LETTER. Reducing the energy cost of human walking using an unpowered exoskeleton

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1 doi:1.138/nture14288 Reducing the energy cost of humn wlking using n unpowered exoskeleton Steven H. Collins 1 *, M. Bruce Wiggin 2 * & Gregory S. Swicki 2 * With efficiencies derived from evolution, growth nd lerning, humns re very well-tuned for locomotion 1. Metbolic energy used during wlking cn be prtly replced by power input from n exoskeleton 2, but is it possible to reduce metbolic rte without providing n dditionl energy source? This would require n improvement in the efficiency of the humn mchine system s whole, nd would be remrkble given the pprent optimlity of humn git. Here we show tht the metbolic rte of humn wlking cn be reduced by n unpowered nkle exoskeleton. We built lightweight elstic device tht cts in prllel with the user s clf muscles, off-loding muscle force nd thereby reducing the metbolic energy consumed in contrctions. The device uses clutch to hold spring s it is stretched nd relxed by nkle movements when the foot is on the ground, helping to fulfil one function of the clf muscles nd Achilles tendon. Unlike muscles, however, the clutch sustins force pssively. The exoskeleton consumes no chemicl or electricl energy nd delivers no net positive, yet reduces the metbolic cost of wlking by % for helthy humn users under nturl conditions, comprble to svings with powered devices. Improving upon wlking economy in this wy is nlogous to ltering the structure of the body such tht it is more energy-effective t wlking. While strong nturl pressures hve lredy shped humn locomotion, improvements in efficiency re still possible. Much remins to be lerned bout this seemingly simple behviour. Humns re skilled wlkers. Over genertions, our bodies hve evolved musculr 1, skeletl 3 nd neurl 4 systems well-suited to locomotion. We lern nd embed wlking coordintion strtegies over our lifetimes 5 nd dpt to new locomotor environments in minutes or seconds 6.We tke bout 1, steps per dy 7, or hundreds of millions of steps in lifetime, exceeding the pproximtely 1, h of prctice thought to be needed to ttin expertise 8 by dulthood. We nturlly keep energy expenditure low during wlking, choosing, for exmple, step length 9 nd even rm motions 1 tht minimize energy cost. Nerly ny chnge to the humn musculoskeletl system or its pttern of coordintion increses metbolic rte. Despite this skill nd efficiency, getting bout is still expensive. People expend more energy during wlking thn ny other ctivity of dily life 11, nd ftigue cn limit mobility. Herein lies the chllenge: reducing the effort of norml wlking could grner substntil benefits, but humns re lredy so energy-effective tht mking improvements is extremely difficult. Since t lest the 189s 12, engineers hve designed mchines intended to mke wlking esier A survey of these designs cn be found in the Supplementry Discussion. It is only recently tht ny ttempt t reducing the energy cost of wlking with n externl device hs met with success. The first mchine to do so used off-bord pneumtic pumps nd vlves to replce humn joint with exoskeleton 2, overcoming the surprisingly tricky chllenge of coordinting ssistnce with the humn neuromusculr system. More recently still, powered nd untethered device using similr control strtegies succeeded in reducing energy cost 16, overcoming the dditionl chllenge of utonomous pckging. Reducing the energy cost of wlking with n unpowered device requires different pproch. Insted of dding robotic energy source to replce metbolic sources, one must, in sense, chnge the humn body such tht it is more efficient t locomotion (Extended Dt Fig. 1. For the tsk of crrying hevy lods while wlking, such improvements hve been demonstrted using spring-mounted bckpck 17 nd by trining people to blnce the weight on their hed in just the right wy 18. But is there room for similr improvement in the lredy expert tsk of norml wlking? The possibility of unpowered ssistnce is mde more likely by the fct tht level wlking t stedy speed requires no power input in theory, nd therefore ll energy used in this ctivity is, in sense, wsted. Simultion models with spring-loded legs illustrte this ide 19 ; their springs store nd return energy during ech step, but no is done by ctutors, cpitlizing on the fct tht the kinetic nd potentil energy Spring Tendon c Clutch Muscle Engge pin Bering Pulley Disengge pin Joint centre Tension spring (inside Rtchet Rope Pwl Detent b Figure 1 Unpowered exoskeleton design., The exoskeleton comprises rigid sections ttched to the humn shnk nd foot nd hinged t the nkle. A pssive clutch mechnism nd series spring ct in prllel with the clf muscles nd Achilles tendon. b, Prticipnt wlking with the device. Lod cells mesured spring force. c, The pssive clutch mechnism hs no electronics, but insted uses nd pwl tht ly engge the spring when the foot is on the ground nd disengge it when the foot is in the ir. 1 Deprtment of Mechnicl Engineering, Crnegie Mellon University, 5 Forbes Avenue, Pittsburgh, Pennsylvni 15213, USA. 2 Joint Deprtment of Biomedicl Engineering, North Crolin Stte University nd the University of North Crolin t Chpel Hill, 911 Ovl Drive, Rleigh, North Crolin 27695, USA. *All uthors contributed eqully to this. MONTH 215 VOL NATURE 1

2 RESEARCH LETTER of the body remin constnt on verge. Humns expend metbolic energy during wlking in prt to restore energy tht hs been dissipted, in pssive motions of soft tissues 2 for exmple, but the gretest portion of wste occurs in muscles. Muscles consume metbolic energy to perform positive, s required by conservtion of energy, but they lso use metbolic energy to produce force isometriclly nd to perform negtive 21. This plces metbolic cost on body weight support 22 nd on holding tendons s they stretch nd recoil 23. By contrst, clutches require no energy to produce force. We designed lightweight exoskeleton tht provides some of the functions of the clf muscles nd tendons during wlking, but uses more efficient structures for those tsks. It hs spring in prllel with the Achilles tendon (Fig. 1 connected to the leg using lightweight composite frme with lever bout the nkle joint (Fig. 1b nd Extended Dt Fig. 2. A clutch in prllel with the clf muscles engges the spring when the foot is on the ground nd disengges it to llow free motion when the foot is in the ir (Fig. 1c nd Supplementry Video 1. This design ws inspired by ultrsound imging studies suggesting clutchlike behviour of muscle fscicles to hold the spring-like Achilles tendon 24, the recoil of which leds to the lrgest burst of positive power t ny joint during wlking. The exoskeleton clutch, described in detil in the Supplementry Methods nd Supplementry Video 2, hs no motor, bttery or computer control, nd weighs.57 kg. The entire exoskeleton hs mss of between.48 nd.53 kg per leg, depending on prticipnt size (Extended Dt Tbles 1 nd 2. On the bsis of simultion studies of wlking with elstic nkles 19,25,weexpected n intermedite stiffness to minimize energy cost nd performed tests with rnge of springs. We conducted experiments with helthy prticipnts (N 5 9 wering n exoskeleton on ech leg while wlking t norml speed (1.25 m s 21 on tredmill. The exoskeleton produced pttern of torque similr to tht produced by the biologicl nkle, but with lower mgnitude (Fig. 2. This reduced the nkle moment produced by clf muscles (Fig. 2b nd reduced clf muscle ctivtion, prticulrly in the soleus (Fig. 2c. Joint ngles chnged little cross conditions (Fig. 2d, confirming tht the exoskeleton did not interfere with other norml nkle functions, such s toe clernce during leg swing (6 1% stride. The exoskeleton reduced humn metbolic energy consumption when using moderte-stiffness springs (Fig. 3. Wering lightweight exoskeleton on ech nkle without springs did not mesurbly increse energy cost compred with norml wlking. With incresing spring stiffness, metbolic rte first decresed then incresed, supporting the hypothesis tht n intermedite stiffness would be optiml. The 18 N m rd 21 spring reduced the metbolic cost of wlking to W kg 21 (men 6 stndrd error, down from W kg 21 for norml wlking, reduction of % (pired t-test: P Metbolic energy used for wlking, or net metbolic rte, is clculted s totl metbolic rte minus the rte for quiet stnding, which ws Exoskeleton torque (N m kg scle No exoskeleton No spring (k = k = 13 N m rd 1 k = 18 N m rd 1 k = 24 N m rd 1 k = 31 N m rd 1 k = 4 N m rd 1 Averge exoskeleton torque (N m kg 1.1 *P <.1 Biologicl nkle moment (N m kg b Torque Averge biologicl moment (N m kg *P <.1 Soleus ctivity Ankle ngle (rd c.4 d Angle Rtchet disengges Rtcheting Spring stretching Spring recoil Free rottion Rtchet engges Averge soleus ctivity *P =.7 NE Exoskeleton spring stiffness (N m rd Time (% stride period Figure 2 Mechnics nd muscle ctivity., Exoskeleton torque (normlized to body mss in time (normlized to stride period for ech spring, verged cross prticipnts. Brs t right re the verges of these trjectories in time; N 5 9; error brs, s.e.m.; P vlues indicte the results of nlysis of vrince (ANOVA tests for n effect of spring stiffness; NE, no exoskeleton. Exoskeleton torque incresed with spring stiffness (except with the stiffest spring, which tended to be engged lter in stnce. b, Time course of the biologicl contributions to nkle moment, which decresed with incresing 9 1 spring stiffness. c, Time course of electricl ctivity in the soleus muscle, n nkle plntrflexor, which decresed with incresing spring stiffness. d, Time course of nkle joint ngle, which triggered pssive clutch enggement nd disenggement. The ws engged t heel strike, took up slck through foot flt, held the spring s it stretched nd recoiled through mid- nd lte stnce, nd disengged to llow toe clernce during leg swing. The verge stride period ws s (men 6 s.d.. 2 NATURE VOL MONTH 215

3 RESEARCH Net metbolic rte (W kg NE *P =.23, pired t-test 7.2% reduction Exoskeleton spring stiffness (N m rd W kg 21 in this study. The observed reduction is similr to improvements with high-powered devices 2,16 nd equivlent to the effect of tking off 4 kg bckpck for n verge person 26. It is difficult to ttribute chnges in whole-body metbolic rte to prticulr chnge in muscle mechnics 27, but with this device there is n ssocition with reduced muscle forces t the ssisted nkle joints. Muscles consume energy whenever ctive, even when producing force without performing. Simply reducing muscle force cn therefore sve metbolic energy. For ll exoskeleton springs, we mesured reductions in the biologicl component of nkle moment nd the ctivity of mjor plntrflexor muscles, both indictive of reduced force. Reductions occurred primrily during erly nd mid-stnce ( 4% stride, Fig. 2b, c when muscle fscicles re nerly isometric nd therefore perform little 24. Simultion models estimte tht plntrflexor muscle energy use primrily occurs during this period nd ccounts for bout 27% of the metbolic energy used for wlking 27. With the 18 N m rd 21 spring, the biologicl component of verge nkle moment ws reduced by 14% nd mid-stnce soleus electricl ctivity ws reduced by 22% compred with norml wlking. Extrpolting from these vlues, one might expect bout 4 6% reduction in overll metbolic rte, comprble to the observed 7% reduction. Biologicl contributions to nkle joint were lso prtly replced by the exoskeleton, but it is unlikely tht these chnges were responsible for reductions in metbolic rte. The connections between joint, musculotendon, muscle fscicle nd metbolic rte re complex. Much of the t the nkle joint during wlking is the result of elstic stretch nd recoil of the Achilles tendon 24, which does not directly consume metbolic energy. Becuse of tendon complince, using n exoskeleton to reduce cyclic musculotendon cn ctully preserve or increse the performed by muscle fscicles 28 reducing tendon force reduces its stretch, which cn led to incresed excursion of the muscle itself nd more muscle. Even if reduced joint hd been the result of reduced muscle fscicle, under these circumstnces such chnge would probbly not hve reduced metbolic cost. It hs recently been shown tht for contrction cycles similr to those of the clf muscles during norml wlking, where muscle fscicles undergo stretch shorten cycles with nerly zero net, mking equl nd opposite chnges to both negtive 4% 2% % 2% 4% 6% 8% 1% 12% Figure 3 Humn metbolic rte. Spring stiffness ffected metbolic rte (N 5 9; ANOVA with second-order model; P stiffness 5.16, P stiffness Net metbolic rte, with the vlue for quiet stnding subtrcted out, ws % (men 6 s.e.m. lower with the 18 N m rd 21 spring (ornge br thn during norml wlking (drk grey br; pired two-sided t-test with correction for multiple comprisons; P The dshed line is qudrtic best fit to men dt from exoskeleton conditions (R , P Wering the exoskeleton with the spring removed (light grey br, k 5 did not increse energy cost compred with norml wlking (pired t-test; P 5.9. Error brs, s.e.m., dominted by inter-prticipnt vribility. Chnge in net metbolic rte (% NE nd positive hs no effect on metbolic energy use per unit force 29. Our understnding of the reltionship between muscle ctivity nd metbolic rte remins imperfect, but reduced muscle does not seem to provide good explntion for reduced metbolic cost in this study. Metbolic rte incresed bck to norml levels when using highstiffness exoskeleton springs, pprently the result of severl fctors. Humns tend to select coordintion ptterns with similr net nkle moments cross rnge of exoskeleton torques 2,3, trend lso observed here. With stiff springs, tibilis nterior ctivity countercting exoskeleton torque in erly nd mid-stnce ppered to increse, possibly reducing chnges in totl joint moment. Knee muscle ctivity to prevent hyperextension during mid- nd lte stnce my lso hve contributed to increses in metbolic cost. Unexpectedly, some of the increse in metbolic rte ppers to be ssocited with incresed plntrflexor ctivity t the end of stnce. Furthermore, despite being more ctive during this period, plntrflexor muscles produced lower joint moments. These reduced moments probbly reflect incresed contrction velocity, becuse muscle force drops rpidly s the rte of shortening increses. These two observtions suggest tht exoskeleton support during midstnce led to inefficient, rpid shortening of plntrflexor muscles during the usul burst of positive t the end of the step. Also unexpectedly, it does not pper tht the increse in metbolic rte with high-stiffness springs is well explined by simple dynmic models of wlking, which predict chnges in centre-of-mss tht were not observed here 19,25. These nd other interprettions re presented in expnded form in the Supplementry Discussion nd cn be explored using joint mechnics, muscle ctivity nd centre-of-mss mechnics dt presented in Extended Dt Figs 3 8. The complexity of the neuromusculr system cn impede useful ppliction of simple ides from mechnics nd robotics to humn locomotion. For exmple, it is tempting to equte joint or centre-of-mss with metbolic energy use. However, the benefits derived from reduced muscle ctivity with this unpowered exoskeleton would not hve been discovered using joint-level power estimtes s guide, since these drw ttention towrds terminl stnce nd wy from erly nd mid-stnce when joint power is negtive nd of low mgnitude. The incresed metbolic rte t higher exoskeleton spring stiffness found here lso cnnot be explined using power, becuse humn contributions decresed or remined suppressed with incresing stiffness. The complex neuromusculr fctors underlying these chnges mke effective integrtion of ssistive devices very chllenging nd my explin why the threshold of reducing the metbolic rte of norml wlking, with 2,16 or without dditionl power input, hs tken more thn century to cross. Much remins to be lerned bout humn coordintion, even in this seemingly uncomplicted ctivity. We hve demonstrted tht net energy input is not fundmentl requirement for reducing the metbolic cost of humn wlking. Reducing clf muscle forces while lso fulfilling norml nkle functions nd minimizing penlties ssocited with dded mss or restricted motions cn provide benefit. Pssive clutch-like structures re fesible in nture, mking the use of this type of device nlogous to chnge in ntomy tht improves wlking economy. Similr morphologicl chnges might ugment other lower-limb musculture or locomotion in other nimls. While evolution, growth nd lerning hve driven efficiency, improvements re yet possible. Online Content Methods, long with ny dditionl Extended Dt disply items ndsource Dt, re vilble in the online version of the pper; references unique to these sections pper only in the online pper. Received 11 December 214; ccepted 6 Februry 215. Published online 1 April Alexnder, R. M. Principles of Animl Locomotion Chs 1 nd 7 (Princeton Univ. Press, Mlcolm, P., Derve, W., Glle, S. & De Clercq, D. A simple exoskeleton tht ssists plntrflexion cn reduce the metbolic cost of humn wlking. PLoS ONE 8, e56137 (213. 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4 RESEARCH LETTER 3. Lovejoy, C. O. The nturl history of humn git nd posture: prt 1. Spine nd pelvis. Git Posture 21, ( Dietz, V. Spinl cord pttern genertors for locomotion. Clin. Neurophysiol. 114, ( Forssberg, H. Ontogeny of humn locomotor control I. Infnt stepping, supported locomotion nd trnsition to independent locomotion. Exp. Brin Res. 57, ( Dvidson, P. R. & Wolpert, D. M. Widespred ccess to predictive models in the motor system: short review. J. Neurl Eng. 2, S313 S319 ( Tudor-Locke, C., Johnson, W. D. & Ktzmrzyk, P. T. Accelerometer-determined steps per dy in US dults. Med. Sci. Sports Exerc. 41, ( Ericsson, K. A. & Chrness, N. Expert performnce: its structure nd cquisition. Am. Psychol. 49, ( Zrrugh, M. Y., Todd, F. N. & Rlston, H. J. Optimiztion of energy expenditure during level wlking. Eur. J. Appl. Physiol. Occup. Physiol. 33, ( Collins, S. H., Admczyk, P. G. & Kuo, A. D. Dynmic rm swinging in humn wlking. Proc. R. Soc. B. 276, ( Westerterp, K. R. Physicl ctivity nd physicl ctivity induced energy expenditurein humns: mesurement, determinnts, nd effects. Front. Physiol. 4, 9 ( Ygn, N. Apprtus for fcilitting wlking, running nd jumping. US ptent 42,179 ( Grbowski, A. M. & Herr, H. M. Leg exoskeleton reduces the metbolic cost of humn hopping. J. Appl. Physiol. 17, ( vn Dijk, W., vn der Kooij, H. & Hekmn, E. A pssive exoskeleton with rtificil tendons: design nd experimentl evlution. Proc. IEEE Int. Conf. Rehbil. Rob. ( Zoss, A. & Kzerooni, H. Design of n electriclly ctuted lower extremity exoskeleton. Adv. Robot. 2, ( Mooney, L. M., Rouse, E. J. & Herr, H. M. Autonomous exoskeleton reduces metbolic cost of humn wlking. J. Neuroeng. Rehbil. 11, 1 6 ( Rome, L. C., Flynn, L. & Yoo, T. D. Biomechnics: rubber bnds reduce the cost of crrying lods. Nture 444, ( Heglund, N. C., Willems, P. A., Pent, M. & Cvgn, G. A. Energy-sving git mechnics with hed-supported lods. Nture 375, ( Zelik, K. E., Hung, T. W. P., Admczyk, P. G. & Kuo, A. D. The role of series nkle elsticity in bipedl wlking. J. Theor. Biol. 346, ( Zelik, K. E. & Kuo, A. D. Humn wlking isn t ll hrd : evidence of soft tissue contributions to energy dissiption nd return. J. Exp. Biol. 213, ( Ryschon, T. W., Fowler, M. D., Wysong, R. E., Anthony, A. & Blbn, R. S. Efficiency of humn skeletl muscle in vivo: comprison of isometric, concentric, nd eccentric muscle ction. J. Appl. Physiol. 83, ( Grbowski, A., Frley, C. T. & Krm, R. Independent metbolic costs of supporting body weight nd ccelerting body mss during wlking. J. Appl. Physiol. 98, ( Roberts, T. J. The integrted function of muscles nd tendons during locomotion. Comp. Biochem. Physiol. A 133, ( Ishikw, M., Komi, P. V., Grey, M. J., Lepol, V. & Bruggemnn, G. P. Muscle-tendon interction nd elstic energy usge in humn wlking. J. Appl. Physiol. 99, ( Bregmn, D. J. et l. The effect of nkle foot orthosis stiffness on the energy cost of wlking: simultion study. Clin. Biomech. 26, ( Browning, R. C., Modic, J. R., Krm, R. & Goswmi, A. The effects of dding mss to the legs on the energetics nd biomechnics of wlking. Med. Sci. Sports Exerc. 39, ( Umberger, B. R. & Rubenson, J. Understnding muscle energetics in locomotion: new modeling nd experimentl pproches. Exerc. Sport Sci. Rev. 39, ( Frris, D. J., Robertson, B. D. & Swicki, G. S. Elstic nkle exoskeletons reduce soleus muscle force but not in humn hopping. J. Appl. Physiol. 115, ( Holt, N. C., Roberts, T. J. & Askew, G. N. The energetic benefits of tendon springs in running: is the reduction of muscle importnt? J. Exp. Biol. 217, ( Ko, P. C., Lewis, C. L. & Ferris, D. P. Invrint nkle moment ptterns when wlking with nd without robotic nkle exoskeleton. J. Biomech. 43, (21. Supplementry Informtion is vilble in the online version of the pper. Acknowledgements We thnk A. Westbrook for dt collection, K. Tkhshi nd R. Nuckols for stiffness chrcteriztions, B. Reich for discussions on sttisticl nlysis, R. Jcksonfor dt collection nd mnuscriptediting, nd J. Cputo, P. Collins, S. Diller, N. Donhue, A. Kuo, I. Lu, L. Lu, C. Mjidi, J. Mlen, T. Roberts, A. Robinson, A. Ruin, P. Tggrt, K. Witte, M. Wu nd others for editoril suggestions. The photogrph in Fig. 1b is by S. Thrift. Funding for this reserch ws provided by grnts to G.S.S. from the North Crolin Stte Fculty Reserch nd Professionl Development Fund; the North Crolin Stte Chncellors Innovtion Fund; grnt number from the United Sttes - Isrel Bintionl Science Foundtion; nd wrd number R1NR14756 from the Ntionl Institute of Nursing Reserch of the Ntionl Institutes of Helth. This mteril is bsed upon supported by the Ntionl Science Foundtion under grnt number IIS to S.H.C. The content is solely the responsibility of the uthors nd does not necessrily represent the officil views of the Ntionl Institutes of Helth or other funding gencies listed. Author Contributions G.S.S. nd S.H.C. contributed eqully to study design nd direction; M.B.W., S.H.C. nd G.S.S. designed the device; M.B.W. fbricted the device; M.B.W. ndg.s.s. conductedhumn locomotionexperiments; M.B.W., S.H.C. nd G.S.S. nlysed dt; S.H.C., M.B.W. nd G.S.S. drfted the mnuscript; S.H.C. nd G.S.S. edited the mnuscript. All uthors pproved the finl mnuscript. Author Informtion Source dt re vilble t NturePssiveExoDt/. Reprints nd permissions informtion is vilble t The uthors declre competing finncil interests: detils re vilble in the online version of the pper. Reders re welcome to comment on the online version of the pper. Correspondence nd requests for mterils should be ddressed to S.H.C. (stevecollins@cmu.edu or G.S.S. (greg_swicki@ncsu.edu. 4 NATURE VOL MONTH 215

5 RESEARCH METHODS Prticipnts. Nine helthy dults (N 5 9, 2 femle, 7 mle; ge yers; mss kg; height m; men 6 s.d. prticipted in the study. One dditionl prticipnt dropped out before completing the protocol, in prt owing to hrdwre mlfunctions during trining sessions. Smple size ws chosen on the bsis of dt from previous studies; no sttisticl methods were used to predetermine smple size. All prticipnts provided written informed consent before prticiption nd seprtely provided written consent to publish de-identified photogrphs (s pplicble. The study protocol ws pproved nd overseen by the Institutionl Review Bord of the University of North Crolin t Chpel Hill. Exoskeleton hrdwre. Custom frmes were fbricted for ech prticipnt using modified orthotics methods. A flexible cst ws used to crete positive plster mould of the foot, nkle nd shnk, upon which thin, selectively reinforced crbon fibre frme ws formed. Shnk nd foot segments were removed from the mould nd connected using n luminium hinge joint with plin bering (Extended Dt Fig. 2. The custom clutch 31,32 (Fig. 1c nd Supplementry Methods ws then integrted with the frme. Prt drwings nd CAD files re provided s Supplementry Dt 1 nd 2, detiled ccounting of component mss nd comprisons with other systems re provided in Extended Dt Tbles 1 nd 2, nd demonstrtion of clutch function cn be found in Supplementry Video 2. We used five sets of steel coil extension springs with stiffnesses of 5.6, 7.9, 1.5, 13.3 nd 17.2 kn m 21 nd msses of.59,.61,.68,.92 nd.98 kg, respectively. Springstiffnesses were determined in experiments where springs werestretched to severl displcements using fixture nd forces were mesured using lod cell. Springs were ttched to lever rm on the foot frme with n verge rdius of.152 m, resulting in verge exoskeleton rottionl stiffnesses of 13, 18, 24, 31 nd 4 N m rd 21. This spns the rnge of reported nkle joint qusi-stiffnesses for wlking 33. To mesure force, single-xis lod cell (LC , Omeg Engineering ws plced in series with the spring. Exoskeleton joint torque ws clculted s the product of spring force nd the lever rm, ssuming constnt leverge. The effective stiffness experienced by prticipnts ws lower thn tht indicted by the springs themselves. In follow-up experiment with single prticipnt, qusi-sttic loding of the exoskeleton, nd dditionl mrkers on the exoskeleton frme, complince in the frme nd rope led to bout n 18% decrese in effective stiffness, while complince t the humn exoskeleton interfce led to n dditionl decrese of bout 15%. The effective stiffness of the exoskeleton, when clutched, ws therefore probbly bout 33% lower thn indicted by the springs lone. Such effects probbly vried cross prticipnts, being dependent both on frme construction nd on individul humn chrcteristics. Wlking trils. Prticipnts wlked on tredmill t 1.25 m s 21 under seven conditions: norml wlking without the exoskeleton (No Exoskeleton or NE; wlking with the complete exoskeleton but no spring connected (No Spring or k 5 ; nd wlking with ech of the springs ttched (exoskeleton spring stiffness k 5 13, 18, 24, 31 nd 4 N m rd 21. In previous studies, humns hve tken bout 2 min to dpt fully to tethered pneumtic nkle exoskeletons 34. To llow sufficient time for lerning, prticipnts completed 21 min of trining under ech condition over three or four wlking sessions before dt collection. During trining, prticipnts wlked under ech condition for 7 min. Mechnicl filure of the clutch occurred for some conditions during some trining sessions, resulting in more collection sessions for some prticipnts, but n equl mount of trining (21 min with functioning exoskeleton for ll prticipnts nd conditions. Dt were collected during minutes 5 7 of finl 7 min session, or minutes of the multi-dy experiment. The order of presenttion of conditions ws rndomized for ech prticipnt on the first collection dy nd then held constnt for tht prticipnt over the reminder of the experiment. This ensured tht ech prticipnt s trining progress ws not confounded by ordering effects. Blinding ws not prcticl in this protocol. Biomechnics nd energetics mesurements. Body segment motions were mesured using reflective mrker motion cpture system (eight T-Series cmers, Vicon. Ground rection forces were mesured using tredmill instrumented with lod cells (Bertec. Ankle muscle ctivity (soleus, medil nd lterl gstrocnemius, tibilis nterior ws mesured using wired electromyogrphy system (SX23, Biometrics. Whole-body oxygen consumption nd crbon dioxide production were mesured using n indirect clorimetry system (Oxycon Mobile, CreFusion. Dt nlysis. Jointngles, moments nd powers were clculted from body motions nd ground rection forces using inverse kinemtics nd inverse dynmics nlyses 35 (Visul 3D, C-Motion. Components of joint moment nd power ttributed to the humn (biologicl component were clculted 36,37 by subtrcting the exoskeleton torque or power, mesured using onbord sensors, from the totl nkle joint moment or power, estimted using inverse dynmics. Centre-of-mss power ws clculted from ground rection forces using the individul limbs method 38. Muscle ctivity ws bnd-pss filtered (2 46 Hz in hrdwre nd then conditioned by rectifying nd low-pss filtering with cutoff frequency of 6 Hz in softwre. Medil nd lterl gstrocnemius signls were combined to simplify nlysis nd interprettion. Metbolic rte ws estimted from verge rtes of oxygen consumption (V O2 nd crbon dioxide production (V CO2 during the collection window using stndrd formul 39. The metbolic rte during quiet stnding ws subtrcted from gross metbolic rte to obtin the net vlue ttributble to the energetic demnds of wlking 2,1,16,22,26. Net metbolic rte vlues were then normlized to prticipnt body mss. Mechnics dt nd muscle ctivity from ech condition were broken into strides, determined s the period between subsequent heel strikes of single leg, nd n verge stride for ech prticipnt nd condition ws obtined. These verge strides were used to clculte vlues of verge moment, power nd muscle ctivity for ech prticipnt nd condition. Averge moment nd power vlues were clculted s the time integrl of moment nd power time series dt divided by stride period. Positive nd negtive verge joint moments nd powers were seprted out using time integrls of periods of positive or negtive moment or power, respectively. Averge net power ws clculted s the time integrl of power over the whole stride period. Averge moment nd power vlues were normlized to prticipnt body mss. Averge muscle ctivity ws clculted s the time integrl of muscle ctivity divided by stride period. Averge muscle ctivity during dditionl periods of interest ws clculted s the time integrl of muscle ctivity during those periods divided by stride period (for exmple, erly nd mid-stnce, defined s 4% stride, nd lte stnce, defined s 4 6% stride. Muscle ctivity ws normlized to the mximum vlue observed during norml wlking for ech muscle nd for ech prticipnt. For ech condition, study-wide verge trjectories of lower-limb joint ngles, moments nd powers were clculted by verging cross prticipnts, used for disply purposes in Fig. 2 nd Extended Dt Figs 3 8. Sttistics. For ech condition, mens nd stndrd errors of net metbolic rte, verge moment, verge power nd verge muscle ctivity outcomes were clculted cross prticipnts, with stndrd error indicting inter-prticipnt vribility. On the bsis of the expecttion tht user performnce would be nonliner function of exoskeleton stiffness 25, we conducted mixed-model, three-fctor ANOVA (rndom effect: prticipnt; fixed effects: spring stiffness nd squre of spring stiffness to test for n effect of spring stiffness cross exoskeleton conditions (significnce level 5.5; JMP Pro, SAS. For the primry outcome mesure, net metbolic rte, stiffness hd significnt effect. We used pired t-tests with Šídák Holm correction for multiple comprisons 4 to compre spring conditions with ech other nd with the No Exoskeleton condition to identify which exoskeleton springs excted significnt chnge in metbolic rte. We used Jrque Ber twosided goodness-of-fit test to confirm pplicbility of tests tht ssume norml distribution. For the primry outcome mesure, net metbolic rte, we lso used lest-squres regression to fit second-order polynomil (qudrtic function relting men outcome dt to exoskeleton spring stiffness. Additionl two-fctor ANOVA nlyses (rndom effect: prticipnt; fixed effect: spring stiffness were performed to test for n effect of spring stiffness cross exoskeleton conditions for secondry outcomes in joint mechnics, centre-of-mss mechnics nd muscle ctivity. These results re compiled in Supplementry Tble Wiggin, M. B., Collins, S. H. & Swicki, G. S. An exoskeleton using controlled energy storge nd relese to id nkle propulsion. Proc. IEEE Int. Conf. Rehbil. Robot. ( Wiggin, M. B., Swicki, G. S. & Collins, S. H. Apprtus nd clutch for using controlled storge nd relese of energy to id locomotion. US ptent 213/46218 ( Shmei, K., Swicki, G. S. & Dollr, A. M. Estimtion of qusi-stiffness nd propulsive of the humn nkle in the stnce phse of wlking. PLoS ONE 8, e59935 ( Glle, S., Mlcolm, P., Derve, W. & De Clercq, D. Adpttion to wlking with n exoskeleton tht ssists nkle extension. Git Posture 38, ( Winter, D. A. Biomechnics nd Motor Control of Humn Movement Ch. 7 (John Wiley, Frris, D. J. & Swicki, G. S. Linking the mechnics nd energetics of hopping with elstic nkle exoskeletons. J. Appl. Physiol. 113, ( Swicki, G. S. & Ferris, D. P. Mechnics nd energetics of level wlking with powered nkle exoskeletons. J. Exp. Biol. 211, ( Doneln, J. M., Krm, R. & Kuo, A. D. Simultneous positive nd negtive externl in humn wlking. J. Biomech. 35, ( Brockwy, J. M. Derivtion of formule used to clculte energy expenditure in mn. Hum. Nutr. Clin. Nutr. 41, ( Glntz, S. A. Primer of Biosttistics 65 (McGrw-Hill, Tucker, V. A. The energetic cost of moving bout: wlking nd running re extremely inefficient forms of locomotion. Much greter efficiency is chieved by birds, fish nd bicyclists. Am. Sci. 63, ( Doneln, J. M. et l. Bioenergy hrvesting: generting electricityduring wlking with miniml user effort. Science 319, ( Collins, S. H. & Kuo, A. D. Recycling energy to restore impired nkle function during humn wlking. PLoS ONE 5, e937 (21.

6 RESEARCH LETTER b c Energy Input System: Humn Wlking Energy Output Energy Input System: Humn Wlking with Powered Exoskeleton Energy Output Energy Input System: Humn Wlking with Unpowered Exoskeleton Energy Output metbolic energy muscle (η m+, η m- het metbolic energy muscle (η m+, η m- het metbolic energy muscle (η m+, η m- het tendon (E P het* tendon (E P het* tendon (E P het* body (E K, E P het* body (E K, E P het* body (E K, E P het* Mechnicl energy (E K, E P is constnt on verge (ll energy input is converted to het, totl system efficiency is zero Muscle efficiency for positive production (η m+.25 (costs more metbolic energy thn done Muscle efficiency for negtive bsorption (η m (costs metbolic energy to bsorb Muscle lso uses (wstes energy to perform functions tht do not produce, such s ctivting or producing isometric force synthetic energy (e.g. electricity Extended Dt Figure 1 Energy digrms for humn exoskeleton wlking. Ech digrm includes energy inputs, outputs, storge nd trnsfers within the system, depicted for stedy-stte wlking. In ech cse, ll chemicl or electricl energy input is eventully output s het, since the energy of the system is constnt on verge nd no useful is performed on the body or the environment. Energy efficiency, strictly defined, is therefore zero in ll cses, nd so energy effectiveness or energy economy is insted chrcterized in terms of cost of trnsport, which is the energy used per unit weight per unit distnce trvelled 41., Energy digrm for norml humn wlking. Muscles consume metbolic energy both to produce nd to bsorb it (nd to perform vriety of other functions, such s ctivting or producing force, nd so metbolic energy flows only into the system. Energy loss in muscle mnifests s het. Inside the system, tendons exchnge energy with both the muscle nd the body, while kinetic nd grvittionl potentil energy re exchnged within the body segments, ll t high efficiency. Body segment energy is dissipted only in dmping in soft tissues, for exmple during collisions, which is smll (bout 3% of the totl metbolic energy input 2, nd in friction from slipping of the feet ginst the ground, deformtion of the ground or ir resistnce, ll of which re negligible under typicl conditions. All of these losses mnifest s het. b, Energy digrm for wlking with powered exoskeleton. An dditionl energy input is provided in the form of, for exmple, electricity. The totl energy input (nd corresponding eventul dissiption of the system cn therefore increse, even if smller spring (E P ctutor (η +, η - Desired outcome: with electricl energy input, metbolic energy input decreses (totl dissiption my increse, system energy is unchnged, overll system energy economy my be worsened het* het spring (E P Desired outcome: metbolic energy input decreses (dissiption must lso decrese, system energy is unchnged, overll system energy economy must be improved * Typiclly smll frction of totl energy use (e.g. 3% in the cse of dmping in body segments 2 het* portion is borne by the humn, resulting in poorer overll energy economy. This hs been the cse with the two powered devices tht hve reduced the metbolic energy cost of humn wlking 2,16. In theory, overll energy economy could still be improved with powered device in three wys. First, positive from muscles could be replced by done by motor with higher efficiency. Second, negtive could be replced by genertion done by motor with higher (thn 212% efficiency, thereby usefully recpturing energy tht would otherwise be dissipted s het. In fct, becuse muscle expends metbolic energy to bsorb, it is theoreticlly possible to simultneously reduce metbolic rte nd cpture electricl energy with zero electricl input 42, lthough this hs yet to be demonstrted in prctice. Third, the powered device could pproximte n unpowered device, with negligible mounts of electricity used only to control the timing of elements such s clutches 43. c, Energy digrm for wlking with n unpowered exoskeleton. No dditionl energy supply is provided; so, unlike the powered cse, the only wy to decrese metbolic energy use is to reduce totl system energy dissiption, or, equivlently, to improve the energy economy of the system s whole. Note tht the only difference from norml humn wlking, in terms of energy flow, is the ddition of elements such s springs tht store nd trnsfer energy within the system. In this sense, reducing metbolic rte with pssive exoskeleton is kin to chnging the person s morphology such tht it is more energy-effective t locomotion.

7 RESEARCH shnk frme clutch spring nkle joint foot frme Extended Dt Figure 2 Exoskeleton frme design. A rigid crbon fibre shnk frme nd foot frme were custom-mde for ech prticipnt. The shnk section clmps onto the user s lower leg just below the knee nd connects to the foot frme through rotry joint t the nkle. The foot frme includes lever rm protruding to the rer of the heel, to which the prllel spring is connected. The clutch is mounted to the shnk frme posterior to the clf muscles.

8 RESEARCH LETTER Totl nkle moment (N m kg No exoskeleton No spring (k = k = 13 N m rd 1 k = 18 N m rd 1 k = 24 N m rd 1 k = 31 N m rd 1 k = 4 N m rd 1 Averge totl nkle moment (N m kg 1 b Whole stride *P = NE c Erly & mid stnce *P =.34 NE Pek totl nkle moment (N m kg 1 d Pek P = NE Exoskeleton torque (N m kg 1.5 e Ave. exoskeleton torque (N m kg 1.1 f Whole stride g Erly & mid stnce h Pek *P <.1 *P <.1 *P <.1.5 NE NE Pek exoskeleton torque (N m kg 1 1 NE Biologicl nkle moment (N m kg i disengges ing spring stretching spring recoil free rottion engges Averge biologicl nkle moment (N m kg j Whole stride NE k Erly & mid stnce NE Pek biologicl nkle moment (N m kg 1 Exoskeleton spring stiffness (N m rd 1 l Pek *P <.1 *P <.1 *P < NE Time (% stride period 9 1 Extended Dt Figure 3 Ankle moment contributions., Totl nkle moment, mesured using motion cpture system. Averge totl nkle moment (b during the entire stride nd (c during erly nd mid-stnce, defined s 4% stride, nd (d pek nkle moment. All spring conditions incresed verge totl joint moment slightly during erly stnce, but pek totl joint moment ws mintined cross conditions. e, Exoskeleton torque contribution, s mesured using onbord sensors. Averge exoskeleton torque (f during the entire stride nd (g during erly nd mid-stnce, defined s 4% stride, nd (h pek exoskeleton torque. Averge nd pek exoskeleton torque incresed with incresing exoskeleton spring stiffness, except with the highest stiffness spring. i, Biologicl contributions to nkle moment, clculted s the subtrction of the exoskeleton moment from the totl moment. Averge biologicl nkle moment (j during the entire stride nd (k during erly nd mid-stnce, defined s 4% stride, nd (l pek nkle moment. Ankle moments rising from muscle ctivity decresed with incresing exoskeleton spring stiffness, but with diminishing returns t high spring stiffness. N 5 9; brs, men; error brs, s.e.m.; P vlues, two-fctor ANOVA (rndom effect: prticipnt; fixed effect: spring stiffness.

9 RESEARCH Soleus ctivity No exoskeleton No spring (k = k = 13 N m rd 1 k = 18 N m rd 1 k = 24 N m rd 1 k = 31 N m rd 1 k = 4 N m rd 1 Averge soleus ctivity b Whole stride c Erly & mid stnce d Lte stnce *P =.7 *P <.1 P =.1 NE NE NE e f Whole stride g Erly & mid stnce h Lte stnce Gstrocnemius ctivity Averge gstrocnemius ctivity *P =.14 P = 1. *P =.7 NE NE NE Tibilis nterior ctivity i disengges ing spring stretching spring recoil free rottion engges Averge tibilis nterior ctivity j Whole stride NE k Erly & mid stnce NE Exoskeleton spring stiffness (N m rd 1 l Lte stnce *P =.18 P =.2 P =.3 NE Time (% stride period 9 1 Extended Dt Figure 4 Ankle muscle ctivity., Activity in the soleus, mono-rticulr muscle group tht cts to plntrflex the nkle. Averge soleus ctivity over (b the whole stride, (c erly nd mid-stnce, defined s 4% stride, nd (d lte stnce, defined s 4 6% stride. Soleus ctivity decresed with incresing spring stiffness. e, Activity in the gstrocnemius, birticulr muscle group tht cts to plntrflex the nkle nd flex the knee. Averge gstrocnemius ctivity over (f the whole stride, (g erly nd mid-stnce, defined s 4% stride, nd (h lte stnce, defined s 4 6% stride. Gstrocnemius ctivity ws reduced compred with the No Exoskeleton condition during erly nd mid-stnce, but incresed with incresing spring stiffness during lte stnce. i, Activity in the tibilis nterior, mono-rticulr muscle group tht cts to dorsiflex the nkle. Averge tibilis nterior ctivity over (j the whole stride, (k erly nd mid-stnce, defined s 4% stride, nd (l lte stnce, defined s 4 6% stride. Tibilis nterior ctivity seemed to increse during erly nd mid-stnce, nd ws unchnged during lte stnce. All vlues were mesured using electromyogrphy nd normlized to mximum ctivity during norml wlking. N 5 8; brs, men; error brs, s.e.m.; P vlues, two-fctor ANOVA (rndom effect: prticipnt; fixed effect: spring stiffness.

10 RESEARCH LETTER Totl nkle power (W kg No exoskeleton No spring (k = k = 13 N m rd 1 k = 18 N m rd 1 k = 24 N m rd 1 k = 31 N m rd 1 k = 4 N m rd 1 Averge totl nkle power (W kg 1 b Positive power c Negtive power d Net power *P <.1 *P <.1 P = NE NE NE Exoskeleton power (W kg e Averge exoskeleton nkle power (W kg 1 f Positive power g Negtive power h Net power.1 *P <.1 *P <.1 *P < NE NE NE Biologicl nkle power (W kg i disengges ing spring stretching spring recoil free rottion engges Averge biologicl nkle power (W kg j Positive power NE k Negtive power NE Exoskeleton spring stiffness (N m rd 1 l Net power *P <.1 *P <.1 *P =.2 NE Time (% stride period 9 1 Extended Dt Figure 5 Ankle power contributions., Mechnicl power of the combined humn exoskeleton system, mesured using motion cpture system, (b verge positive power, defined s positive divided by stride time, (c verge negtive power, defined s negtive divided by stride time, nd (d verge net power, equivlent to verge power, defined s the sum of positive nd negtive divided by stride time. Totl positive nkle joint power decresed with incresing stiffness, while net joint power incresed. e, Exoskeleton power, mesured using onbord sensors for torque nd motion cpture for joint velocity, (f verge positive exoskeleton power, (g verge negtive exoskeleton power nd (h verge net exoskeleton power. Net exoskeleton power ws lwys negtive. i, Biologicl nkle power, defined s the subtrction of exoskeleton power from totl nkle power, (j verge positive biologicl power, (k verge negtive biologicl power nd (l verge net biologicl power. Net biologicl power incresed with the exoskeleton compred with norml wlking. N 5 9; brs, men; error brs, s.e.m.; P vlues, two-fctor ANOVA (rndom effect: prticipnt; fixed effect: spring stiffness.

11 RESEARCH Knee joint moment (N m kg disengges ing spring stretching spring recoil free rottion b Whole stride, rectified No exoskeleton c Erly stnce d Lte stnce No spring (k = P =.2 *P =.6 *P <.1 k = 13 N m rd 1.2 k = 18 N m rd 1 k = 24 N m rd 1 k = 31 N m rd 1.15 k = 4 N m rd 1.1 engges Averge knee moment (N m kg NE NE Exoskeleton spring stiffness (N m rd 1 NE Time (% stride period 9 1 Extended Dt Figure 6 Knee moment., Knee moment in time s mesured by motion cpture, (b verge bsolute knee moment over the entire stride, (c verge knee moment during erly stnce, defined s the positive impulse within pproximtely 1 3% stride divided by stride period, nd (d verge knee moment during lte stnce, defined s the negtive impulse within pproximtely 3 5% stride divided by stride period. Averge knee moment during lte stnce incresed in mgnitude with the highest stiffness springs. Positive vlues denote knee extension. N 5 9; brs, men; error brs, s.e.m.; P vlues, two-fctor ANOVA (rndom effect: prticipnt; fixed effect: spring stiffness.

12 RESEARCH LETTER Hip joint moment (N m kg 1 Hip joint ngle (rd d No exoskeleton No spring (k = k = 13 N m rd 1 k = 18 N m rd 1 k = 24 N m rd 1 k = 31 N m rd 1 k = 4 N m rd 1 Knee joint moment (N m kg 1 Knee joint ngle (rd b e Biologicl nkle joint moment (N m kg 1 Ankle joint ngle (rd c f Hip joint power (W kg g disengges ing spring stretching spring recoil free rottion engges Knee joint power (W kg h disengges ing spring stretching spring recoil free rottion Biologicl nkle joint power (W kg 1 engges i disengges ing spring stretching spring recoil free rottion engges Time (% stride period 9 1 Extended Dt Figure 7 Hip, knee nd nkle joint mechnics. Joint ngles, moments nd powers re presented t the sme scle to fcilitte comprisons cross joints., Hip joint ngle, (b knee joint ngle nd (c nkle joint ngle. Joint ngle trjectories did not pper to chnge substntilly cross conditions. d, Hip moment, (e knee moment nd (f biologicl component of nkle moment. Hip moment did not pper to chnge substntilly cross conditions, while knee moment nd nkle moment showed trends detiled in Time (% stride period Time (% stride period 9 1 Extended Dt Figs 6 nd 3, respectively. g, Hip joint power, (h knee joint power nd (i the biologicl component of nkle joint power. Hip nd knee power did not pper to chnge substntilly cross conditions, while biologicl nkle power showed trends detiled in Extended Dt Fig. 5. Positive vlues denote hip extension, knee extension nd nkle plntrflexion with respect to stnding posture. N 5 9.

13 RESEARCH Biologicl centre of mss power (W kg ing spring stretching spring recoil free rottion No exoskeleton No spring (k = k = 13 N m rd 1 k = 18 N m rd 1 k = 24 N m rd 1 k = 31 N m rd 1 k = 4 N m rd 1 Averge biologicl centre of mss power (W kg 1 b Collision.25 P = NE c Rebound NE d Prelod *P <.1 P =.1 NE Exoskeleton spring stiffness (N m rd 1 e Push-off *P <.1 NE Time (% stride period 9 1 Extended Dt Figure 8 Centre-of-mss mechnics., The biologicl contribution to centre-of-mss power for ech individul limb, defined s the dot product of ground rection force with centre-of-mss velocity, both determined from force plte dt, minus the nkle exoskeleton power. b, Averge collision power, defined s the negtive performed during the first hlf of stnce divided by stride time. c, Averge rebound power, defined s the positive performed during mid-stnce divided by stride time. d, Averge prelod power, defined s the negtive performed during mid-stnce divided by stride time. e, Averge push-off power, defined s the positive performed during lte stnce divided by stride time. With incresing spring stiffness, the humn contribution to push-off decresed, while the humn contribution to rebound incresed substntilly. N 5 9; thin lines, contrlterl limb; brs, men; error brs, s.e.m.; P vlues, two-fctor ANOVA (rndom effect: prticipnt; fixed effect: spring stiffness.

14 RESEARCH LETTER Extended Dt Tble 1 Pssive nkle exoskeleton mss by component Segment US Size 8 US Size 13 Crbon Fiber Foot Section Aluminum Ankle Joints (x2 Crbon Fiber Shnk Section 13 g 16 g 4 g 4 g 15 g 17 g Frme Mss 275 g 37 g Averge Spring 76 g 76 g Mechnicl Clutch 57 g 57 g Totl Mss 48 g 53 g

15 RESEARCH Extended Dt Tble 2 Comprison of nkle exoskeleton msses Author Mooney et l. 16 Mss of Exoskeleton (per leg 2, g Swicki et l. 37 1,21 g* Mlcolm et l g* Pssive Elstic (US size 13 Pssive Elstic (US size 8 53 g 48 g *Does not include tethered hrdwre.