation v� = |�!OA|.

Push-o↵ entirely before heel-strike. In Figure S1b,�!OA and

�!OC are identical to those in

Figure S1a. A push-o↵ impulse along the trailing leg produces a velocity change�!AE to bring the

velocity to�!OE. Next, a heel-strike impulse along the leading leg produces a velocity change

�!EC,

bringing the velocity to�!OC.

Again, because each impulse performs work of a fixed sign (entirely positive or entirely negative),the work done can be computed as the kinetic energy di↵erence between

�!OA or

�!OC and

�!OE:

|Work| =12m|�!OE|2 � 1

2m|�!OA|2 =

12m

�����

�!OAcos ↵

�����

2

� 12m|�!OA|2 =

12m|�!OA|2 tan2 ↵. (3)

Model metabolic cost ratio (stance cost only)Sideways walking : Forward walking

Met

abo

lic c

ost

rat

io

0 0.2 0.4 0.6 0.8 10

2

4

6

8

10

12

(Push-off first) : (Push-off first)

(Push-off first) : (Foot-strike first)

(Foot-strike first) : (Push-off first)

(Foot-strike first) : (Foot-strike first)

1:1

Speed (m/s)

Figure S2: Metabolic cost ratios. Ratios of metabolic cost between sideways walking and forwardwalking models each with either foot-strike (heel-strike) first or push-o↵ first. Velocities range from 0 to 1m/s and step length is equal to 0.5 m. The ratios are the same at a given speed whether one uses metaboliccost per time or metabolic cost per distance. These metabolic cost estimates are based on the stance workalone; they do not have a leg swing cost or added resting cost.

Computing v� = |�!OA|. Computer programs (in MATLAB) that compute v� as a function offorward speed v and step length d

step

are part of the Supplementary Information. As noted in the

4

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Experimental Data versus Model predictions (with resting cost added, no leg swing cost)

00

1

1

2

3

4

5

6

7

8

9

Speed (m/s)

Po

siti

ve w

ork

rat

es p

er u

nit

mas

s (W

/kg

)

Experimental data

Model, push-off first

Model, foot-strike first

00

1

1

2

3

4

5

6

7

8

9

Speed (m/s)

Po

siti

ve w

ork

rat

es p

er u

nit

mas

s (W

/kg

)

Forward data (Ralston)

Model, push-off first

Model, foot-strike first

a) Sideways walking b) Forward walking

Resting metabolic rate erest Resting metabolic rate erest

Figure S3: Comparison of experiment and stance cost model. The experimental metabolic rateE = a0 + a2v2 is compared with the stance work-based metabolic rate predicted by the model with restingcost added: Estance + erest, for a) Sideways walking and b) Forward walking. The models had a constrainton step length that did not exist in the experiment and did not involve any cost for leg swing.

main manuscript, we compute the v� as that required to achieve the correct average forward speedover the inverted pendular phase (see also [9]), as follows.

For a given ✓(0+), starting at the vertical position ✓ = 0, we integrate the pendulum di↵erentialequations ✓ + (g/`) ✓ = 0, until ✓ becomes consistent with half-step length d

step

/2. i.e., the inte-gration is stopped when ✓ = sin�1(d

step

/2`). The time at the end of integration is t = Tstep

/2 andthe corresponding body speed just before step-to-step transition is v� = `✓(T

step

/2). We computecorresponding average speed is v

avg

= dstep

/Tstep

. We determine the ✓(0+) at initial vertical posi-tion so that the computed average forward speed is as desired: v

avg

= v, accomplished by solvinga root-find problem with MATLAB’s fsolve. See appended supplementary programs.

Note that, in our models, the speed v� just before the step to step transition is identical forall four gaits. The sideways walking gait has the same v� as the forward walking gaits becausethe stopping and starting at mid-stance for sideways walking is assumed to take infinitesimal time,while the rest of the inverted pendular motion is identical in all gaits considered.

Stopping and starting at mid-stance. In addition to the work of the step-to-step transition,the sideways walking gait has an additional cost due to coming to rest and accelerating back toappropriate speed, when the legs are in the vertical position. The positive and negative work bothequal m`2 ˙✓(0+)

2

/ 2, the kinetic energy just after the hip impulse brings the body to the necessaryspeed.

Stance cost comparisons between sideways and forward walking. To compare the costsof sideways and forward walking, we simply compare their stance costs, for given speed v and fixedstep length d

step

. We consider four di↵erent gait variations: two sideways walking gaits and twoforward walking gaits, one with foot-strike/heel-strike before push-o↵ and another with push-o↵before heel-strike. For these four gait variations, Figure 2b of the main manuscript shows these

5

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work-based metabolic rate estimates for a fixed step length dstep

= `/2 and ` = 1 m. The sameordering of the four costs is found at all other step lengths explored as well (0 < d

step

< 1). FigureS2 shows the ratio of sideways to forward walking stance metabolic rates, considering both impulsesequences for each gait.

We ignore the leg swing cost in this comparison for the following reason. In a single step offorward walking, only one of the two legs swings forward by the angle consistent with the steplength. In a single step of sideways walking, both legs take turns swinging forward, but only forhalf the step length each. Thus, at a given speed and step length, the leg swing cost in sidewaysand forward walking are likely to be comparable, with sideways walking leg swing cost being larger(by a factor of two according to the simple kinetic energy based leg swing cost model describedbelow). Thus, ignoring the leg swing cost is likely to underestimate the ratio of sideways andforward metabolic costs.

Stance cost comparison with experimental metabolic data. Figure S3 compares the ex-perimental metabolic rate, with the model-based stance metabolic rate (again, for d

step

= `/2 and` = 1 m). We add e

rest

to the model, as the model does not have a resting metabolic rate. Wesee that the explanatory power of the stance cost of this simple model is about the same for bothsideways walking and forward walking.

S3 Adding a leg swing cost and obtaining model-based optimal

speeds

Adding further terms to the stance work-based metabolic cost model allows us to not constrainthe step length and also predict meaningful (non-zero) optimal speeds. The simplest modificationinvolves the addition of two terms (1) a leg swing cost and (2) a constant o↵set cost (a

0

or erest

).Note that for the calculations in this section, we used foot-strike entirely before push-o↵, as thischoice gives the higher costs among the two impulse sequences.

Leg swing cost. First, to be able to predict step lengths, our biped model needs a leg swingcost, as described in [9, 10]. Even though [10, 11] have argued that a force-based leg swing costfits data slightly better than a work-based leg swing cost, for simplicity and consistency, we use awork-based leg swing cost. In particular, we use the simplest possible additive leg swing cost asfollows. On average, the foot has to move with the body at speed v, but it comes to rest twiceevery step. That is, positive work is done on the leg/foot to accelerate it, twice every step, sothat the foot has the same average speed as the body. We approximate this work as 0.5m

foot

v2,as in [9, 12], where m

foot

= 0.0435m, so as to match the moment of inertia of the leg [13] with amass at the foot. Now, instead of a root find procedure, we use numerical optimization to obtainthe midstance ✓(0+) and the step time T

step

so that the biped travels at a given speed v and hasthe least metabolic rate, E

stance

+ Eswing

, defined as the cost over a step divided by Tstep

. Thismodel-predicted metabolic rate goes to zero as v ! 0. Therefore, we add e

rest

to this cost whencomparing with experimental data in Figure S4 i.e., we plot e

rest

+ Estance

+ Eswing

. Because theexperimental metabolic rate has a zero-speed cost a

0

> erest

, we also show comparisons in FigureS4 with a

0

+ Estance

+ Eswing

.

Optimal speeds from model. As can be gleaned from the metabolic cost per unit distancecurves of Figure S4b, the optimal speeds obtained from the model with leg swing cost are 0.5319m/s when e

rest

is added and 0.6420 m/s when a0

is added.

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0

10

20

30

40

50

60

Me

tab

olic

co

st p

er

dis

tan

ce (

J/kg

/m)

0 0.2 0.4 0.6 0.8 1

Speed (m/s)

0 0.2 0.4 0.6 0.8 10

2

4

6

8

10

Speed (m/s)

Me

tab

olic

co

st r

ate

(W

/kg

)

Experimental data (fit, a0 + a2 v2)

Biped model + erest

Biped model + a0

a) b)

Figure S4: Biped model with leg swing cost. a) Metabolic rate from experiment and biped model withan additional leg swing cost. We show two versions of model predictions, one with resting cost erest addedand another with zero-speed cost a0 added. The latter is closer to experimental data. b) Metabolic cost perunit distance for experiment and biped model, again using two di↵erent o↵sets erest and a0. These curvesare obtained by dividing the corresponding curves in panel-a by speed v. This panel is identical to Figure2c of the main manuscript. All model predictions assumed push-o↵ before heel-strike. The step length wasnot constrained; at each speed, the step length was selected so as to minimize Estance + Eswing

Metabolic cost is underestimated by the model. As seen in Figure S4, the metabolic costis underestimated by the model. Perhaps this underestimation is partly explained by force-relatedcost terms e.g., [11, 14, 15], partly due to the fact that the step length cannot go to zero forreal human walking because of finite hip width. Also, the model is vastly simpler than than thehuman body, with fewer degrees of freedom. Finally, the model assumes ideal impulsive push-o↵and foot-strike of infinitesimal duration; it is shown in [6, 16] that spreading these impulses overnon-infinitesimal time durations, with smooth and finite ground reaction forces, will increase thecost substantially; after all, the ideal impulsive model was shown to be energy optimal in [17], asalso elaborated at the end of this section.

Of course, even the fraction of the metabolic cost that we have explained using mechanical workcould be partly due to force-related terms if muscle positive and negative work could be replacedby tendon positive and negative work.

Predicting the metabolic cost as a function of speed without actually fitting the model to dataremains even an open problem for forward walking. Earlier detailed attempts to explain metaboliccost trends (e.g., [18]) have fallen short of quantitative predictions, or have required some fittingof model to data (e.g., [10] for the step length dependence). For instance, the articles that explainthe metabolic cost as a function of speed using a force-based metabolic cost, while quite successful,have all only found correlations [11, 14, 19] or used fitting to data, rather than explaining the actualmagnitudes through a priori models that start from a basic understanding of how muscles work.In contrast, our metabolic cost comparisons involve no fitting.

In future work, we hope to improve upon this work to predict and explain the observed metaboliccost variations and be consistent with as much extant data. With a force-plate measurement ofground reaction forces for each foot, we could estimate the work performed by the legs (using theso-called “external work” calculations [20, 21]) and compare with those predicted by our models.We could also use such force measurements to determine the sequence or overlap of push-o↵ andfoot-strike. Measurement of step length and step periods would also let us compare them withmodel predictions, as well as to use them to constrain the models better.

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Why did we choose impulsive walking strategies? Our sideways walking model consistsof passive inverted pendulum motions interrupted by discrete impulses, for instance, foot-strike,push-o↵, and hip torque impulses, which perform finite work in infinitesimal time. Similarly, theforward walking model consists of passive pendulum motions interrupted by heel-strike and push-o↵impulses. Why did we choose these specific walking models, as opposed to other simpler modelchoices such as, say, passive dynamic walking models [22]?

First, given a point-mass biped model with extensible legs, capable of an infinite variety ofwalking motions, it has been shown (in [6, 9, 17]) that the optimal forward walking gait minimizinga work-based metabolic cost is the inverted pendulum walking motion with push-o↵ and heel-strikeimpulses. Similarly, swinging a leg (pendulum) or moving a mass from one position to another canbe accomplished with least work by an impulsive strategy for the torque or force, as demonstratedin [9] and the appendix of [6]. Thus, in this article, we have used these impulsive sideways andforward inverted pendulum walking gaits, because such impulsive gaits are known to minimizework-based metabolic cost models for related more general biped models.

Note that the sideways walking described here cannot be achieved without hip torques, withjust push-o↵ and heel-strike. In our model, the hip-torques arrest the forward speed when thelegs are together and vertical, and restart the motion again. When the legs are together, thepush-o↵-heel-strike along the legs have no ability to kill the forward speed, because the legs areperpendicular to the forward body speed.

Another class of simple walking models is the so-called passive dynamic walking models(e.g., [22]), in which a completely passive biped (no muscles or motors) walks downhill underthe power of gravity. The main di↵erence between our models and these slope-walking passivedynamic walking models is that passive dynamic walking replaces the push-o↵ or other positivework impulses by gravity and the leg swing is entirely passive. This replacement also means thatpassive dynamic walking is limited to walking on shallow slopes; it is physically infeasible to modeluphill walking, for instance, by such passive walking. Similarly, for biped models with point-massand point-feet (as here), we do not find any passive walking motions similar to sideways walking.Sideways walking involves coming to rest with both feet together every mid-stance; starting fromsuch a rest state on the slope leads to the walker falling down or not moving, without additionalforcing (like hip torques).

S4 Covariances and error estimates for the metabolic rate fits

Fits to pooled data. For metabolic rate data pooled over the subject population, we obtaineda

0

= 2.742 W/kg and a2

= 7.313 W/(m s�1)2/kg. The error covariances between the coe�cientswere obtained via a bootstrap re-sampling procedure (see [23]).

This bootstrap re-sampling procedure involves resampling from the 80 data points of (v, E)across the 10 subjects, thereby creating new 80-data-point data sets (called bootstrap samples),and re-computing the regression coe�cients for each such bootstrap sample. The error covariancesestimated from this distribution of regression coe�cients were �2

00

= 0.015, �2

22

= �0.033 and �2

02

=0.13 in appropriate units. The standard deviations of the respective coe�cients may be obtainedby taking the square root of the variances �2

ii, respectively �00

= 0.123 W/kg and �22

= 0.36W/(m s�1)2/kg.

A distribution of optimal speeds vopt

was also determined from the boostrap distribution ofregression coe�cients, giving a standard deviation of 0.027 m/s and a 95% confidence interval of0.495-0.754 m/s, serving as error estimates for the computed v

opt

.

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Fits to individual data. By fitting the equation to each individual’s metabolic data and thenaveraging the obtained coe�cients, we get roughly the same average coe�cients: a

0

= 2.746 W/kgand a

2

= 7.306 W/(m s�1)2/kg, with covariances between the di↵erent subjects’ coe�cients being�2

00

= 0.38, �2

22

= 0.56 and �2

02

= 0.252 in appropriate units.

Fits with a linear term. We obtained roughly the same optimal speeds when we used a moregeneral regression equation, now including a linear term (although not conventional in the literature[24, 25]): E = b

0

+b1

v+b2

v2. The best-fit coe�cients were b0

= 2.4622 W/k, 1.1791 W/(m s�1)/kg,and b

2

= 6.2715 W/(m s�1)2/kg, and the optimal speed vopt

=p

b0

/b2

= 0.6266 m/s, compared topa

0

/a2

= 0.6124 m/s. See also section S5.

S5 Metabolic cost of walking at zero speed versus cost of resting

We note that the metabolic rate of sideways walking at zero speed, namely a0

= 2.742 W/kg, isstrictly greater than the resting (sitting) metabolic rate e

rest

= 1.542 W/kg; in fact, this is almostan 80% increase over sitting metabolic rate, as a percentage of metabolic rate. Is this substantialdi↵erence a real phenomenon, or an artifact of data processing or assumptions?

First, note that the metabolic cost of standing rest is only about 13% on average higher asopposed to sitting rest [26]. Thus, that walking very slowly requires standing cannot explain thecost increase.

Second, as noted in the main manuscript, a similar but smaller di↵erence (about 30-40% over)is observed in regular forward walking, as already established in early work on walking [24] andrepeated in subsequent studies [25]. Because a

0

is obtained by extrapolating the equation obtainedby fitting to metabolic measurements at speeds substantially di↵erent from zero, one might suspectthat the a

0

� erest

is an extrapolation artifact. However, Ralston already addressed this suspicionby explicitly performing experiments of subjects walking very close to zero speed (“as slowly aspossible compatible to normal balance”) and observing that there was about a 33% di↵erence overstanding cost, and the cost he obtained for very slow walking was indeed close to his regressed a

0

.Thus, very slow walking seems qualitatively di↵erent from standing still. Perhaps the increased

cost is due to stability issues or due to the cost of switching weight between the feet. The reasons forthis di↵erence have not been established in the literature. Independent of the reason, this di↵erenceseems a real phenomenon, as opposed to being a data processing artifact. This di↵erence has realconsequences to behavioral predictions based on metabolic energy optimality (see also [1, 27] forsimilar discussions).

Note that while we get a lower zero-speed cost b0

= 2.46 W/kg when using a di↵erent regressionmodel, now with an additional linear term, this cost is still significantly above e

rest

. In any case, asnoted above, Ralston [24] showed that a

0

approximates the zero-speed cost well, at least in forwardwalking.

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11