©2015.PublishedbyTheCompanyofBiologistsLtd|TheJournalofExperimentalBiology(2015)218,711-719doi:10.1242/jeb.106518 RESEARCHARTICLE Biomechanics and energetics of running on uneven terrain AlexandraS.Voloshina1,2,*andDanielP.Ferris1 ABSTRACT McAndrew et al., 2010) and could utilize the same strategy to improve running stability as well. A recent study showed that In the natural world, legged animals regularly run across uneven assistingwithlateralbalanceduringrunningresultedinreducedstep terrain with remarkable ease. To gain understanding of how widthvariabilityandenergyexpenditureinhumans(Arellanoand runningonuneventerrainaffectsthebiomechanicsandenergetics Kram, 2012). In contrast, if uneven terrain leadsto increased step of locomotion, we studied human subjects (N=12) running at 2.3ms−1onanuneventerraintreadmill,withuptoa2.5cmheight width variability, it may contribute to increased energetic coststo maintainbalance. variation. We hypothesized that running on uneven terrain would Changes in surface height variability are likely to alter muscle show increased energyexpenditure, step parameter variabilityand activation patternsand mechanical work duringrunning.Running leg stiffness compared with running on smooth terrain. Subject energy expenditure increased by 5% (0.68W kg−1; P<0.05) when onsand,forexample,resultsingreatermuscleactivity,greaterhip andkneemotion,andgreaterpositivemechanicalworkcompared runningonuneventerraincomparedwithsmoothterrain.Stepwidth with running on a smooth flat surface (Lejeune et al., 1998; andlengthvariabilityalsoincreasedby27%and26%,respectively Pinningtonetal.,2005).Thesechangesarelikelycontributorstothe (P<0.05). Positive and negative ankle work decreased on uneven terrainby22%(0.413Jkg−1)and18%(0.147Jkg−1),respectively increasedenergyexpenditureforrunningonsandcomparedwitha smooth,hardsurface(Pinningtonetal.,2005).Inaddition,wehave (P=0.0001 and P=0.0008). Mean muscle activity increased on previouslyfoundthathumansubjectsshowedgreaterhipandknee uneventerrainforthreemusclesinthethigh(P<0.05).Legstiffness jointflexionmotionsduringswingwhenwalkingonuneventerrain also increased by 20% (P<0.05) during running on uneven terrain comparedwitheventerrain(Voloshinaetal.,2013).Itisreasonable comparedwithsmoothterrain.Calculationsofgravitationalpotential toexpectsimilarmodificationsinswinglegdynamicsforrunning energyfluctuationssuggestthatabouthalfoftheenergeticincreases onasimilarunevensurface.Inadditiontoincreasedmuscleactivity, canbeexplainedbyadditionalpositiveandnegativemechanicalwork runningontheunevensurfacemayalsodisruptpatternsofmuscle for up and down steps on the uneven surface. This is consistent recruitment.Effectiveenergystorageandreturnduringlocomotion betweenwalkingandrunning,astheabsoluteincreasesinenergetic requiresmuscleactivationtoproduceaconcertedcontraction(Hof costforwalkingandrunningonuneventerrainweresimilar:0.68and 0.48W kg−1, respectively. These results provide insight into how etal.,1983),orcontractionsthatminimizethechangeinlengthof themusclefiberandmaximizetendonandaponeurosisstretchand surface smoothness can affect locomotion biomechanics and recoil. Because work produced from elastic energy storage and energeticsintherealworld. return contributes to about half of the total mechanical work KEYWORDS:Energyexpenditure,Jointwork,Kinematics,Leg performed during running (Cavagna et al., 1964), a reduction in stiffness elastic work would require increased muscle work and would be more energetically costly. As a result, these factors have the INTRODUCTION potentialtocontributetorunningenergeticcostsrelatedtosurface Empiricalmeasurementshavedocumentedthatrunningonnatural smoothness. surfaces such as sand, grass or irregular trails requires greater Legstiffnessisalsolikelytochangewithincreasedsurfaceheight metabolicenergyexpenditurethanrunningonsmoothhardsurfaces variability. During human reaching in the presence of expected (Jensenetal.,1999;Lejeuneetal.,1998;PinningtonandDawson, mechanicalperturbations(Burdetetal.,2001;Franklinetal.,2007), y 2001; Zamparo et al., 1992). Such natural terrain has many arm stiffness tends to increase compared with reaching without g o mechanicalpropertiesthatcaninfluencerunningbiomechanics.For perturbations.Thenervoussystemmayrespondtoexpectedlower l o example,humansandanimalsneedtoconstantlyadjustforchanges limbperturbationssimilarly.Inaddition,Grimmeretal.haveshown i B insurfacedamping,complianceandsmoothnessduringlocomotion thathumanrunnersincreaselegstiffnessinanticipationofasingle l in the real world. To identify the energetic and biomechanical step-up when running on an uneven track (Grimmeret al., 2008). ta changes during running caused by increased surface height However, runners then decrease their leg stiffness for the actual n e variability, we studied human running on an uneven surface step-up, possibly to smooth out the perturbation to the center of m designedtomimicnaturalterrain. mass trajectory. It is likely that runners would also adjust leg ri e Step parameter adjustments are one potential factor that could stiffnessinresponsetorunningonuneventerrain. p contribute to increased energy expenditure during running on In this study, we examined the energetic and biomechanical x E uneven terrain. In particular, humans adjust step width for changes during running on uneven terrain when compared with f maintaining lateral balance during walking (Hak et al., 2012; runningonsmoothterrain.Weusedanuneventerrainsurfacethat o l was attached to a standard exercise treadmill (Fig. 1) to collect a n 1SchoolofKinesiology,UniversityofMichigan,AnnArbor,MI,USA.2Departmentof continuous energetic and kinematic data of human runners. We r MechanicalEngineering,UniversityofMichigan,AnnArbor,MI,USA. hypothesizedthat,onuneventerrain,subjectswouldshowgreater u o energy expenditure and step parameter variability. Based on J *Authorforcorrespondence(voloshis@umich.edu) e previous research indicating increased limb stiffness under h Received1July2014;Accepted18December2014 conditions of anticipated mechanical perturbations, we also T 711 RESEARCHARTICLE TheJournalofExperimentalBiology(2015)218,711-719doi:10.1242/jeb.106518 Fig.1.Studyapparatus.(A)Uneventerraintreadmillusedfor therunningstudies.(B)Schematicrepresentationoftheuneven surface,withsteppingareasofthreedifferentheights(arrows indicatethetreadmill’slongaxis).(C)Close-upoftheblocks comprisingthesteppingareas.Dimensions:H,1.27cm;L, 15.2cm;W,2.54cm. expected runners to increase leg stiffness on uneven terrain the percentage increase found during walking on uneven terrain. compared with smooth terrain. Our overall objective was to Incontrasttorunning,metabolicenergyexpenditureduringwalking provide insight into how the biomechanical adjustments lead to onuneventerrainincreasedfrom2.51±0.24to3.19±0.14Wkg−1 greaterenergyexpenditureduringrunningonunevensurfaces. (P=0.0004), or by ∼27%. This increase in metabolic cost was consistentwiththe28%energyincreasefoundinourpreviousstudy RESULTS onwalkingonuneventerrain(Voloshinaetal.,2013).Thissuggests Runningonuneventerrainresultedinincreasedenergyexpenditure thatthebiomechanicaladaptationsduringwalkinginthisstudyare compared with running on smooth terrain. Several biomechanical likely the same as we have previously described, even though adjustmentscontributedtothisincreaseinenergeticcost.Subjects walking surfaces and subject footwear differed between the two did not exhibit changes in mean step parameters between the two studies. Although the percentage increases in energy expenditure conditions,butthereweredifferencesinstepparametervariability. weredifferentbetweenwalkingandrunning,theabsoluteincreases Jointangle,torqueandpowerweremostlyunaffectedbytheterrain in energetic cost were similar: 0.68 and 0.48W kg−1 for walking and only the ankle joint showed a significant decrease in joint and running, respectively. The mean standing metabolic rate was power.Inaddition,weobservedincreasedmuscleactivityinthree 1.46±0.17Wkg−1. proximal leg muscles (vastus medialis, rectus femoris and medial hamstring), and increased muscle mutual contraction between the Kineticsandkinematics vastus medialis and medial hamstring muscles. Subjects also Wesawnochangesinmeanstepparameters(width,length,height demonstrated higher leg stiffness when running on uneven terrain and period), although step variability increased for all parameters comparedwithsmoothterrain. during running on uneven terrain compared with even terrain (Table1).Inparticular,stepwidth,lengthandheightvariabilityall Metabolicenergyexpenditure increased significantly by approximately 27%, 26% and 125%, Running andwalking ontheuneven terrainresulted insignificant respectively (P<0.05) on uneven terrain. In addition, step period increases in energyexpenditurewhen compared with runningand variability on uneven terrain increased significantly by 30% walking on the even surface (Fig. 2). During running, energetic (P<0.05). cost increased from 9.72±0.65 to 10.2±0.94W kg−1 (mean±s.d., Subjects showed few changes in joint kinematics and kinetics P=0.008),orabout5%fromeventouneventerrain.Thispercentage duringrunningonuneventerraincomparedwitheventerrain,with increase in running energy expenditure was much lower than mostnotablechangesoccurringattheanklejoint.Duringrunning onuneventerrain,jointanglesinthesagittalplaneshowedslightly higherpeakflexionanglesinthekneeandhipduringmid-stance, possibly to allow for greater leg clearance (Fig. 3). Qualitative y examinationoftheankleangleshowedaslightlydecreasedrangeof g o motion on uneven terrain compared with even terrain, although l o subjectsappearedtomaintainasimilarheel-strikefootfallpatternon i B thetwosurfaces.Thisreducedrangeofanklemotionsuggeststhat l a subjectsranwithslightlyflatterfeetwhenonunevenground.The t n ankle joint also showed an approximately 14% decrease in peak e joint moment, around mid-stance. In contrast, the knee and hip m jointsshowedlittlechange.Changesinjointpowerwereonlyseen ri e aroundtheankleandknee,withthetwojointsshowingdecreasesin p power around mid-stance (by 29% and 23%, respectively), when x E running on uneven terrain. Ankle power also decreased by 25% f Fig.2.Netmetabolicrateforwalkingandrunningontheevenanduneven priortopush-offandat∼40%ofstridetime.Thetimingoftoe-off o l surfaces.Allnetmetabolicratesarenormalizedtosubjectmassandshowthe withrespecttostridetimingdidnotdifferbetweenthetworunning a n absolutechangesinenergeticswhenwalkingandrunningonuneventerrain conditions. r comparedwithsmoothterrain.Percentagesindicatetheincreasesinenergetic u Joint motion variability was also greater on uneven terrain o costcausedbyuneventerrainwhencomparedwithevenwalkingorrunning. comparedwitheventerrain(Fig.3).Surfaceunevennessincreased J Asteriskssignifyastatisticallysignificantdifferencebetweentheevenand e unevenwalkingandrunningconditions(posthocpair-wisecomparisons, ankle and knee angle variability by approximately 25%, and hip h α=0.05). angle variability by 35% when compared with even terrain (all T 712 RESEARCHARTICLE TheJournalofExperimentalBiology(2015)218,711-719doi:10.1242/jeb.106518 Table1.Stepparametersforrunningontheevenandunevensurfaces Even Uneven P-value Mean±s.d. Variability(mean±s.d.) Mean±s.d. Variability(mean±s.d.) Mean Stepvariability Stepwidth 0.055±0.029 0.022±0.004 0.059±0.033 0.028±0.006* 0.353 <0.0001 Steplength 0.881±0.051 0.035±0.009 0.884±0.044 0.044±0.011* 0.385 0.0002 Stepheight – 0.004±0.001 – 0.009±0.002* – <0.0001 Stepperiod(s) 0.729±0.041 0.010±0.003 0.731±0.033 0.013±0.003* 0.427 0.0014 Parametersincludestepperiodandthemeanstepwidth,lengthandheightandtheirrespectivevariabilities(allnormalizedtosubjectleglength,mean0.944m). Stepvariabilityisdefinedasthes.d.ofstepdistancesoveratrial,reportedasthemean(±s.d.)acrosssubjects. Asteriskssignifyastatisticallysignificantdifferencebetweentheevenandunevenrunningconditions(posthocpair-wisecomparisons,α=0.05). P<0.05). Ankle moment variability also increased by about 60%, All but three muscles showed a significant increase in while knee and hip moment variability more than doubled on electromyographic (EMG) variability when running on the uneven terrain (all P<0.05). Joint power variability increased by uneven terrain (Fig. 5). Only two muscles in the lower leg and 50%fortheankleand∼70%forthekneeandhip(allP<0.05). three muscles in the thigh showed increases in variability (s.d. of Running on the uneven surface also affected the amount of muscleactivity),withthemeanincreaseinvariabilitybeingslightly positiveandnegativejointworkdoneattheankle(Fig.4).Positive higherinthethighmuscles(meanincreaseof14%and25%inthe ankleworkdecreasedby0.413Jkg−1(22%)whilenegativeankle lowerlegandthighmuscles,respectively).Inthelowerleg,boththe work decreased by 0.147J kg−1 (18%; P=0.0001 and P=0.0008, soleus(SO)andlateralgastrocnemius(LG)showed14%increases respectively).Positiveandnegativejointworkforthekneeandhip in s.d. (P<0.05), while the tibialis anterior (TA) and medial werenotstatisticallydifferentbetweenthetworunningconditions. gastrocnemius(MG)showednosignificantchanges.Forthethigh muscles,VM,RFandMHshowed15%,35%and26%increasesin Muscleactivation musclevariability,respectively(P<0.05). Subjects showed increases in muscle activity variability, mean Out of the three pairs of antagonistic muscles, we observed muscleactivityandmuscleco-activationinthethighmuscleswhen increasedmuscleco-activationovertheentirestrideonlyintheMH/ runningonuneventerraincomparedwithrunningonevenground VMmusclepair(Table2).However,whenwebrokedownthestride (Fig. 5). Significant increases in mean muscle activity were only into 1%increments,we noticedsignificant increases in muscle co- noted in three of the thigh muscles; vastus medialis (VM), rectus activationinthefirst5%ofthestrideintheMH/VLmusclepairas femoris(RF)andmedialhamstring(MH)activityincreasedby7%, well. Similarly, the MH/VM pair showed increased muscle co- 20%and19%,respectively(P<0.05).However,thevastuslateralis activationduringthefirst5%ofthestridebutalsoslightlybeforeand (VL) and all muscles in the lower leg showed no significant duringtoe-off.Themusclepairalsodemonstratedincreasedmuscle differencesinmeanmuscleactivitybetweenconditions(Fig.6). co-activation during swing, although, because of minimal muscle activityofthetwomusclesduringthistime,theseincreasesarelikely Fig.3.Jointangle,torqueandpowerversusstride timeforrunningonevenanduneventerrain.Plotted insolidlinesarethemeantrajectoriesfortheankle, kneeandhipagainstpercentagestridetimeforrunning duringunevenandeventerrainconditions.Shaded areasdenotethemeans.d.envelopesacrosssubjects fortheunevencondition,dashedlinesfortheeven condition.Stridesstartandendatsame-sideheel- strike.Dashedverticalgraylineindicatestoe-off.Ext., extension;Flex.,flexion. y g o l o i B l a t n e m i r e p x E f o l a n r u o J e h T 713 RESEARCHARTICLE TheJournalofExperimentalBiology(2015)218,711-719doi:10.1242/jeb.106518 compared with even terrain (P=0.0002). In addition, vertical ground reaction force variability more than tripled when running onuneventerrain(P<0.05). Subjectsraninaslightlymorecrouchedposturewhenonuneven terrain compared with running on the even surface (Fig. 7A). Subjects contacted the ground at heel-strikewith a more bent leg, and hence a shorter leg length (0.992±0.022 and 0.984±0.022, dimensionless, for even and uneven terrains, respectively; P=0.0018), defined as the straight-line distance from the greater trochanter marker to the fifth metatarsal markerof the stance foot and normalized to mean subject leg length. Similarly, leg length before toe-off decreased significantly from 1.02±0.011 to 1.01± 0.015 (dimensionless; P<0.0001). In addition, the minimum leg length during mid-stance was longer on uneven terrain (0.907± 0.014 and 0.912±0.015, dimensionless, for even and uneven terrains, respectively; P=0.0041). This resulted in a 15% decrease in themaximum changein leg length, from 0.085±0.023on even ground to 0.072±0.019 on uneven terrain (dimensionless; P<0.0001). Fig.4.Ankle,kneeandhipworkperstrideforthetworunningconditions. Primarily due to different leg length dynamics, subjects ran on Valuesareshownforpositiveandnegativeworkforthethreejoints,witherror stifferlegswhenrunningonuneventerraincomparedwithrunning barsdenotings.d.Dashedlinesindicatenetworkforthespecificjointand condition,andasteriskssignifyastatisticallysignificantdifferencebetweenthe onevenground(Fig.7B).Usingthemoretraditional legstiffness evenandunevenrunningconditions(posthocpair-wisecomparisons,α=0.05). calculation (defined as the ratio between the maximum vertical groundreactionforceandthemaximumleglengthdisplacement), inconsequential. The TA/SO muscle pair showed no significant wefounda20%differenceinlegstiffnessbetweenthetwosurfaces increasesinmuscleco-activationatanypointinthestride(Fig.5). (from 27.9±6.40 on even terrain to 33.4±7.54 on uneven terrain, dimensionless; P<0.0001). Similarly, the second leg stiffness Verticalgroundreactionforcesandlegstiffness calculation(definedasthelinearfittotheverticalgroundreaction Vertical ground reaction forces, normalized to subject weight, force versus leg displacement) showed a 10% increase in leg remained largely unchanged for running on uneven terrain stiffness (from19.7±2.10oneventerrainto 21.8±2.74onuneven compared with even terrain (Fig. 7A). The maximum force, fmax, terrain,dimensionless;P<0.0001). occurred around 40% of stance and had a peak at 2.19±0.11 (dimensionless; P=0.753). The peak maximum force was not DISCUSSION statisticallydifferentforthetworunningconditions.However,the In this study we quantified the changes in energetics and impact peak increased byapproximately 17% (from 1.34±0.19 to biomechanics between running on uneven terrain and on flat, 1.57±0.25, dimensionless) when running on uneven terrain smooth terrain. Our findings supported our hypotheses, primarily Fig.5.Averagedelectromyographic(EMG) activityversusstridetimeforrunningoneven anduneventerrain.AllEMGprofileswere normalizedtothemaximummeanmuscleactivity overthetworunningconditions,foreachmuscle andsubject.Stridesstartandendatsame-side heel-strikes.Dashedverticalgraylineindicates toe-off.Shadedareasdenotethemeans.d. y g envelopesacrosssubjectsfortheuneven o condition,dashedlinesfortheevencondition. l o Graybarsindicatestatisticallysignificant i B increasesinmutualmusclecontraction,with l darkercolorsindicatinglargerpercentage a t increasesfromtheeventotheunevenrunning n condition.TA,tibialisanterior;SO,soleus;MG, e m medialgastrocnemius;LG,lateral gastrocnemius;RF,rectusfemoris;MH,medial ri e hamstring;VL,vastuslateralis;VM,vastus p medialis. x E f o l a n r u o J e h T 714 RESEARCHARTICLE TheJournalofExperimentalBiology(2015)218,711-719doi:10.1242/jeb.106518 Fig.6.MeanrectifiedEMGactivityvalues.MeansubjectEMGprofileswere firstnormalizedtomaximummeanmuscleactivityoverthetworunning conditions,foreachmuscleandsubject,andthenaveragedoverstridetimeto producesubjectaverageEMGactivityvalues.SubjectaverageEMGactivity wasthenaveragedoversubjectstoproducemeanEMGactivityvalues.Bars indicates.d.acrosssubjects.Asteriskssignifyastatisticallysignificant differencebetweentheevenandunevenrunningconditions(posthocpair- wisecomparisons,α=0.05). that running is more energetically costly on uneven terrain compared with even terrain. However, this increase was much smaller than the increase caused by the same surface during walking.Morespecifically,wefounda0.68Wkg−1(27%)increase inmetaboliccostduringwalkinganda0.48Wkg−1(5%)increase Fig.7.Verticalgroundreactionforces,effectiveleglengthandleg stiffnesscalculationsforthetworunningconditions.(A)Meanvertical during running. Although the percentage changes were quite groundreactionforcesnormalizedtosubjectweight(solidlines),andeffective differentbetweenthetwolocomotiontypes,itisimportanttonote leglengthsnormalizedtomeansubjectleglength(thickdashedlines),versus that the absolute increases were very similar. These absolute stancedurationforrunningonevenanduneventerrain.Shadedareadenotes energeticincreasescouldberelatedtothetotalmechanicalenergy themeans.d.envelopeacrosssubjectsfortheverticalgroundreactionforce fluctuations caused by the uneven surface. For example, running ontheunevencondition,thindashedlinesindicatetheenvelopefortheeven condition.(B)Normalizedverticalgroundreactionforceplottedagainstthe uphill and downhill for an equal distance would result in greater normalizedeffectiveleglengthforthetworunningconditions.Meanleg energyexpenditurethanrunningonlevelgroundforthesametotal stiffnessvaluesarepresentedfortwolegstiffnesscalculationmethods:k max distance (Margaria, 1968). If we equate the uneven surface to a equalsthemaximumforcedividedbythemaximumleglengthdisplacement series of steps up and down an incline, it would be reasonable to andk istheslopeofthelinearfittothelegstiffnesscurve.s.d.valuesare fit expectanincreaseinenergyexpenditureaswell.Ifweconsiderthe acrosssubjects. meansteplengthofourrunners(0.884m)andthemaximumstep y height change of the uneven terrain (0.025m), our uneven terrain smaller.Thissuggeststhatfactorsotherthanchangesinmechanical og surface would be roughly equivalent to running up and down a work contribute to energy expenditure on uneven terrain during ol 1.6%incline.Inaddition,wecouldexpectthisinclinetoresultinan running. Bi energyincreaseof∼0.35Wkg−1(Margariaetal.,1963).However, As expected, we saw changes in step length and width l a thetrueenergetic increaseduetoinclinevariationsislikelymuch variabilities across the two surfaces. On uneven terrain, runners t n showed33%and26%increasesinstepwidthandlengthvariability, e respectively(P<0.05).Thisisconsistentwithpastresearch,which m Table2.Musclemutualcontractionovertheentirestride has shown that challenges to locomotor stability tend to produce ri Even(mean±s.d.) Uneven(mean±s.d.) P-value morestepvariabilityduringwalking(Thiesetal.,2005;Voloshina pe TA/SO 105.7±36.34 109.5±32.83 0.6527 et al., 2013). Greater step variability during walking also seems x E MH/VM 106.4±28.05 134.7±34.31* 0.0168 related to active stabilizing adjustments for maintaining lateral f MH/VL 123.3±66.60 125.5±28.02 0.9244 balance(BaubyandKuo,2000;Donelanetal.,2001).Incontrast, o l Valuessignifythedimensionlessareaundertheminimumofthenormalized duringrunning,humanstendtoprefernarrowstepwidthscloseto a n EMGcurvesforthetwomusclesofinterest.Threemuscleantagonistpairs themidlineofthebody(Cavanagh,1987).Thisisbecausenarrow r arecompared:tibialisanterior/soleus(TA/SO),medialhamstring/vastus u step widths result in reduced lateral moments about the center of o medialis(MH/VM)andmedialhamstring/vastuslateralis(MH/VL).s.d.are mass and tend to reduce energetic cost compared with larger step J calculatedacrosssubjects.Asteriskssignifyastatisticallysignificant e differencebetweentheevenandunevenrunningconditions(posthocpair- widths. Based on previous research (Arellano and Kram, 2011), h wisecomparisons,α=0.05). reducingstepwidthandstepwidthvariabilityduringrunningleads T 715 RESEARCHARTICLE TheJournalofExperimentalBiology(2015)218,711-719doi:10.1242/jeb.106518 to a reduction in energy expenditure. However, our subjects only stiffness adjustments across the surfaces. Vertical ground reaction showeda27%increaseinstepwidthvariabilityandnochangein force profiles were also largely unchanged, with only the impact the mean step width. These changes are relatively small and peak magnitude increasing by 17%. This increase suggests that nowherenearthemagnitudenecessarytoproducea5%increasein subjectslandedwithahighercontactforce,likelyduetoflatterfeetat energyexpenditure(ArellanoandKram,2011).Thissuggeststhat groundcontact.However,themaincauseofincreasedlegstiffnessis the energetic increase caused by changes in step parameters was thechangeinlowerlimbposture.Whenrunningonuneventerrain, negligible. subjectscontactedthegroundatheel-strikewithashorterleglength, Asignificantfindingofourstudyisthattheabsolutechangesin and had a longer leg length during mid-stance and a shorter leg energetic cost are independent of locomotor gait. Although lengthattoe-off.Thischangeinposture,andinturninlegstiffness, percentage increases in energetic cost were significantly different canbetheresultofseveralfactors.Previousresearchonupperlimb (27% and 5% for walking and running, respectively) the absolute movementshasshownthathumanstendtostiffentheirjointswhen changeswererelativelyclose(0.68and0.48Wkg−1forwalkingand presented with unfamiliar tasks, likely in anticipation of potential running,respectively).Thesimilarabsolutechangesforwalkingand perturbations. Similarly, Blum and colleagues (Blum et al., 2011) runningsuggestthatthedominantfactorresponsibleforincreasesin haveshownthatamorecrouchedlegpostureduringavianrunning metaboliccostduringlocomotiononunevensurfacesmayberelated maybeanadaptationmechanism,asitallowsforlengtheningand tosurfaceheightvariabilityandthecorrespondingverticalmotionof shortening of the limb. As a result, the more crouched running the center of mass. It would be interesting to examine a range of postureandoveralllargerlegstiffnessonuneventerrainislikelyan surfaceheightvariabilitiesandtheireffectsonwalkingandrunning adaptationresponsetoanunfamiliarenvironment.Infuturestudies, energetics. This could provide insight into whether walking and it may be interesting to look into the changes in leg stiffness running have similar biomechanical mechanisms responsible for throughouttrainingperiods,wheresubjectsareallowedtobecome energeticcostdifferences. familiarwiththesurfaceoverlongerperiodsoftime. Another important finding of this study is that the lower limb This study had several limitations related to kinetic joints that compensate for locomotion on uneven terrain are very measurements. The accuracy of the force measurements during differentbetweenwalkingandrunning.Duringwalking,anklejoint uneven terrain running was one such limitation. As described dynamics remain invariable while the knee and hip joints previously, the uneven terrain treadmill was placed atop two compensate with greater positive work production (Voloshina supports,eachofwhichwasplacedontopofaforceplatform.The et al., 2013). In contrast, running on uneven terrain only forces recorded from each platform were then added together to significantlyaffects work done at the ankle joint. The most likely obtainthetotalgroundreactionforces.Thetreadmillwasnotrigidly explanation for this contrast in joint kinetic adaptations is the attachedtothesupportsandtherewassomeslackinthebelttowhich relianceondifferentbiomechanicalmechanismsforthetwogaits. the uneven surface was attached. As a result, the force data were Runningcanbecomparedtoaspring-masssystem,withthelower noisier than data collected with our in-ground, instrumented limb functioning as if it were a single compression spring (Farley treadmill.Toaccountfortheadditionalnoise,welow-passfiltered andFerris,1998;McMahonandCheng,1990).Incontrast,walking the ground reaction force data using a cut-off frequency of 6Hz, hasinvertedpendulumdynamicswithdifferentiationbyjointthatis ratherthanamoretraditionalcut-offfrequencyof25Hz.Weused unlike running (Alexander, 1992; Farley and Ferris, 1998; Kuo, thesamefilteringtechniquesforbothsurfaceconditions.Totestthe 2001;McGeer,1990).Thesedifferencesinfundamentaldynamics validity of comparing running for these different experimental suggestthateachgaithasdifferentbenefitsanddrawbackstojoint- setups, we compared a representative subject running on the in- specificadaptationsonuneventerrain. groundinstrumentedtreadmillwiththesamesubjectrunningonthe The decrease in ankle work seen during running on uneven regulartreadmillonsupportswithabarebelt.Averagepeakvertical terrain compared with even ground is likely due to the high load and anterior–posterior ground reaction forces, as well as average sensitivity of the ankle joint. Muscles at the distal joints rely on peak ankle moments, were within 4% of each other and highly high-gain proprioceptive feedback and are often the first to correlated(i.e.R>0.997).Meancenterofpressuretrajectoriesonthe encounter perturbations due to uneven terrain (Daley and regular treadmill were also within 6% of mean center of pressure Biewener, 2006). In contrast, the more proximal knee and hip trajectoriesrecordedontheinstrumentedtreadmill.Fortheuneven y joints are largely feed-forward controlled. This control strategy surface, the terrain attached to the supported treadmill likely g o improves runningstability by maintaining consistent limb cycling introduced additional variability to calculations of the center of l o buthasamorepronouncedeffectonthedistaljoints(Daleyetal., pressure, because foot orientation during ground contact is highly i B 2007).Inaddition,wesawasmallreductionintheanklerangeof variable on uneven terrain. However, this error would have been l a motion,whichcouldhavealsoledtoareductioninjointwork.This multidirectional and likely did not affect the mean results of the t n reductioninanklemotionlikelystabilizedthejointinresponseto inverse dynamics calculations. Instead, the main effect on the e theunpredictablerunningsurface.However,itcouldalsohaveled inversedynamicscalculationswouldhavebeenincreasedvariability m toareductioninenergystorageandreturnintheAchillestendon, in parametersthroughout the stance phase. Examination of s.d. in ri e leading to reduced work at the ankle joint. Recently, a numberof theankleprofilesinFig.3showsslightlygreatervariabilityinthe p research groups have demonstrated that ultrasound imaging can anklemomentcalculationsbutincreasedvariabilityisalsopresent x E track both muscle fiber and tendon displacements during human in the ankle angle data. The ankle angle data are independent of f o running. Future experiments using ultrasound imagining could centerofpressurecalculations,sosimilarchangesinvariabilityseen provide greater insight into the muscle–tendon mechanics on inotherparameterssuggestthattheeffectofthecenterofpressure al n uneventerrain. variabilityfromtheuneventerrainsurfacewasnotlarge. r u Inconjunctionwithourhypotheses,subjectsexhibitedgreaterleg Anotherlimitationofthestudywasthatsubjectsranatonlyone o stiffness when running on uneven terrain compared with even prescribed speed. They could not negotiate the terrain by altering J e terrain. Therewerechanges in muscle co-activation but they were their speed as is possible when running on natural surfaces. We h small in magnitude and were likely not the major drivers of leg choseaslowrunningspeedtomaximizeoursubjects’comfortlevel T 716 RESEARCHARTICLE TheJournalofExperimentalBiology(2015)218,711-719doi:10.1242/jeb.106518 anddidnottestarangeofspeeds.Running atfasterspeedscould fabric.Theothersideofthehook-and-loopfabricwasgluedontowooden have resulted in more pronounced biomechanical differences. We blockswithawidthof2.55cmandlengthof15.2cm,andofthreevarying also tested only one pattern of stepping areas and one range of heights(1.27,2.54and3.81cm).Then,weattachedtheblockstothebelt, surfaceheightsfortheuneventerrainsurface.However,assubjects oriented lengthwise across the belt. As a result, the blocks could curve around the treadmill rollers, because of their relatively short width. The didnotappeartogetaccustomedtothesurface,wedonotbelieve blocks comprised 15.2×15.2cm stepping areas (after Voloshina et al., the inherent pattern of the uneven terrain affected gait dynamics. 2013),inapatternthatwasdifficultforsubjectstoadopt.Wethenplacedthe Largersurfaceheightvariabilitywouldhavelikelycausedamplified unevensurfacebeltontopoftheregulartreadmillbeltandconnectedthe biomechanicalandenergeticeffects. ends of the second belt using zip-ties to form one continuous surface. Additionallimitationsrelatetosubjecttrainingandtheinherent Subjects also ran on a separate, custom-built in-ground instrumented difference between treadmill and overground running. For one, treadmill (Collins et al., 2009). The even surface served as the control subjectswerealsonotallowedmultipledaystotrainandadjusttothe condition and allowed us to determine the biomechanical effects of the terrain.Itmaybehelpfulinfuturestudiestodeterminewhetherthere unevensurfaceongaitbiomechanicsandenergetics. are long-term adaptation effects. In addition, subjects ran with a Forbothsurfaces,subjectsranataspeedof2.3ms−1andwiththetrial limitedvisibilityoftheterrainbecauseofthelengthofthetreadmill. orderrandomizedforeveryparticipant.Subjectsparticipatedinjustonetrial foreachcondition,witheachtriallasting10minandwithaminimumof Allsubjectswerecomfortablerunningonthetreadmillanddidnot 5minrestallowedbetweentrials.Onbothsurfaces,subjectswereinstructed appear to be affected by limited visibility. However, it is possible to run normally and not look down at their feet unless they felt it was thatsubjectsmaynegotiatetheterraindifferentlyifmorevisibility necessary.Generally,subjectschosenottolookattheirfeetduringrunning. were allowed. For overground locomotion, runners typically have Aftertherunningtrialswerecompleted,subjectswalkedat1.0ms−1foran extended visual feedback on the terrain and may choose different additional10minoneachsurface,whilewecollectedmetabolicdatatouse pathsandfootplacementsinresponsetoterrainproperties. as a comparison with our previous study on walking on uneven terrain In summary, we found that changes in mechanical work can (Voloshinaetal.,2013).Subjectsworerunningshoesoftheirchoiceforthe explain approximately half of the energetic cost increase when experiments. running on uneven terrain surfaces compared with flat, smooth Metabolicrate surfaces.Theotherhalfoftheenergeticcostincreasemayberelated Wemeasuredtherateofoxygenconsumption(V̇ )forallrunningtrials to less efficient energy storage and return in elastic tendons and O2 using an open-circuit respirometry system (CareFusion Oxycon Mobile, ligaments. Future studies using ultrasound imaging could provide Hoechberg,Germany).Werecordedrespirometrydataforall10minofthe greater insight into muscle fiber and tendon dynamics on various runningandwalkingtrialsandalsofor7minduringquietstandingpriorto terrains. We did find thathuman runners did not vary mechanical each datacollection. We allowed subjectsthe first 7.5min of the trial to work done at their knee and hip joints when running on uneven reachsteady-stateenergyexpenditureandonlyusedthelast2.5minofdata terraincomparedwithsmoothterrain.Instead,subjectsreducedlimb tocalculatethemetabolicenergyexpenditurerateofeachsubject.Tofind mechanicalworkdoneattheanklejointwhenrunningontheuneven the metabolic rate, Ė (W), we used standard empirical equations as met surface. Using a similar control approach for legged robots with describedelsewhere(Brockway,1987;Weir,1949).Thenetmetabolicrate biomimeticlimbarchitecturesmighthavebenefitsinincreasingthe wasfoundbysubtractingthestandingmetabolicpowerfromthemetabolic power of all running conditions. All net metabolic power data were relativestabilityofrunningasitaltersthelimbbiomechanicsclosest tothefoot–groundinterface(Daleyetal.,2007). normalizedbysubjectbodymass(kg). Kineticsandkinematics MATERIALSANDMETHODS For both even and uneven conditions, we recorded the positions of 31 Wemodifiedaregularexercisetreadmillbyattachinganadditionalbeltwith reflectivemarkersusinga10-cameramotioncapturesystem(framerate: wooden blocks of varying heights to the original treadmill surface. The 100Hz;Vicon,Oxford,UK).Weplacedmarkersonthepelvisandlower blocks simulated an uneven surface on which subjects could run limbsasdescribedpreviously(Voloshinaetal.,2013)andtapedthemon continuously while we collected biomechanical and metabolic data. totheskinorspandexshortswornbythesubjects.Althoughtrialslasted Subjectsalsoranonaseparate,smoothtreadmillsurface,resultingintwo for 10min, the first 7.5min allowed subjects to reach steady-state testing conditions termed ‘uneven’ and ‘even’. For both surfaces, the dynamics and we only used the last 2.5min of data to calculate step runningspeedwasmaintainedat2.3ms−1,whilewecollectedkinematic, parameters such as step width, length and height. For each subject and kinetic,metabolicandEMGdata. y trial,the2.5minofdataanalyzedconsistedofaminimumof250stepsand g upto400steps.Toreducemotionartifact,welow-passfilteredallmarker o l Subjects dataat6Hz(fourth-orderButterworthfilter,zero-lag).Wedefinedstep o Twelve young, healthy subjects participated in the study (seven males, width,lengthandheightasthedistancebetweenthelateral,fore–aftand Bi fivefemales;mean±s.d.:age24.3±4.0years,mass68.6±7.1kgandheight verticaldistancesbetweenthecalcaneousmarkersonthetwofeetattheir al 175.5±7.1cm).Subjectsranontheevenandunevensurfacesduringthe respectiveheel-strikeinstances.Stepheightmeasurementswereusedonly t n same datacollection. For running on both surfaces,we collected oxygen to determine changes in step height variability caused by the uneven e consumption (N=11), step parameter (N=12), EMG (N=10) and joint surface. We calculated the effective leg angle as the angle relative to m kinematicsandkineticsdata(N=11).Becauseoftechnicalissues,somedata horizontalmadebythestraight-linedistancefromthegreatertrochanter ri werenotcollectedforparticularsubjects,resultinginavalueofNlessthan markertothecalcaneousmarkerofthestancefoot.Theeffectivelegangle pe 12insomedatasubsets. andthepositionofthecalcaneousmarkersactedasameanstodetermine x Priortotheexperiment,allsubjectsprovidedwritteninformedconsent. the time of heel-strike. This method of determining heel contact agreed E Experimental procedures were approved by the University of Michigan wellwiththeonsetoftheverticalgroundreactionforce.Inaddition,we of HealthSciencesInstitutionalReviewBoard. normalizedallmeasurementstosubjectleglengthmeasuredpriortoeach l a data collection and defined as the mean distance between the greater n Runningsurfacesandtrialprocedures trochanterandcalcaneousmarkersofbothlegs. ur Wecreatedanunevensurfacetreadmillbelt(Fig.1)thatweattachedtothe We recorded ground reaction forces using a custom-built in-ground o J regulartreadmillbeltofamodifiedexercisetreadmill(JASFitnessSystems, instrumentedtreadmill(Collinsetal.,2009)fortheevenconditionandtwo e TrackmasterTMX22,Dallas,TX,USA).Tocreatetheunevensurfacebelt, in-ground force platforms for the uneven condition. For the uneven h we sewed one side of the hook-and-loop fabric on to thick, non-stretch condition,weplacedthetreadmillontopoftwosupports,eachofwhich T 717 RESEARCHARTICLE TheJournalofExperimentalBiology(2015)218,711-719doi:10.1242/jeb.106518 restedsolelyonanin-groundforceplatform(samplerate:1000Hz;AMTI, integralsovertheentirestrideandin1%increments,todeterminewherein Watertown,MA,USA).Toobtaintotalgroundreactionforces,weaddedthe the stride cycle mutual contraction occurred. The purpose of calculating recorded forces from each of the force plates. For the even condition, mutualcontractionwasnottodeterminetheamountofco-activationrelative subjects ran on one belt of the split-belt instrumented treadmill and we towhateachmusclepaircouldhavedoneduringrunning,buttotestfor recordedonlyonesetofforces(samplerate:1000Hz).Forceplatformswere differencesinco-activationstrategiesbetweenthetwosurfaces. re-zeroedpriortoeachtrial.Forcedatausedtodeterminethetimeofheel contactandtocalculatetheaverageverticalgroundreactionforcesforeach Legstiffness subjectwerelow-passfilteredat25Hz(fourth-orderButterworthfilter,zero Inordertocomparethesensitivityofourresults,wecalculatedlegstiffness lag). However, forces synced to kinematic data and used for inverse valuesusingtwomethods.First,wereducedsubjectdynamicstothatofa dynamicsanalysiswerelow-passfilteredat6Hz(fourth-orderButterworth spring-massmodel(McMahonandCheng,1990)anddefinedlegstiffness filter,zerolag)becauseofthehighnoisesensitivityoftheinversedynamics tobetheratiobetweentheverticalgroundreactionforceandthechangein calculations.WeusedVisual-3D(C-Motion,Germantown,MD,USA)to effectiveleglength: conductinversedynamicsanalysisandtodeterminejointangles,moments F and powers in the sagittal plane for the stance limb. For both running k ¼ max ; ð2Þ conditions,wedeterminedanypositionoffsetoftheforcevectorrelativeto max DL max therunningsurfaceandcorrectedforitslocationinVisual-3D.Fortheeven wheretheeffectiveleglengthwasthestraight-linedistancefromthegreater condition,thiscorrectionwasminimal.However,fortheunevencondition, trochanter marker to the fifth metatarsal marker of the stance foot, the ground reaction force was measured across two force plates located normalized to subject leg length. We defined ΔL asthe difference in leg substantiallybelowthesurfaceofthetreadmill.Tocompensateforthis,we lengthatheel-strikeandanyotherpointduringstance,suchthatmaximum transformedthemeasuredforcesandtorquesattheforceplatformsintoa leglengthdeflection,ΔL ,occurrednearmid-stancewhenleglengthwas commonreferenceframewithanoriginattheheightofthetreadmillsurface, max shortest. In addition, we defined F as the maximum vertical ground and added them together. This introduced a small error into the inverse max reactionforceaftertheimpactforce.Wethencalculatedlegstiffness,k , dynamicscalculations,astheactualgroundreactionforcewasappliedonthe max foreachstrideastheratiobetweenthepeakverticalgroundreactionforce terrain,whichwasupto2.54cmhigherthanthesurfaceofthetreadmill.We andthemaximumleglengthdeflection(GüntherandBlickhan,2002). estimatethecenterofpressureerrorintroducedbythissimplificationtobe Weusedanalternativemethodforcalculatinglegstiffnessasameansto lessthan1.5cmbasedonprojectingaforcefromthehighestpointonthe ensure that methodology did not alter the conclusions of the study. We terraintothesurfaceofthetreadmill.Meansubjectforceswerenormalized computedthesecondlegstiffness,k ,byfindingalinearfittothecurve tosubjectweightandthenaveragedoversubjects. fit producedbyplottingeffectiveleglengthagainsttheverticalgroundreaction forceoverastride.Theslopeofthislinearfitdefinedtheapproximateleg Electromyography stiffness(GüntherandBlickhan,2002).Forbothcalculations,wefoundleg For all trials, we recorded and processed EMG signals as previously stiffnessateachstepforeverysubjectandthenaveragedthestridestofind described(Voloshinaetal.,2013).Bipolarsurfaceelectrodes(samplerate: subject means for both running conditions. The mean inter-subject leg 1000Hz;Biometrics,Ladysmith,VA,USA)wereplacedoverthebellyof stiffness for each running surface was the average leg stiffness across fourlowerlegandfourthighmuscles.Inparticular,werecordedEMGdata subjects. fromthetibialis anterior(TA),soleus(SO),medialgastrocnemius(MG), lateral gastrocnemius (LG), rectus femoris (RF), vastus medialis (VM), Dataandstatisticalanalyses vastuslateralis(VL)andthesemitendinosusofthemedialhamstring(MH) Wedefinedvariabilityforstepparameters,jointparameters(consistingof muscles of the right leg only. The surface electrodes had a diameter of jointangles,torquesandpowers)andEMGdataastheaverages.d.ofeach 1.0cm, an inter-electrode distance of 2.0cm, and an EMG amplifier bandwidth of 20–460Hz. Only the last 2.5min of data were used for parameteracrosssubjects,perrunningtrial.Forexample,forstepparameter data, variability was calculated by averaging the s.d. of consecutive step analysis. EMG data were first high-pass filtered at 20Hz (fourth-order distancesorperiodsovertimeforeachsubject,acrosssubjects.Similarly, Butterworthfilter,zerolag)andthenfull-waverectified.Foreachsubject, jointparameterandEMGvariabilitywerefoundbyaveragingthes.d.ofthe wethenaveragedthedataoverstepstocreateEMGmeansforeachmuscle parameter at each time point, per condition, across subjects. We then and normalized these means to the maximum mean value for the two reportedthemeanvariability(andthes.d.ofthevariabilityoversubjects)for runningconditionstominimizeinter-subjectvariability(YangandWinter, eachcondition.Weusedrepeated-measuresANOVAtoassessdifferences 1984). These signals were then averaged over subjects to create betweenconditions.Thesignificancelevel,α,wassetat0.05,andposthoc representativeEMGprofiles.Wealsofoundthes.d.oftheEMGsignalat Holm–Sidakmultiplecomparisontestswereconductedwhereappropriate. each time point, for each subject. These s.d. were also averaged over y subjects,tocreatemeans.d.envelopesforeachrunningcondition.Although g Acknowledgements o variabilityinmuscleactivitycannotdirectlyberelatedtochangesinenergy expenditure,itcandemonstratetheamountofperturbationexperienceddue TheauthorsthankDrJohnRebulaforhelpfuldiscussionsandassistancewithdata ol analysis,aswellasBryanSchlinkandmembersoftheHumanNeuromechanics i touneventerrain.Inaddition,wequantifiedchangesinmuscleactivationby B Laboratoryforassistanceincollectingandprocessingthedata. averaging, over the stride time, the normalized subject EMG profiles for al eachsubjectandcondition.Thesesubjectaveragevalueswerethenaveraged Competinginterests nt oversubjectstoproduceonemeanvalue,foreachmuscleandcondition, Theauthorsdeclarenocompetingorfinancialinterests. e m indicativeofmuscleactivity.WealsousedthemeansubjectEMGprofiles to calculate muscle mutual contraction (MC), or ‘wasted’ contraction as Authorcontributions ri e defined by Thoroughman and Shadmehr (1999), for three pairs of A.S.V.andD.P.F.developedtheconceptsanddesignoftheexperiments, p antagonisticmuscles(SO/TA,MH/VMandMH/VL): interpretedtheresultsandpreparedandrevisedthearticle.A.S.V.executedthe x E experimentsandperformeddataanalysis. ð f o MC¼ minðf1;f2Þdt; ð1Þ Funding l a ThisresearchwassupportedbygrantsfromtheArmyResearchLaboratory n such that f1 and f2 are the mean EMG profiles of the two antagonistic [MWic9h1ig1NanF-R0a9c-1k-h0a1m39GtroaDdu.Pa.tFe.,SWtu9d1en1tNFFe-l1lo0w-2s-h0ip02to2tAo.SD..VP..F.]andtheUniversityof ur musclesandmin(f ,f )istheminimumofthetwoprofilesateachtimepoint o 1 2 J (Voloshinaetal.,2013).Inotherwords,whenmeanEMGprofilesfromtwo References e musclesdonotoverlap,wecanexpectzeromutualcontraction,whereasany Alexander,R.M.(1992).Amodelofbipedallocomotiononcompliantlegs.Philos. h overlapwouldproduceanon-zero,sharedactivitylevel.Wecomputedthe Trans.R.Soc.Lond.BBiol.Sci.338,189-198. 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1 Biomechanics and energetics of running on uneven terrain 2 Alexandra S. Voloshina and Daniel ...

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