J Anim Physiol Anim Nutr. 2017;1–10. wileyonlinelibrary.com/journal/jpn  | 1© 2017 Blackwell Verlag GmbH

Received:14February2017  |  Accepted:11October2017DOI:10.1111/jpn.12840

O R I G I N A L A R T I C L E

The biomechanical construction of the horse`s body and activity patterns of three important muscles of the trunk in the walk, trot and canter

K. Kienapfel1  | H. Preuschoft2 | A. Wulf3 | H. Wagner3

1DepartmentofAnimalEcology,EvolutionandBiodiversity,RuhrUniversityBochum,Bochum,Germany2AnatomicalInstitute,RuhrUniversityBochum,Bochum,Germany3InstituteofSportandExerciseScience,UniversityofMünster,Münster,Germany

CorrespondenceK.Kienapfel,DepartmentofAnimalEcology,EvolutionandBiodiversity,RuhrUniversityBochum,Bochum,Germany.Email:Kathrin.Kienapfel@rub.de

SummaryTheactivitypatternsoftrunkmusclesarecommonlyneglected,inspiteoftheirimpor-tance formaintainingbodyshape.Analysisof thebiomechanicsof thetrunkunderstaticconditionshasledtopredictionsoftheactivitypatterns.Thesehypothesesaretested experimentally by surface electromyography (EMG). Five horses, with andwithoutarider,wereexaminedinthewalk,trotandcanter.FootfallwassynchronisedwithEMGbyanaccelerometer.Averagesoftenconsecutivecycleswerecalculatedandcomparedbystatisticalmethods.Thestartandstoptimesofthemuscleactivitiesof5–10undisturbedEMGplotsweredeterminedandtheaveragesandstandardde-viationscalculated.Inwalking,muscleactivitiesareminor.Electromyography(EMG)activitywasincreasedinthem.rectusduringthethree-limbsupport.Whenthebend-ingmomentsassumetheirgreatestvalues,forexamplewhilethehorses’massisac-celeratedupward(twotimesearthacceleration)inthediagonalsupportphasesintrotandcanterthem.rectus,connectingthesternumwiththepubicboneismostactive.Them. obl. externus ismost activewhen the torsional and bendingmoments aregreatestduringthesamesupportphases,butnotbilaterally,becausetheforcesex-ertedononesidebythe(recorded)m.obl.externusaretransmittedontheothersidebythe(notrecorded)m.obl.internus.Whilethehindlegstouchthegroundinthetrotandcanter, ground reaction forces tend to flex thehip joint and the lumbar spine.Therefore,thevertebralcolumnneedstobestabilisedbytheipsilateralm.longissimusdorsi,whichinfactcanbeobserved.Asawhole,ourEMGdataconfirmexactlywhathasbeenpredictedbytheoreticalanalysis.

K E Y W O R D S

bowandstringtheory,dressage,electromyography,finiteelements

1  | INTRODUCTION

Theconstructionofthebodystem(thatishead,neck,trunkandtail)inquadrupedalanimalscanbeexplainedwithatheoreticalconsider-ation.Thiscanbecalledthe“beam-theory,”whichhasbeendevelopedfromtheolderandcommonlyknown“bow-stringtheory.”Inspiteofbeingmorepopular,thelatterexplainsnotmorethanthetrunkalone.The beam theory has been developed on the basis of mechanical

theory (Kummer,1959;Preuschoft,1976;Preuschoft&Fritz,1977;Preuschoft, Witzel, Hohn, Schulte, & Distler, 2007; Slijper, 1946).Althoughthetheoreticalapproach iswell-established inengineeringsciencesandsinceseveralyearsconfirmedbyFiniteElementSystemsAnalysis (Witzel,Mannhardt,Goessling, deMichaelis,&Preuschoft,2011),ithasnotbeentestedexperimentally.Becausethebeamthe-ory implies predictions concerningmuscle activities, an experimen-tal approach is possible by means of the electromyography (EMG)

2  |     KIENAPFEL Et AL.

method,whichallowscontrollingoftheactivityofmusclesinrealtime.Unfortunately,theexertedforcecannotbedetermined.Accordingtoseveral authors (Konrad, 2011; Larson, 1995; Stern,Wells, Vangor,&Fleagle,1977), itcanbeexpectedthatmuscleactivitiesaremostpronounced while muscles exert most force, that means: duringlocomotion.

Inthecaseoftrunkmuscles,thenecessaryexcursionsareminimalduringstanding,sothatnecessaryforcesmaybeexertedbyconnec-tivetissue,suchas ligaments (headandneck), strongfasciae (abdo-men)oraponeuroses(lumbarregion).These(“passive”)structuresmaywellberesponsibleforthemaintenanceofbodyposture,particularlyatrestunderstaticconditions,whentension-resistantstructuresmustnotchangetheirlengths.Duringlocomotion,however,muscleshavetoassumedifferentlengthsbyactivecontractions,whichexistsonlyforshortperiodsoftime,alternatingwithshortperiodsoflesseractiv-ityinamotioncycle.ThiscanbedocumentedbyEMGthatiswhyweputmostemphasisongaits,ratherthanstatics.

Thebodystemofaquadrupedcanbecomparedtoaheavybeamontwosupports.Thisbeamisexposedtoshearingforcesandbendingstressesunderitsownweight.AsillustratedbyPreuschoftandFritz(1977),theanteriorcantilever(=headandneck)isbentdownward,soproducingcompressionatitslowermarginandtensionontheupper.Betweenthesupports, the trunk tends tosagventrallydownwards,sothatcompressingforcesoccuralongtheuppermarginandtensionatthelower.Thisdistributionofinternalforcesisinagreementwiththearrangementofthecompression-resistantskeleton(vertebralcol-umnandsternum,pelvis,(Preuschoft&Fritz,1977))andthetension-producing musculature (neck, cranial thoracic dorsal musculatureandseveralshouldermuscles,asdetailedinKienapfel(2014)).Asidefromthemuscles,thereexistverystrongstrandsofconnectivetissue,whichcantakeoveratleastpartofthetensileforces,andareclaimedbyseveralresearchers(Gellman&Bertram,2002;Nickel,Schummer,Seiferle,&Frewein,2004;Slijper,1946;Zschokke,1892)todoso.

During locomotion, maintaining body shape becomes more de-mandingthanatrest,becausethemassofthebodyisacceleratedup-wards.AccordingtoPreuschoft(1985)andWitte,Lesch,Preuschoft,andLoitsch (1995a,b), theaccelerations in thegaits trot andcantercommonly are two times earth acceleration. This means that theweightforce,whichmustbecountered, is twiceasmuchasat rest.Inaddition,thebodyissupportedonallfour,three,twoextremitiesorevenonelimbalone.Thereoccurevenphaseswithoutanygroundcontact,whilethebodyisfloatingfreely.Becauseofthesephasesofaerialfloating,thereactionforcesbetweengroundandthebodyvaryconsiderably.Inthetake-offphaseforajump,horsesproduceaccel-erationsof2.5g, during landing after a jump3.7g (as calculated in(Preuschoft&Fritz,1977)).Insmallermammals,especiallyadaptedtoleaping, theaccelerationsmaywell reachmore than10 timesearthacceleration(Demes&Gunther,1989;Gunther,Ishida,Kumakura,&Nakano,1991).

Theoccurringshearingforcesreachtheirmaximumattheshoulderanddeclinetowardsthehindlimbsupport,changingtheirsignataboutthoracal/lumbarregion.Shearingforcesareinafirmmathematicalre-lationshiptobendingmoments.Astructure,wellsuitedforsustaining

shearing forcesaretheribsplus the intercostalmuscles (Preuschoftetal.,2007).

Assoonasonlyonelimbisliftedfromtheground(forexampletoplaceitforwardandsoinitiatelocomotion),torsionalmomentsoccurinside the trunk (that is that part of thebody stembetweenante-rior andposterior limbs (Preuschoftetal., 2007;Preuschoft,Hohn,Distler,Witzel,&Sick,2005)).Tosustaintorsionalmomentsinsidethetrunk,thereexistwell-suitedstructures:ribsforcompressiveforcesandtheobliquemusclesofthebodywall(Mm.obliquusexternusandinternus,intercostales)fortensileforces.Torsionalmomentsconcen-trate near the periphery of the twisted part and therefore the pe-ripheralarrangementoftheribsaswellasoftheobliquemusclesfitsperfectlytothetheoreticalexpectations.Aclose-up(stilltheoretical)analysisofthesestructuresshowsexactagreementbetweentheoret-icaldemandsandmorphologyinvariousanimals(Hohn,Preuschoft,Witzel,&Distler,2013;Preuschoft&Klein,2013;Preuschoftetal.,2005,2007).

Weconcentratedoureffortsonhorses,whicharetypicalcursorialmammals.ThelocomotormodesandEMGactivitiesoftheseanimalsareknownindetail.Theyareusedtobeinghandledbyhumansandsocaneasilybeinducedtoperformallnecessaryactionsforastudy.Theirgaitsarerhythmic,thecyclesreliablyuniformandnotinfluencedordisturbedinnormalconditionsbyhumans,thatisridersorresearch-ers (commonexperienceamongriders;ownresults)and inaddition,horsesareavailableinnumberssufficientforprovingtherelevanceoftheexperiments.Theyarewellsuitedtoserveasmodelstostandforall cursorialmammals.Becausewewantedtoexamine thegaitpat-terns inpracticalriding,thehorseswereexaminedontrackandnotonatreadmill.

Thepatternsofmuscleactivityhavebeenstudiedrepeatedly. Inmostcases, the interestof theauthorswasfixedonmusclesof thelimbs.Thishasresultedinafairlycompleteoverviewofmuscleactionsduring several performancesof avarietyofvertebrates.Rare, how-ever,arestudiesdesignedtoobtainingempiricalprovestoverifythebalanceofforcesinsidethemoreorlesshorizontallyorientatedbodystem(Carrier,1990,1993;Ritter,1996;Ritter,Nassar,Fife,&Carrier,2001;Schilling&Carrier,2009).

Theknowledgeoftheregularmuscleactivitypatternsofthetrunkevidentlypromisesanunderstandingofthebiomechanicalconstruc-tionofaquadrupedalanimal`sbody.Italsowillgiveusefulanswerstoquestionsconcerningtrainingtechniques,ortoidentifypain.

Muscles lyingnearthesurfacesothattheyprovidetherequiredinformationarethem.longissimusdorsiasmostobviousmuscleofthetopline,them.rectusabdominisasstraightmuscleofthebellyandthem.obliquusexternusasdiagonalabdominalmuscle.

Theactivityofthem.longissimusdorsiisknowninthewalkandtrot(Cottriall,Ritruechai,&Wakeling,2009;Licka,2001;Licka,Frey,&Peham,2009;Robert,Audigie,Valette,Pourcelot,&Denoix,2001;Robert,Valette,&Denoix,2000;vonScheven,2010).Justonestudymentionsonepeakactivityinthecanter(Robertetal.,2000),butnofurtherinformationwasprovided.

Them.rectusabdominiswasmentionedinthesamestudyinthecanterwithonepeakactivity,butagainwithnofurther information

     |  3KIENAPFEL Et AL.

aboutthestageofmovement.Inthewalkandtrot,itsactivityisdoc-umentedbythestudiesofseveralauthors(Robert,Valette,&Denoix,2001;Robertetal.,2000;Zsoldos,Kotschwar,Rodriguez,Peham,&Licka,2010).Them.obliquusexternuswasalsopartofthelatterstudyandinvestigatedinthewalkandthetrot.

Inaheavybeam,whichissupportedlikebodystemofhorseonan-teriorandposteriorlimbs,wecanexpecttensileforces—thatismuscleactivity—alongtheventralsideofthebellyaswellasalongthedorsalsideoftheanteriorthoraxandproximalneck.The latterhas indeedbeenfoundinanearlierstudy(Kienapfel,2014).Ifthesamebeamissupportednearitsrear(caudal)endbyaforwardlyinclinedleg,withground contact underneath its belly, tensile forceswill occur at theposteriorbackandrearmarginofthebeam.Theforceswilloccuronlyforshortperiodsoftimeineachmotioncycle.Ifweimaginethebeamonstiltsreplacedbyahorse′sbody,aforwardlyplacedhindlimbneedsto be balanced in the hip joint bymuscles. Some of thesemuscles(hamstrings,ischiofemoralpartofm.gluteus)pulltheischiumdown-wardsandsoleadtoanupwardmovementoftheiliosacral junctionplusposterior lumbarvertebrae. Sucha flexionmustbeblocked, atleastcontrolled,bymuscles:mm.gluteusmedius,iliocostalisandlon-gissimus.Diagonalsupportofthe“beam”onafrontlimbanditscontra-lateralhindlimbleadstoatwistingofthe“beam”—ortrunk—betweenthesupportinglimbs.Twistingimpliestensileforcesbetweenthesup-portingdiagonallimbs,whichcanbeproducedbytheobliquemusclesofthetrunkwall.

Therefore, the correctness and reliability of our theoretical ap-proach would be confirmed if three hypotheses turn out to becorrect:

(i) Thestraightventralmusclesofthetrunkhavetobeactivatedinthephasesofsupport,whenthegreatestforcesareactingdownwards

(ii) Thedorsal/epaxialmusclesofthetrunk(m.longissimusdorsi)areactivatedduringthestancephaseoftheipsilateralhindleg.

(iii)Torsional stresses lead toanactivationof theobliqueabdominalmusclesinthephasesofdiagonalsupport.Moreprecisely,them.obliquusabdominisexternus(whichalonecanbecontrolledbysur-faceelectrodes)ofonesideshouldbeactiveduringsupportontheipsilateralfore-andcontralateralhindlimb.

2  | MATERIALS AND METHODS

2.1 | Ethics statement

Thistypeofnon-invasiveresearchisapprovedundertheGermanani-malprotectionactanddoesnotrequireastudy-specificpermission.Thehorseswerehandledbytheirusualriderswithoutaddingstress-orsorpaintotheanimals.

2.2 | Methods

Themeasurementsweretakenfromfivewarmbloodgeldingswithoutbackpainor lameness according to theirprofessional trainers.Theirheightatwithersvariedbetween1.68and1.74mandtheirageswere

between9and16years.Thehorseswereusedfortrainingofridersonbasictoadvancedlevels.

ThemeasurementsweredoneinaLongehall(diameter20m).Formeasuringmuscleactivation,bipolarself-adhesiveelectrodes

were fixed on the shaved and cleaned skin.Two bipolar electrodes(2,000Hz)werepositioned3cmapart in thedirectionofmuscle fi-breson themusclebellies.Them.obliquusexternuswasmeasuredbilaterallyatthe levelofthe16thrib.Electrodesonthem. longissi-musdorsiwereplacedasfarcranialaspossibleonthesaddledhorsewiththesaddlenottouchingtheelectrodes.ThiswasapproximatelyontopofL3–L4.Thereferenceelectrodewasplacedonthehighestpointof thepelvis,which is not coveredbymusculature.TheEMGsignalswerefilteredwithaButterworthfourth-orderhighpass(40Hz)andthenrectified.Thereafter,thedataweresmoothenedbymovingaverageprocedure(window40datapoints)foreachhorseandcondi-tion.Movementsweresynchronisedbyrecordingaccelerationsalongtheleftforeleg.Theaccelerometerwasfixedtothemetacarpalbyabandage. The locomotor cycles were identified in close analogy to(Falaturi,2001)usingthemaximumpeaksoftheaccelerometerdataastriggers.

Werecorded1–3cyclesineachgaitintheLongehallandcollecteddatafortenormoreclearrhythmicstridesinarowinthedesiredposi-tion.First,theprogramwasperformedunderariderandthenwithout.Thetenconsecutivecycleswerechosenforeachrunonthebasisofthevideotapes.Selectionwasbasedoncorrectrhythm,maintenanceof constant speed and relaxed head-neck position. Averages werecalculatedseparatelyperhorseandexperimentalrun.

For the searching of divergences between themuscles on bothsides,with andwithout a rider and on both sides, statistical analy-seswereperformed.Theon- andoff-timesof themuscle activitiesweredeterminedandmeanvaluesandstandardvariationscalculated.Because no clear on- and off-data of activity in the case of them.obliquus externus could be discerned, only themaximum activitieswereusedforthecalculationsofmeanvalueandstandardvariation.

2.3 | Statistical analyses

Toevaluatedifferencesbetweenthemusclesofbothsides,withandwithoutarider,andleftversusrightturns,thedataweretestedwiththeKolmogorov–SmirnovtestforaGaussiandistribution.Equalityofthevarianceswas testedby theLevene’s test. If therewerediffer-ences,theywerelocatedwiththeMann–Witney(independentdata,e.g.,comparisonbetweenbothsides,withandwithoutarider),ifthedatadidnotshowaGaussiandistribution.IfthedataweredistributedsymmetricallyaccordingtoGauss,theStudent’sttestwasperformed.Everytestwastakenfordependentvariables.Significancelevelwasconsideredtobeatp≤.05.

Forthegraphsoftheactivitypatterns,fivetypicalEMGplots(eachbeingthemeanvalueof10cycles)foreveryhorsewereoverlain,andforeachtimeunit,themedianlineshowingtheactivitywasdrawnbyhand.

Theaccelerometerplotwassynchronisedwiththefootfallpat-ternofPreuschoftandGünther(1994),thelengthofthestridecycle

4  |     KIENAPFEL Et AL.

wasthesame inbothfigures,sothat itcouldbeadaptedwithoutfurtherchanges.“Adapting”heremeansshiftingthedataalongthetimeaxisuntilthefootfallpatternsmatchedwiththeaccelerometerdata.

3  | RESULTS

Theactivitiesofallthreetrunkmusclesbecomesignificantlygreater(p<.01)fromwalkovertrottocanter—soincantertheactivitywasthegreatest.Nosignificantdifferencesoccurredbetween themus-clesoftheleftandtherightsideorbetweenmovingontheleftandrightrein.Inthewalk,themm.longissimusdorsiandrectusabdominis

show significantlymore activitywith a rider thanwithout (p<.05).Neitherinthetrotnorinthecantersuchdifferencescouldbefound.Inthefastergaitstrotandcanter,whichincludephasesofaerialsus-pension,andthereforehighergroundreactionforces,allEMGactivi-tiesaremoremarkedthaninthewalk(Figure1a,b).

Inwalking, them. obliquus externus is activewhile one of thefrontlimbsandthecontralateralhindlimbsupportthetrunk.

Them.longissimusdorsishowsnoclearactivitiesinthewalk.Them.rectusabdominisisactivetwotimesineachcycle,assoonasoneoftheforehoovesistouchingtheground.Itsactivityendsinalaterstageofthestancephaseoftheforehoof.Whiletheforehoofisincontactwiththegroundandthem.rectusabdominisisactive,bodyweightissupportedbythreelimbs,twoforeandonehind.

F IGURE  1  (a)Walk.Meanactivityphasesasgreensegmentsofthesolidcolumns.Thehorizontalaxisisdividedin%ofthecycleduration.Standarddeviations±SDareshownasnarrowbars.Atthetop,thefootfallisdisplayed.Onecycleinthewalkhadameandurationof1s.Them.longissimusdorsishowednomeasurableactivityduringthewalk. Forthem.obliquuusexternus,onlythemaximumpeaksareconsidered.(b)Walk.Ontop,thefootfallsequenceisdisplayed.Theboldlinesarethemedianelectromyography(EMG)signalsfromfivehorsesovertencyclesperhorse.Thethinlinerepresentstheaccelerometeratfrontleftmetapodium,beingidenticalinalldiagrams.IthasthesamelengthinallillustrationsandallowsconnectingtheEMGdatawithfootfallsequence.Obl.le/re:m.obliquusexternusleftandright,Lonle/re:m.longissimusleftandright,Rele/re:m.rectusabdominisleftandright.HR,hindright;HL,hindleft;FR,frontright;FL,frontleft

(a)

(b)

     |  5KIENAPFEL Et AL.

In the trot (Figure2a,b) the activity of them. obliquus externushas three to five peaks of activity throughout each cycle,with onehighandseveral lowerspikes.Themainpeakoftheleftm.obliquusexternusoccursduringthestancephaseofLFandRH.Therightm.obliquusexternushasitsmainpeakduringthediagonalstancephaseRFandLH.Thismuscleobviouslyisactiveatthestancephaseoftheipsilateralfore-andcontralateralhindlimb.

Themainactivityofthem.longissimusdorsitakesplacefromthemiddleoftheswingphaseuntilshortlyaftertouchdownoftheipsilat-eralhindlegwithanadditionallowpeakatliftoff.Them.rectusshows

twopeaksfromthebeginningtothemiddleofeachdiagonalstancephaseofbothfore-andthecontralateralhindhoof.

Inthecanter(Figures3a,b,4a,b),them.obliquusexternusoftheleadingsideshowsonehighpeakofactivityshortlyafterthetouch-downof the leading foreleg (forexample the left foreleg in the leftleadcanter)untilthemiddleofitsstancephase(includingthethree-legsupportof the leading front, the trailing frontand leadinghind).The contralateral obliquushas threepeaksof activity: a lowoneatgroundcontactofthetrailinghindleg, thebigpeak inthemiddleofthethree-legsupportphase(HL,HR,FLinrightleadandHR,HL,FR

F IGURE  2  (a)Trot.Meanactivitymarkedgreen,±SDbynarrowbars.Thehorizontalaxisisdividedin%ofthecycleduration.Ontop,thefootfallisdisplayed.Eachfullcycleintrothadameandurationof0.8s,orafrequencyofca.85/min,likeinPreuschoft(1987).Forthem.obliquusexternus,onlythehighestpeaksareshown.(b)Trot.Footfallontop.Eachcycleofthetrothadameandurationof1s.ConventionsasinFigure1.HR,hindright;HL,hindleft;FR,frontright;FL,frontleft

(a)

(b)

6  |     KIENAPFEL Et AL.

inleftlead)andanotherlowoneinthemiddleofthestancephaseoftheleadingforeleg.ThemaximumpeaksareshowninFigure3a.Them.longissimusdorsiisactiveshortlybeforetouchdownoftheipsilat-eralhindleguntilthemiddleofthestancephase,nomatterifitistheleadingortrailing.

Them.rectusabdominisisactiveonbothsidesshortlyaftertouch-downofthetrailinghindleguntiltheendofthediagonalstancephase.Them.obliquusexternusshowsmostactivityalwaysslightlyafterthepeakactivityofthem.rectusabdominisinthediagonalstancephaseofthetrotaswellasinthethree-legsupportinthecanter,whilemostweightissupportedbythediagonal.

4  | DISCUSSION

Tomakethemost importantpoint first,ourpresentstudyprovidesdataobtainedduringtruelocomotion.Acomparisonwiththelitera-ture, however, shows that thedifferencesbetweenour results andthoseobtainedfromthetreadmillareminor.MostEMGdata intheliterature(exceptRobert,Valette,Pourcelot,Audigie,&Denoix,2002)who recorded muscle activities in two horses under natural con-ditions)were not taken at track but on the treadmill. This artificialcondition,whichisnottheonetowhichhorsesareadaptedbyevolu-tion,providesdatawhichtheoreticallymaywelldivergefromnormal

F IGURE  3  (a)Canterleftlead.Meanactivityphasesaremarkedpink,±SD shownbynarrowbars.Thehorizontalaxisisdividedin%ofthecycleduration.Ontop,thefootfallsequenceisdisplayed.Onecycleinthecanterhadameandurationof0.6s.Forthem.obliquuus,onlythemaxi4mumpeaksaredisplayed.(b)Canterleftlead.Atthetop,thefootfallisdisplayed.Onestridecycleincanterhadameandurationof0.6s.ConventionsasinFigure1.HR,hindright;HL,hindleft;FR,frontright;FL,frontleft

(a)

(b)

     |  7KIENAPFEL Et AL.

conditions outside on the grounds or even in a riding hall. On thetreadmill,thehorsecannotmoveonits individuallypreferredspeedorstridelengths,hasnofeedbackbytheprogressitismakinginthechosengait,anddoesnotneedtobalancetheuneven,permanentlychangingconditionsofthesoilinovergroundlocomotion.Accordingtoown,unpublisheddata,groundreactionforcesmayvaryonroughgroundsby±40%oftheaveragevalues.Differencesbetweenthesetwo conditions occur especially in the lumbar regions of the back(Álvarez,Rhodin,Byström,Back,&Weeren,2009).Usingatreadmillhas advantages such as constant environment, speed and ground

conditions; therefore, experiments promise to better repeatability(Sloet vanOldruitenborgh-Oosterbaan&Clayton, 1999). The sameauthorsadmit,ontheotherhand,thattestingontrack,especiallywiththeaimtostudylocomotion,isclosertonaturalconditions.

AccordingtoMilner-BrownandStein (1975), itshouldbepossi-bletocreateanapproximatelylinearrelationshipbetweenEMGsignalandforceaslongastherecordingisconfinedtoonemuscleandtheelectrodesarenotmoved.Larson(Larson,1995)alsousedtwostagesofEMGactivityasbenchmarkformuscle force, lowandhighactiv-ity, following in thispointSternetal. (1977).Thepatternofmuscle

F IGURE  4  (a)Canterrightlead.Meanactivityphasesaremarkeddarkgrey,±SD indicatedbynarrowbars.Thehorizontalaxisisdividedin%ofthecycleduration.Ontop,thefootfallpatternisdisplayed.Eachcycleinthecanterhadameandurationof0.6s.Forthem.obliquus,onlythemaximumpeaksareshown.(b)Canterrightlead.Atthetop,thefootfallisdisplayed.Onecycleincanterhadameandurationof0.6s.ConventionsasinFigure1.HR,hindright;HL,hindleft;FR,frontright;FL,frontleft

(a)

(b)

8  |     KIENAPFEL Et AL.

activitiescanbeunderstoodbest,iftheirfittothemajorexchangeofforcesbetweenhorseandgroundistakenintoconsideration.

In the trot, groundcontact (and thatmeansapossibility toexertforces from thegroundon thehorse′sbody)exists aloneduring thephases of diagonal support. In the canter, the “diagonal” in fact rep-resentsaphaseofthree-leggedsupport,duringwhichfirsttheleadinghindlimb,secondthetrailinghindandcontralateralforelimb(diagonalstance)and third theother forelimbareon theground.According toPreuschoftandFritz(1977),thegreatestaccelerationsupwardcoincidewiththesupportonthediagonal limbs. Ifthehorse is inthesupportphaseoftrotandcanter,andmostoftheweightcarriedbythediago-nal,thebendingmomentsshouldreachtheirhighestvalues(Preuschoft,1987):Theweightsofallheavysegmentsbetweenthesupportinglimbs,thoraxandabdomen(togetherabout70%oftotalbodymass)aremov-ingdownwardsatexactlythistime(Preuschoft,1987).Wemustexpectthosemuscles,whichkeepthetrunkinbalanceagainstweight,tobehighlyactive.Thisisindeedthecase,them.rectusabdominisisalwaysactiveduringthediagonalstancephaseofthetrot,aswellasduringthestancephaseinthecanter,whichisdominatedbythe“diagonal.”

Theactivitiesofm.rectusabdominisare incompleteagreementwiththeliterature(Robert,Audigie,etal.,2001;Robert,Valette,etal.,2001;Robertetal.,2002;Zsoldosetal.,2010)withtwoactivitypeaksintrotandoneincanter,aswellasthetimingoftheactivityphases.

AsZsoldosetal. (2010)notedaswell, them.obliquusexternusshowsahighvariabilityinthewalkandinthetrot.Theauthorssup-posedthiscouldbeduetotheassumedrespiratoryfunction(Nickeletal.,2004). If the inconsistentactivity in the trotwould indeedbecausedbybreathing(Ainsworthetal.,1997;Bramble&Carrier,1983),itsactivityinthecanter(wherebreathingandlocomotionarecoupledaccordingtoBrambleandCarrier(1983)andAinsworthetal.(1997))shouldbemorepronouncedandsteadier.Asthisisnotthecase,an-otherreasonseemstoberesponsible.Theskinmusclem.cutaneoustrunci,forexample,wassuspectedbyNickeletal.(2004)toplayaroleinmotion.Asitsfibreshavethesamedirectionasthem.obliquusex-ternus,itcouldindeedinterferewiththeobliquussignal.Maybethereisalsosomecrosstalkfromthem.obliquusinternusandthem.rec-tusabdominis,whichmakesthesignalsovariable.Inspiteofalltheseproblems,themainactivityofthem.obliquusabdominisexternusco-incidesconsistentlywithsupportondiagonallimbs.

In fact, thediagonal support requires a tension-resistant tie be-tweenthestancelimbs.This isprovidedbytheobliquusinternusoftheipsilateralsideofthehindlimbandthem.obliquusexternusofthecontralateralside.Toavoidadislocationofthelineaalba,thetensileforceofthedeepobliquemustbepassedontothesuperficialobliqueofthecontralateralside.Oursuperficialelectrodesdidnotallowcon-trollingthem.obliquusinternusbutthem.obliquusexternusofthecontralateral sidewas in fact active. This is in full agreementwithDeban,Schilling,andCarrier(2012)ondogs.

Them.longissimusdorsihasamaximumactivitybeforeandwhilethe ipsilateralhindleg ison theground (thatmeans,whileweight isbornebythislimb)andalowerpeakatliftoffintrotbutnotincanter.

Carrying loadon theantevertedhindlimb requiresacontractionoftheverystrongextensorsofthehip joint,namelymm.gluteiand

the hamstrings. Following the theory, them. gluteus should be ac-tive(notstudiedinthispaper,butinRobert,Valette,Degueurced,&Denoix,1999)aswellasthem.longissimus,whichisindeedthecaseforbothmuscles(Robertetal.,1999).Thesemusclesnotonlyextendthehipjointtheyalsoliftthecranialpartofthepelvis,theilium.Tocompensate the resulting torqueat the iliosacral joint andbetweenthe lowermost lumbarsegments,acontractionofthedorsalmuscu-latureisrequired.Regardingthispoint,weareinfullagreementwiththeresultsobtainedbySchillingandCarrier(Schilling&Carrier,2009)ondogs.

Themostpowerful flexorof thehip jointused for initiating theforeswingofthehindlimbisthem.psoas,locatedventraltotheverte-bralbodiesofthelumbarsection.Itseemslogicalthatthiscontractionofthepsoasleadstoaflexionofthelumbarsegmentswhichmustbecounteractedby theextensor—them. longissimusdorsi.Thiswouldresultintheminorpeakofactivityobservedatliftoffoftheipsilateralhindlimb.Inthecanter,suchastabilisingcounteractionisnotneces-sary,becausebothhindlegsareswungforwardtogetherandthemostposterior segmentsof the trunkare flexedventrally (Loitsch,1993).This ventral flexion is followed by an extension (or dorsiflexion) ofthe trunk.Thatmovement seems to be induced by elastic recoil ofmusclesandtheirtendonsandhasbeeninterpretedbiomechanicallybyWitteetal.(1995a)asameanstoacceleratetheforeswingofthehindlimbs.Ifthehindlegistouchingthegroundandweightisshiftedonthis limb,thevertebralcolumnneedstobestabilisedagainsttheventralflexingmomentofthehamstringsandotherextensorsofthehipjoint.StudiesofLicka(2001),Lickaetal.(2009),Robert,Audigie,etal.(2001),Robertetal.(2000),vonScheven(2010);Cottrialletal.(2009)confirmthatinwalkandtrot,theactivityofthelongissimusisconnectedwiththeipsilateralhindleg.Licka(2001)reportedtwomax-imapercycleinthetrotlikewehaveobservedinmostcasesofourstudy,buttheydescribedtheactivitytooccurabitlaterinthemotioncyclethanwecanreport.

Former investigationshave shown that in thephaseof forelimbsupport,thedorsalneckmuscles(m.splenius,anteriorpartofm.tra-pezius)areactive(Kienapfel,2014).

Themostconflictingamongourresultsisthemissingofaclear-cutactivityofthem.longissimusdorsiinthewalk.Acontractionofthismuscleisevidentfrompalpationbehindthesaddlebytherider.Simpleobservationshowsthattheperceivedcontractionofthedorsalmusclecoincideswiththestancephaseoftheipsilateralhindlimb.Lickaetal.(2009)observedEMGactivitiesofthem.longissimusdorsiinthewalk,whichwedidnotfindatall.Thereasoncouldbethedivergentloca-tionoftheelectrodes.WeplacedtheelectrodesatthelevelofL2/L3becauseofthesaddle(whichisforriding),whereasLicka(2001)foundaloweractivityatthislevelincomparisonwithmorecranialregionsof them. longissimus dorsi.Our results of them. longissimus dorsiconcerningthepeaksofthetrotmatchwellwiththetimingobservedbyRobertetal.(2000)andCottrialletal.(2009).vonScheven(2010)reportedonetofourinconsistentactivityburstsofthismuscle.

Incanter,wefoundtheexpectedburstpercycleofthem.longissi-musandconstantactivitypatternsinallmeasuredhorses.Wakeling,Ritruechai,Dalton,andNankervis(2007)founddifferencesbetween

     |  9KIENAPFEL Et AL.

theleftandrightrein,withtheinnermusclesidegivinghigherEMGactivitiesthantheouterside.Wecouldnotdetectsuchdifferences,butthiscouldbeduetothebigcirclediameterof20m,wherethehorsesdonotneedtobendmarkedly,andbecausethiseffectwasdetectedinthemorecranialpartofthelongissimusdorsi.

Ifa rider ismountedonahorse,he isaddinghisweighton topof theweightof the segmentsbetween the supporting legs.This isreflected inmoremuscleactivity inwalkingwitha rider in compar-isonwithwalkingwithout.Ahorsewithnormalheighthasaweightof approximately 500kg, a rider plus saddle hardly less the 80kg.Inmore rapidmovements, up to two timesearthaccelerations (seeIntroduction)areleadingtoamultiplicationoftheweightforce,inthiscaseyielding1,000kg.Therefore,muchmoremuscleforceisneededinthetrottingandcanteringhorsewithouttheriderthaninthewalkevenwith.The difference betweenmuscle force requiredwith andwithout the rider is toominimal in relation to themuscle force re-quiredanywayforstabilisingthetrunk.

Theanteriorcantileverofthe“beam,”whichistheneckplushead,isflexeddownwards.Itsbendingmomentswillassumetheirgreatestvalues,iftheneckisstretchedorifaccelerationforcesaretransmittedthroughtheforelimbs,especiallyinthecanter.Bothrequireincreasedmuscle activities, which indeed have been observed by Kienapfel(2015).

5  | CONCLUSION

Asexpectedfromatheoreticalanalysis,inwhichthebodystemofahorseiscomparedtoaheavybeam,them.rectusisactiveatthosephasesofthestridecycle, inwhichthebendingmomentsassumetheirgreatestvalues,namelythediagonalstancephasesintrotandgallop.Them.obliquusexternusisactive,whiletorsionalforcesareactingonthebody,becausethehighestupwardacceleratingforcesaresupportedbythediagonallimbs.Them.longissimusdorsiisal-waysactiveattouchdownoftheipsilateralhindleg;itsbiomechani-calfunctionisthestoppingofthetrunkmovementandstabilisationofthetrunk.

Thismeans that the theoretical predictions based on the beamtheoryareconfirmed.

ACKNOWLEDGEMENTS

WehavetothankhugelytheWestfälischeReit-undFahrschuleandespeciallyMartinPlewaandBiancaSchwarzerforgivingtheirhorsesandrider.Also,wehavetothankBernhardGlenszczykforthegreathelpwiththelittlepilottestforthisstudy.AtlastwehavetothankJanSoerenKochforhelpinstatisticalquestionsandHans-GertKienapfelfortakingthevideotapes.

ORCID

K. Kienapfel http://orcid.org/0000-0001-5123-0242

REFERENCES

Ainsworth,D.,Smith,C.,Eicker,S.,Ducharme,N.,Henderson,K.,Snedden,K.,&Dempsey,J.(1997).Pulmonary-locomotoryinteractionsinexer-cisingdogsandhorses.Respiration Physiology,110,287–294.https://doi.org/10.1016/S0034-5687(97)00094-7

Álvarez, C., Rhodin,M., Byström,A., Back,W., &Weeren, P. R. (2009).Backkinematicsofhealthytrottinghorsesduringtreadmillversusovergroundlocomotion.Equine Veterinary Journal,41,297–300.https://doi.org/10.2746/042516409X397370

Bramble,D.,&Carrier,D.R. (1983).Runningandbreathing inmammals.Science,219,251–256.https://doi.org/10.1126/science.6849136

Carrier,D. (1990).Activityof thehypaxialmusclesduringwalking in thelizardiguanaiguana.Journal of Experimental Biology,152,453–470.

Carrier,D.(1993).Actionofthehypaxialmusclesduringwalkingandswim-minginthesalamanderdicamptodonensatus.Journal of Experimental Biology,180,75–83.

Cottriall, S., Ritruechai, P., &Wakeling, J. (2009). The effects of training aids on the longissimus dorsi in the equine back (accessed20October 2011).

Deban,S.M.,Schilling,N.,&Carrier,D.R.(2012).Activityofextrinsiclimbmuscles in dogs atwalk, trot and gallop.The Journal of Experimental Biology,215,287–300.https://doi.org/10.1242/jeb.063230

Demes,B.,&Gunther,M. (1989).Biomechanicsandallometricscaling inprimatelocomotionandmorphology.Folia Primatologica,53,125–141.https://doi.org/10.1159/000156412

Falaturi,P.(2001).Computerkinematographie(CKG)alsgeeignetesVerfahrenzurobjektivenBewegungsanalyse-BeschreibungundErgebnisse.Pfer­deheilkunde,1,30–41.https://doi.org/10.21836/PEM20010104

Gellman,K.,&Bertram,J.(2002).Theequinenuchalligament1:Structuralandmaterialproperties.Veterinary and Comparative Orthopaedics and Traumatology,15,1–6.

Gunther,M.,Ishida,H.,Kumakura,H.,&Nakano,Y.(1991).Thejumpasafastmodeoflocomotioninarborealandterrestrialbiotopes.Zeitschrift fur Morphologie und Anthropologie,78,341–372.

Hohn,B.,Preuschoft,H.,Witzel,U.,&Distler,C.(2013).Biomechanicsandfunctionalpreconditionsforterrestriallifestyleinbasaltetrapods,withspecial consideration ofTiktaalik roseae.Historical Biology,25, 167–181.https://doi.org/10.1080/08912963.2012.755677

Kienapfel,K. (2015).Theeffectofthreedifferenthead–neckpositionsontheaverageEMGactivityofthreeimportantneckmusclesinthehorse.J Anim Physiol Anim Nutr,99,132–138.http://doi.org/10.1111/jpn.12210

Konrad, P. (2011).EMG­Fibel, Eine praxisorientierte Einführung in die kine­siologische Elektromyographie,1.1thed.USA:Velamed,NoraxonINC.

Kummer,B.(1959).Biomechanik des Säugetierskelets.Berlin:deGruyter.Larson, S. (1995) Unique aspects of quadrupedal locomotion in nonhu-

manprimates.InE.Strasser,J.Fleagle,A.Rosenberger&H.Mc.Henry(Eds.),Primate locomotion, Recent advances (pp.157–173).NewYork:PlenumPress.

Licka,T.(2001).Electromyographicactivityofthelongissimusdorsimuscleinhorsesduringtrottingonatreadmill.American Journal of Veterinary Research,2,155–158.

Licka,T.,Frey,A.,&Peham,C.(2009).Electromyographicactivityofthelongis-simusdorsimusclesinhorseswhenwalkingonatreadmill.The Veterinary Journal,180,71–76.https://doi.org/10.1016/j.tvjl.2007.11.001

Loitsch,C.(1993).Kinematische Untersuchung über den Canter von Pferden (Equus caballus).Bochum:RuhrUniversitätBochum.

Milner-Brown, H., & Stein, R. (1975). The relation between the surfaceelectromyogram abd muscular force. The Journal of physiology, 246,549–569.https://doi.org/10.1113/jphysiol.1975.sp010904

Nickel, R., Schummer, A., Seiferle, E., & Frewein, J.(2004). Lehrbuch der Anatomie der Haustiere, Band I: Bewegungsapparat, 8. Stuttgart: un-veränd.Aufl.Parey.

Preuschoft, H. (1976). Funktionelle Anpassung evoluierender Systeme.5. Arbeitsgespräch zu Phylogenetik und Systematik. In G. Altmann,

10  |     KIENAPFEL Et AL.

J.Dörjes,P.Dullemeijer,J.L.Franzen,M.Grasshoff,W.F.Gutmann,H. Heine, G. W. Hoffmann, W. Lehfeldt, D. Mollenhauer, D. S.Peters & H. Preuschoft (Eds.), Evoluierende Systeme I und II. 4. und 5. Arbeitsgespräch zu Fragen der Phylogenetik und Systematik in der Außenstelle Lochmühle, 1.-4.4.1974 und 10.-13.3.1975. 1-202, 45Abb.,1976.Franfurt:KramerVerlag,ISBN3-7829-1062-1.

Preuschoft, H. (1985). On the quality and magnitude of mechanicalstresses inthe locomotorsystemduringrapidmovements.Zeitschrift für Morphologie und Anthropologie,75,245–262.

Preuschoft,H. (Ed.), (1987)Studien zu den Bewegungen von Sportpferden. Warendorf: Wissenschaftliche Publikation. Deutsche ReiterlicheVereinigungVol.9.Verl.d.Dt.Reiterl.Vereinigung.

Preuschoft, H., & Fritz, M. (1977). Mechanische Beanspruchungen imBewegungsapparat von Springpferden. Fortschritte der Zoologie, 24,75–97.

Preuschoft,H.,&Günther,M.M. (1994).Biomechanics andbody shapein primates compared with horses. Zeitschrift für Morphologie und Anthropologie,80,149–165.

Preuschoft, H., Hohn, B., Distler, C.,Witzel, U., & Sick, H. (2005). Ribsand rib cages in terrestrial vertebrates: Their mechanical functionand stressing, analysed with the aid of FESA. Journal of Vertebrate Paleontology,31(suppl3),101.

Preuschoft,H.,&Klein,N. (2013).Torsion andbending in theneck andtail of sauropoddinosaurs and the function of cervical ribs: Insightsfromfunctionalmorphologyandbiomechanics.PLoS ONE,8,e78574.https://doi.org/10.1371/journal.pone.0078574

Preuschoft, H., Witzel, U., Hohn, B., Schulte, D., & Distler, C. (2007)Biomechanicsoflocomotionandbodystructureinvaranidswithspe-cialemphasisontheforelimbs.InH.-G.Horn,W.Böhme&U.Krebs(Eds.), Proceedings of the “Third Multidisciplinary World Conference on Monitor Lizards”. Mertensiella, advances in monitor research III (pp.59–78).Bonn. https://www.sauropod-dinosaurs.uni-bonn.de/publika-tionen(accessed21October2016).

Ritter,D.(1996).Axialmusclefunctionduringlizardlocomotion.Journal of Experimental Biology,199,2499–2510.

Ritter,D.,Nassar,P.,Fife,M.,&Carrier,D.(2001).Epaxialmusclefunctionintrottingdogs.Journal of Experimental Biology,204,3053–3064.

Robert, C., Audigie, F., Valette, J., Pourcelot, P., & Denoix, J. (2001).Effectsof treadmill speedon themechanicsof theback in the trot-ting saddlehorse.Equine Veterinary Journal,33, 154–159. https://doi.org/10.1111/j.2042-3306.2001.tb05380.x

Robert, C., Valette, J., Degueurced, C., & Denoix, J. (1999). Correlationbetween surface electromyography and kinematics of the hindlimbof horses at trot on a treadmill.Cells Tissues Organs,165, 113–122.https://doi.org/10.1159/000016681

Robert,C.,Valette,J.,&Denoix,J.(2000).Surfaceelectromyographicanal-ysisofthenormalhorselocomotion:Apreliminaryreport.Conference on Equine Sports Medicine and Science,32,80–85.

Robert,C.,Valette,J.,&Denoix,J.(2001).Theeffectoftreadmillinclinationandspeedontheactivityofthreetrunkmusclesinthetrottinghorse.Equine Veterinary Journal,33,466–472.

Robert, C., Valette, J., Pourcelot, F., Audigie, J., & Denoix, J. (2002).Effects of trotting speed on muscle activity and kinematics in

saddlehorses. Equine Veterinary Journal, 34, 295–301. https://doi.org/10.1111/j.2042-3306.2002.tb05436.x

Schilling,N.,&Carrier,D. (2009).Functionoftheepaxialmusclesduringtrotting.The Journal of Experimental Biology,212,1053–1063.https://doi.org/10.1242/jeb.020248

Slijper,E.J.(1946).Comparative biologic­anatomical investigations on the ver­tebral column and spinal musculature of mammals.Amsterdam:North-HollandPublishingCompany.

Sloet van Oldruitenborgh-Oosterbaan, M., & Clayton, H. (1999).Advantages and disadvantages of track vs. treadmill tests. Equine Exercise Physiology,31,645–647.

Stern, J.,Wells, J.,Vangor,A., & Fleagle, J. (1977). Electromyography ofsomemusclesof theupper limb inAtelesandLagothrix.Yearbook of Physical Anthropology,20,498–507.

vonScheven,C.(2010).The anatomy and function of the equine thoracolumbar Longissimus dorsi muscle.München:Ludwig-Maximilians-Universität.

Wakeling,J.,Ritruechai,P.,Dalton,S.,&Nankervis,K. (2007).Segmentalvariation in theactivityandfunctionof theequine longissimusdorsimuscleduringwalkandtrot.Equine and Comparative Exercise Physiology,4,95–103.

Witte,H.,Lesch,C.,Preuschoft,H.,&Loitsch,C.(1995a).DieGangartender Pferde: Sind S chwingungsmechanis- men entscheidend? Teil I:Pendelschwingungen der Beine bestimmen den Schritt. Pferdeheil­kunde,11(3),199–206.https://doi.org/10.21836/PEM19950305

Witte,H.,Lesch,C.,Preuschoft,H.,&Loitsch,C.(1995b).DieGangartender Pferde: Sind Schwingungsmecha- nismen entscheidend? TeilII: Federschwingungen bestimmen den Thab und den Galopp.Pferdeheilkunde,11(4),265–272.

Witzel,U.,Mannhardt,J.,Goessling,R.,deMichaelis,P.,&Preuschoft,H.(2011).Finiteelementanalysesandvirtualsynthesisofbiologicalstruc-tures and their application to sauropod skulls. InN.Klein,K.Remes,C. Gee and M. Sander. (Eds.), Biology of the Sauropod dinosaurs: Understanding the life of giants (pp. 171–181). Bloomington: IndianaUniversityPress,ISBN:978-0-253-35508-9.

Zschokke,E.(1892).Untersuchungen über das Verhältnis der Knochenbild ung zur Statik und Mechanik des Vertebratenskelettes.Zürich:OrellFüssli.

Zsoldos, R., Kotschwar,A., Rodriguez, C., Peham, C., & Licka, T. (2010).Activity of the equine rectus abdominis and oblique external ab-dominalmusclesmeasuredby surfaceEMGduringwalkand trotonthe treadmill. Equine Veterinary Journal, 42, 523–529. https://doi.org/10.1111/j.2042-3306.2010.00230.x

How to cite this article:KienapfelK,PreuschoftH,WulfA,WagnerH.Thebiomechanicalconstructionofthehorse`sbodyandactivitypatternsofthreeimportantmusclesofthetrunkinthewalk,trotandcanter.J Anim Physiol Anim Nutr. 2017;00:1–10. https://doi.org/10.1111/jpn.12840