Feeling stiffness in the back: a protective ... - DOCKSCI.COM

Feeling stiffness in the back: a protective perceptual inference in chronic back pain Tasha R. Stanton1,2, G. Lorimer Moseley1,2, Arnold Y. L. Wong3,4 ... 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www.nature.com/scientificreportsOPENReceived:22December2016Accepted:27July2017Published:xxxxxxxxFeelingstiffnessintheback:aprotectiveperceptualinferenceinchronicbackpainTashaR.Stanton1,2,G.LorimerMoseley1,2,ArnoldY.L.Wong3,4&GregoryN.Kawchuk3Doesfeelingbackstiffnessactuallyreflecthavingastiffback?Thisresearchinterrogatesthelong-heldquestionofwhatinformsoursubjectiveexperiencesofbodilystate.Weproposeanewhypothesis:feelingsofbackstiffnessareaprotectiveperceptualconstruct,ratherthanreflectingbiomechanicalpropertiesoftheback.Thishasfar-reachingimplicationsfortreatmentofpain/stiffnessbutalsoforourunderstandingofbodilyfeelings.Overthreeexperiments,wechallengetheprevailingviewbyshowingthatfeelingstiffdoesnotrelatetoobjectivespinalmeasuresofstiffnessandobjectivebackstiffnessdoesnotdifferbetweenthosewhoreportfeelingstiffandthosewhodonot.Rather,thosewhoreportfeelingstiffexhibitself-protectiveresponses:theysignificantlyoverestimateforceappliedtotheirspine,yetarebetteratdetectingchangesinthisforcethanthosewhodonotreportfeelingstiff.Thisperceptualerrorcanbemanipulated:providingauditoryinputinsynchronytoforcesappliedtothespinemodulatespredictionaccuracyinbothgroups,withoutalteringactualstiffness,demonstratingthatfeelingstiffisamultisensoryperceptualinferenceconsistentwithprotection.Together,thispresentsacompellingargumentagainsttheprevailingviewthatfeelingstiffisanisomorphicmarkerofthebiomechanicalcharacteristicsoftheback.Bodilyfeelingsconstituteafundamentalaspectofself-awarenessandprovidecriticalhomeostaticfunctions–e.g.,feelingcoldmakesoneseekwarmth1;feelingpainmakesoneseekprotection2;feelingparchedmakesonedrink3.Weassumethatthesebodilyfeelingsreflectthebiologicalstateofourbodytissues–a‘read-out’,sotospeak,ofsomatosensoryandvisceralinput–particularlywhenthefeelingislocatedsomewhereinthebody,asitisforpainorstiffness.Thereisgrowingevidenceforpainhowever,thatitishighlymodulatedbyawiderangeofcognitiveandcontextualvariables4,5.Forexample,visuallymanipulatingtheperceivedsizeofone’shandaltersthepainexperiencedinexperimentalcontexts6andduringmovementofachronicallypainfullimb7,andilluminatingablueorredlightinsynchronywithdeliveringanoxiouscoldstimuluscantransformthefeelingevokedfromuncomfortablycoldtopainfullyhot5.Thatsomaticinputtriggeredbyphysiologicalresponsesisimportantincognitiveprocesses–so-called‘embodiedcognition’–hasrecentlybeencounteredwiththeideathatbodilyawareness(e.g.,oursenseofbodilyownership)mightdirectlymodulatephysiologicalregulationofbodytissueinananatomicallyspecificway8,9.Indeed,wenowknowthatthesenseofbodilyownership,thefeltlocation,andtheanthropometriccharacteristicsofourbodyparts,aretightlylinkedtotheirphysiologicalregulationinabi-directionalmanner7,10.Extensivehumandatafrombothhealthyanddiseasedpopulationshaveledtotheproposalofthecorticalbodymatrixtheory11,thepredictionsofwhichareyieldingnewdevelopmentsinourunderstandingandtreatmentofsomepathologicalpainconditions12.Onefeelingthatisalmostuniversallyexperienced,whichimpactsonourdailylives13,14,butwhichremainsrelativelyignored,isfeelingstiff.Feelingjointstiffnessisunanimouslyattributedtoactuallyhavingstiffjoints.Takeforexamplehavinga‘stiffback’.Weassumethatthisfeelingreflectsalteredforce-responseprofilesofthetissuesinourback(objectivebiomechanicalstiffness).Butdoesit?Afeelingofjointstiffnesshasbeenshownto1TheSansomInstituteforHealthResearch,SchoolofHealthSciences&PainAdelaideConsortium,TheUniversityofSouthAustralia,Adelaide,SA,Australia.2NeuroscienceResearchAustralia,Sydney,NSW,Australia.3DepartmentofPhysicalTherapy,FacultyofRehabilitationMedicine,TheUniversityofAlberta,Edmonton,Alberta,Canada.4DepartmentofRehabilitationSciences,FacultyofHealthandSocialSciences,TheHongKongPolytechnicUniversity,HongKongSpecialAdministrationRegion,HongKong,China.CorrespondenceandrequestsformaterialsshouldbeaddressedtoT.R.S.(email:[email protected])SCIENTIFICReports|7:9681|DOI:10.1038/s41598-017-09429-11www.nature.com/scientificreports/remaindespitelossofthelimb15suggestingthatthebodilyfeelingofstiffnesscanbeindependenttothebiologicalstateofthetissues.Feelingstiffisasignificantpredictorofdisability16andisaprimarytargetofinterventionsformanymusculoskeletalconditionsincludingbackpain,arthritis,andneckpain.Worldwide,themostburdensomeoftheseconditionsislowbackpain(LBP).Affecting~10%oftheworld’spopulation(~632millionpeople),chronicLBPisalsotheleadingcauseofdisability17.Despiteincreasinghealthcareexpenditure,clinicaloutcomesremainsub-optimal18,spurringacalltore-examinebasicmechanismsassociatedwithLBPanditssymptoms19,mostobviouslystiffness.Herewedescribeaseriesofexperiments,theresultsofwhichcompelustorethinkwhatitmeanstofeelstiff,whatdetermineshowstiffwefeel,andwhatecologicalvaluefeelingstiffmighthave.First,weaimedtoestablishwhetherfeelingbackstiffnessisrelatedto(i)actualstiffnessofthebackasreflectedinforce-responseprofiles,and(ii)amanifestationofactualstiffnessthatwouldofferaprotectivebehaviouraladvantage–theabilitytojudgethemagnitude(andchange)ofappliedforcetotheback.Specifically,Study1ainterrogatedtheprevailingviewthatfeelingsofstiffnessreflectobjectivebiomechanicalbackstiffness.Wehypothesisedthatifthistheoryiscorrect,subjectiveandobjectivebackstiffnessmeasureswouldcloselyrelate,andpeoplewhofeelbackstiffnesswouldobjectivelyhaveastifferspinethanthosewhodonot.Study1bevaluatedwhetherpeoplewithfeelingsofbackstiffnessshowprotectiveperceptualresponses–dotheydifferfromthosewithoutfeelingsof stiffnessatestimatinghowmuchforcewasappliedtothespineandatdetectingchangeinthisforce?Wehypothesisedthattheywouldoverestimateforce,butbemoresensitivetochangesinforce,suggestiveofaprotectiveprofile.Second,wehypothesisedthatfeelingstiffshouldbemodulatedbysensorycuesthatareunrelatedtoactualbackstiffness.Toinvestigatethis,weexploitedthebrain’spredilectionforcross-modalintegrationbysynchronisingmechanicalloadingofthebackwithtwodifferentauditorysignals–thesoundofa‘creakydoor’andagentle‘whooshing’sound.Giventhecommonpairingofsounds(grinding,popping)withmovementofastiffback,weanticipatedthatpairingsoundwithforceappliedtothespinewouldprovideecologicallyvalidinformationthatmayalterprotectiveperceptualresponses.Specifically,Study2evaluatedtheempiricalsupportforournewtheorythatfeelingstiffnessinthebackrepresentsaperceptualconstruct,whichcouldbemodifiedbyadditionalbody-relevantsensoryinformation,suchassound.Wehypothesisedthatsoundwouldmodifybackperceptionandthatthismodificationwouldbeenhancedinthosethatreportfeelingbackstiffness.Overall,wepostulatethatfeelingbackstiffnessrepresentsaprotective,perceptualinference:abodilyfeelingcreatedtoprovidethecriticalhomeostaticfunctionofpreventingmovementandpotentialre-injury.Wedosobasedonthebi-directional,intimaterelationshipbetweenperceptionandmovement:whenwemove,weconstantlyreceivesensoryfeedback,asaresultofthemovement,thatinformsourperceptionofbodyposition,butwealsoperceivethingsinlinewithhowwewillact20.Forexample,peopleunderestimatethedistancefromtheirbodytoapain-relievingswitch,butonlywhentheyareabletoreachforit20.Thefollowingseriesofexperimentscomprehensivelyinterrogateboththeprevailingviewthatfeelingbackstiffnessequatestohavingobjectivebackstiffness(Study1a)andournewhypothesisofstiffnessasaprotectiveperceptualinference(Study1bandStudy2).ResultsWerecruited15peoplewithchronicLBPwhoalsoreportedhavingchronicfeelingsofbackstiffnessand15age-andgender-matchedhealthycontrolswithoutLBPorfeelingsofback stiffness.Table 1presentstheirdemographicandclinicalinformation.Study1a.FeelingstiffdoesnotequatetobeingstiffinchronicLBP. Study1ausedanestablished,customiseddevice,validatedinhumans21,thatprovidesastandardisedforcetothespine,measuringdisplacementoftheapplicationprobe(Fig. 1a).Objectivestiffnessmeasuresarecalculatedbyconsideringthisforce–displacementrelationship(AverageStiffness[AvgStiff]andTerminalStiffness[TermStiff];seeMethods).Weestablishedhowstiffparticipants’backs‘felt’(subjective/perceivedstiffness;0–100numericalratingscale[NRS],rangingfrom“notstiffatall”to“moststiffimaginable”)andhowstifftheirbacksobjectivelywere(customiseddevice).Todetermineiffeelingsofstiffnesscorrespondtohowstiffthebackactuallyis,weusedSpearman’srho.Wefoundnosignificantrelationshipsbetweenperceivedandactualstiffnessatanyappliedforcelevel(55 N,60 N,70 N)oranystiffnessmeasure(AvgStifforTermStiff)inpeoplewithLBPandstiffness(p = 0.24–0.99;Fig. 1b).Wewereunabletoinvestigatethisrelationshipinhealthycontrolsduetoinsufficientvariability(8ofthe15controlsdidnotreportfeelinganybackstiffness[ratingof0onthe100-pointNRS]andtheremainderallreportedstiffnessof5).Second,wetestedifobjectivemeasuresofstiffnessdifferedbetweenthosewhoreportedfeelingLBPandstiffnessandthosewhoreportedtheydidnot(n = 30).Weconsideredobjectivestiffnessmeasuresatthestartandendoftestingtoevaluateforanybetween-groupdifferencesinbiomechanicalspinepropertiessecondarytorepeatedtissueloading(factor:‘time’).Therewerenosignificantdifferencesbetweengroupsineitheroftheobjectivespinalstiffnessmeasuresatanyappliedforcelevel(Fig. 1c).Specifically,at60 N(±1 N),therepeatedmeasuresMANOVAfoundnosignificantbetween-groupdifferenceforobjectivebackstiffnessmeasures(AvgStiffandTermStiff)overtime(F2,27 = 1.04,p = 0.37,partialη2 = 0.072).Univariatetestresultsfromthisanalysis(stiffnessmeasurespecific)arepresentedinTable 2andsupportthelackofeffectofgroup,timeorgroupxtimeinteraction.Asensitivityanalysis,evaluatingonlyparticipantswhoreceived60 N(n = 22),confirmedtheabovefindings(SupplementaryTable S1).Additionally,aMANOVAconfirmedthattherewasnodifferencebetweengroups(n = 30)forAvgStiffandTermStiffat55 N(F2,27 = 2.45,p = 0.11,partialη2 = 0.153)andat70 N(F2,27 = 0.98,p = 0.39,partialη2 = 0.068)suggestingthatthislackofobjectivestiffnessdifferenceholdsacrosstheappliedforcespectrum(SeeTable 2forunivariateanalysesresults;SupplementaryFigure S1).Usingthesevalidatedmethods,feelingstiffnessinone’sbackwasnotrelatedtothebiomechanicalpropertiesofthespine.SCIENTIFICReports|7:9681|DOI:10.1038/s41598-017-09429-12www.nature.com/scientificreports/Study1aand1bStudy2p-valueCLBP&stiffness(n = 10)Healthycontrols(n = 10)0.5423.4(4.8)25.7(5.4)0.330.697M,3F6M,4F0.64170.2(11.1)0.14176.0(11.2)170.5(13.5)0.3373.5(15.3)0.8573.1(16.5)71.3(13.3)0.80DemographicvariablesCLBP&stiffness(n = 15)Healthycontrols(n = 15)Age(years)27.1(8.3)28.9(8.3)Gender11M,4F10M,5FHeight(cm)176.5(11.1)Weight(kg)74.5(16.5)p-valueCurrentpain34.3(15.5)1.2(2.2) 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