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The acquisition and generalization of cued and contextual pain-related fear: An experimental study using a voluntary movement paradigm

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The acquisition and generalization of cued and contextual pain-related fear: An experimental study using a voluntary movement paradigm
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  This article appeared in a journal published by Elsevier. The attachedcopy is furnished to the author for internal non-commercial researchand education use, including for instruction at the authors institutionand sharing with colleagues.Other uses, including reproduction and distribution, or selling orlicensing copies, or posting to personal, institutional or third partywebsites are prohibited.In most cases authors are permitted to post their version of thearticle (e.g. in Word or Tex form) to their personal website orinstitutional repository. Authors requiring further informationregarding Elsevier’s archiving and manuscript policies areencouraged to visit:http://www.elsevier.com/copyright  Author's personal copy The acquisition and generalization of cued and contextual pain-related fear:An experimental study using a voluntary movement paradigm Ann Meulders a, ⇑ , Johan W.S. Vlaeyen a,b,c a Research Group on Health Psychology, University of Leuven, Leuven, Belgium b Center of Excellence Generalization Research in Ill Health and Psychopathology, University of Leuven, Leuven, Belgium c Department of Clinical Psychological Science, Maastricht University, The NetherlandsSponsorships or competing interests that may be relevant to content are disclosed at the end of this article a r t i c l e i n f o  Article history: Received 21 April 2012Received in revised form 3 September 2012Accepted 30 October 2012 Keywords: Contextual pain-related fearCued pain-related fearFear conditioningFear generalizationUnpredictabilityVoluntary movement paradigm a b s t r a c t Recentevidenceindicatesthatpain-relatedfearcanbeacquiredthroughassociativelearning.Intheclinic,however, spreading of fear and avoidance is observed beyond movements/activities that were associatedwithpainduringthesrcinalpainepisode.Onemechanismaccountingforthisspreadingoffearis stimulus generalization .Inavoluntarymovement-conditioningparadigm,healthyparticipantsreceivedpredictablepain(ie,onemovementpredictspain,anotherdoesnot)inonecontext,andunpredictablepaininanothercontext. The former procedure is known to induce cued pain-related fear to the painful movement,whereas the latter procedure generates contextual pain-related fear. In both experimental pain contexts,we subsequently tested fear generalization to novel movements (having either proprioceptive featuresin common with the srcinal painful movement or nonpainful movement). Results indicated that in thepredictable pain context, pain-related fear spreads selectively to novel movements proprioceptivelyrelatedtothesrcinalpainfulmovement, andnottothoseresemblingthesrcinalnonpainful movement.Intheunpredictablecontext,nondifferential feargeneralizationwasobserved, suggestingpersistentcon-textualpain-relatedfearandpoorsafetylearning.Thesedataillustratethatspreadingofpain-relatedfearis fostered by previously acquired movement-pain contingencies. Based on recent advances in anxietyresearch, we proposed an innovative approach conceptualizing predictable pain as a laboratory modelfor fear of movement in regional musculoskeletal pain, and unpredictable pain generating contextualpain-related fear as a prototype of widespread musculoskeletal pain. Consequently, fear generalizationmight play an important role in spreading of pain-related fear and avoidance behavior in regional andwidespread musculoskeletal pain.   2012 International Association for the Study of Pain. Published by Elsevier B.V. All rights reserved. 1. Introduction Evidencefromcross-sectionalstudieswithchronicpainsufferers[20] and prospective studies in acute pain [10,16,40] corroborates the fear-avoidance model’s assumption that pain-related fear is akey factor in the srcins of chronic musculoskeletal pain [46,47]. Arecentconditioningstudyusingjoystickmovementsasconditionedstimuli (CSs) and a painful electrocutaneous stimulus as uncondi-tioned stimulus (US) demonstrated the role of associative learningin the development of pain-related fear in healthy individuals[27].Thatis,duetopropositionalknowledgerelatingpaintoanini-tially neutral movement [31,34], this movement starts to signaldanger/harm and comes to elicit autonomic fear responses and tospur avoidancebehavior.In chronic pain patients, fear and avoidance are often not re-stricted to movements/activities that were associated with painduring the initial pain episode [21]. An intriguing yet empiricallyunder-investigated question entails how spreading of pain-relatedfear and avoidance in chronic pain occurs. From an associativelearning perspective, conditioned fear responses might extend toa range of novel stimuli resembling the srcinal fear-eliciting CS.In essence,  stimulus generalization  is highly adaptive, because theability to detect similarities between unique but related stimulimay contribute to avoiding harm in a dynamic environment[13,15,17]. Yet, together with reducing the risk of missing positivethreat alarms, generalization bears an increased risk to respond tofalse threat alarms, which might be the case in persistent fear andavoidance behavior in chronic pain. It is recognized that in otherpsychological disorders (eg, posttraumatic stress disorder, panic 0304-3959/$36.00    2012 International Association for the Study of Pain. Published by Elsevier B.V. All rights reserved.http://dx.doi.org/10.1016/j.pain.2012.10.025 ⇑ Corresponding author. Address: Department of Psychology, University of Leuven, Tiensestraat 102, Box 3726, Leuven 3000, Belgium. Tel.: +32 0 16 32 6038; fax: +32 0 16 32 61 44. E-mail address:  ann.meulders@ppw.kuleuven.be (A. Meulders). www.elsevier.com/locate/pain PAIN  154 (2013) 272–282  Author's personal copy disorder),  overgeneralization  of fearful responding is critically in-volved [7,8,24,25,38].The identification of the dimensional and componential struc-tures of pain-related fear challenges the view that it is a unitaryconcept [42]. Based on contextual fear-conditioning literature[11,12,29,43], 2 types of pain-related fear can be distinguished,depending on the  temporal (un)predictability  of the US: cued andcontextual pain-related fear. Cued pain-related fear is typically in-duced by  predictable pain  (ie, pairings of movement and pain-US),whereas chronic contextual pain-related fear is induced by u npre-dictable pain  (ie, pain-US explicitly unpaired with movements)[27,28]. Consistent with these observations, we argued that pre-dictable pain may be viewed as a laboratory model for cuedpain-related fear (sometimes termed ‘‘kinesiophobia’’ [19]) in re-gional musculoskeletal pain(eg, back pain) andunpredictable painmaybeaprototypeforwidespreadmusculoskeletalpain(eg,fibro-myalgia) [9,14,35].To date, generalization of fear acquisition has never been sys-tematicallyinvestigatedinthechronicpaindomain. UsingtheVol-untary Joystick Movement Paradigm [27,28,30], we tested feargeneralization to novel diagonal movements (generalization stim-uli; GSs) in both a predictable and an unpredictable pain context.We expected (a) generalization to novel movements propriocep-tively related to the srcinal painful movement (GS+) but not tothose proprioceptively resembling the nonpainful movement(GS  ) in the predictable context, and (b) that contextual pain-re-lated fear fosters nonspecific fear generalization to novel move-ments in the unpredictable context (GS+=GS  ). Becausecategory membership of novel stimuli is more elusive when thecontext acts as a predictor for the pain-US, fear might generalizeto a broader range of stimuli than in the predictable context. 2. Methods and materials  2.1. Participants In total, 40 healthy individuals (28 females; M age  =21years,SD age  =2.81, range=18-30years) participated in this study andwere compensated as follows: (A) psychology students of the Uni-versityofLeuvenreceivedcoursecredits(n=7),and(B)volunteers(mostly nonpsychology university students and highly educatedworking people) were paid  € 10 (n=33). Participants completed ageneral health checklist to make sure they did not suffer fromrespiratory or cardiovascular diseases, neurological diseases (eg,epilepsy), psychiatric disorders, or any other minor or major ill-ness,andtheydidnothaveachronicpainconditionnorwerepreg-nant. Additionalexclusioncriteriawerehearingproblemsandpainat the dominant hand or wrist. The experimental protocol was ap-proved by the Ethical Committee of the Department of Psychologyof the University of Leuven. All participants signed the informedconsentform,whichexplicitlystatedthattheywereallowedtode-cline participation at any time during the experiment.  2.2. Stimulus material and measures The experiment was run on a Windows XP (Microsoft Corpora-tion, Redmond, WA, USA) computer (Dell Optiplex 755; Dell Inc.,Round Rock, TX, USA) with 2GB RAM and an Intel Core2 Duo pro-cessor (Intel, Santa Clara, CA, USA) at 2.33GHz and an ATI Radeon2400 graphics card (Advanced Micro Devices, Sunnyvale, CA, USA)with256MBofvideoRAM,usingAffect4.0[39]. Weused4propri-oceptive stimuli (ie, moving a Logitech [Newark, CA, USA] Attack 3 joystickinthehorizontalplane[left/right]andintheverticalplane[upward/downward]) as CSs. The GSs were diagonal movements,(ie, left-top, right-top, left-bottom, right-bottom). Proprioceptionisrestrictivelydefinedastheperceptionofpostureandmovement,alsoreferredtoasposturalsomesthesis.Therefore,itcanbearguedthat themostrelevantfeaturesthat theGSssharewiththeoriginalCSsareproprioceptiveinnature.However,inthecurrentstudy,vis-uospatial features (ie, location/direction of movement in a 3-dimensional space) of course coincide with proprioception andmay be involved as well. The pain-US was an electrocutaneousstimulus (2-ms duration), which was delivered by a commercialconstantcurrentstimulator(DS7A,Digitimer,WelwynGardenCity,England)throughsurfaceSensorMedics(Homestead,FL,USA)elec-trodes (8mm) filled with K-Y gel (Johnson & Johnson, New Bruns-wick, NJ, USA) that were attached to the wrist of the dominanthand.Duringthecalibrationprocedure,participantsreceivedaser-ies of electrocutaneous stimuli of increasing intensity and wereaskedtoindicatehowintense/painful eachstimuluswas onascalefrom1to10where1means:‘‘  you feel something but this is not pain- ful,itismerelyasensation ’’;2means:‘‘ thissensationstartstobepain- ful,butitisstillaverymoderatepain ’’;upto10,whichmeans:‘‘ thisistheworstpain youcanimagine. ’’Asubjectivestimulusintensityof8,whichrefers to a stimulus that is ‘‘ significantly painful and demand-ing some effort to tolerate ’’ was targeted (mean subjective stimulusintensity was 8.31, SD=0.82, range 5-10). The mean stimulusintensity was 27.8mA (SD=13.65, range 8-64mA).Conditioned pain-related fear was measured through subjec-tive self-reports as well as a more objective psychophysiologicalcorrelate of fear learning, that is, the eyeblink startle response.The startle reflex is a cross-species, full-body reflex involved indefensive response mobilization. It is a very short latency reflextriggered by startle-evoking stimuli (eg, acoustic startle probe)that is mediated by a simple brainstem and spinal cord pathway,both directly and indirectly connected to the amygdala [4]. Inanxiety research, electromyographic (EMG) activity of the orbicu-laris oculi triggered by an acoustic startle probe is often used asan approximation of the eyeblink component of the startle re-sponse.  Startle modulation  refers to the increase or potentiationof the startle reflex during fear states elicited by the anticipationof an aversive stimulus (eg, an electrocutaneous stimulus). In thepresent setup, the startle probe was a 100-dBA burst of whitenoise with instantaneous rise time presented binaurally for50ms through headphones. Eyeblink startle responses elicitedby startle probes delivered  during the CS/GS movements  served asan index of cued pain-related fear. Eyeblink startle responses elic-ited by startle probes  during the intertrial interval (ITI)  served as anindex of contextual pain-related fear.  2.3. Procedure The experiment was conducted during an 80-minute sessionand consisted of a preparation phase, a practice phase, a habitua-tion phase, an acquisition phase, a transfer-of-acquisition phase,and a generalization phase. In a within-subjects design (Table 1),participants received both predictable pain stimuli in one contextand unpredictable pain stimuli in another context. Half of the par-ticipantsmovedthejoystickhorizontally(left/right)inthepredict-able context, and vertically (upward/downward) in theunpredictable context. The other half of the participants had thereversecombination:theymovedthejoystickverticallyinthepre-dictable context, and horizontally in the unpredictable context. Inthepredictablecontext,onemovement(CS p +)wasconsistentlyfol-lowed by the pain-US, and the other movement (CS p  ) was neverfollowed by the pain-US. Note that the direction of joystick move-ment that served as the CS p + and the CS p  in the predictable con-text was counterbalanced across participants. In the unpredictablecontext, however, the pain-US was never delivered contingent oneither of the joystick movements (CS u1  and CS u2 ), but waspresented during the context (ITI). During acquisition training,participants voluntarily initiated their movements, so they freely  A. Meulders, J.W.S. Vlaeyen/PAIN   154 (2013) 272–282  273  Author's personal copy choseinwhichdirectiontheyweregoingtomoveonacertaintrial.During the transfer-of-acquisition phase, however, they could nolonger choose the order of the movements themselves, but themovement direction was signaled. During the generalizationphase, the same signaling procedure was used to test conditionedresponding to novel diagonal movements (GSs) under extinction.  2.3.1. Preparation phase Participants were informed (orally and in writing) that painfulelectrocutaneous stimuli (pain-US) and loud noises (acoustic star-tle probes) would be administered during the experiment. Afterprovidinginformedconsent, participantswenttotheexperimentalroom. The electrodes for eyeblink startle responses were attachedand the intensity level of the pain-US was selected following thecalibration procedure (see Section 2.2. Stimulus material andmeasures).  2.3.2. Practice phase Before initiating the practice phase, participants received de-tailed instructions about the experimental task. In each block, par-ticipantshadtomovethejoystick8timesasquicklyandaccuratelyas possible when prompted by a starting signal ‘‘+’’ (fixation crosspresentedinthemiddleofthecomputerscreen),inwhateverorderthey freely chose. The position of   counter bars  on the computerscreenindicatedinwhichmovementplane(horizontalvs. vertical)they had to move. The counter bars, each divided into 4 equal seg-ments, always appeared on 2 sides of the computer screen (left/right or top/bottom) (Fig. 1). In a horizontal block, these bars weredisplayedontheleftandrightsideofthecomputerscreen,whereasintheverticalblock,thesebarsappearedatthetopandthebottomof the computer screen. Successful movements always resulted inchanging the color of the segments of the corresponding counterbar. That way, participants could instantly evaluate how manymovements in each direction remained to be carried out. In total,2 blocks of 8 trials were run: the first block comprised 4 trials ineach of both directions in the horizontal movement plane (4 left/4 right), and the second block comprised 4 trials in each of bothdirectionsintheverticalmovementplane(4top/4bottom), or viceversa.Duringthepracticephase,noacousticstartleprobesorpain-USswerepresented,andonlineverbalfeedbackaboutthetaskper-formance was provided by the experimenter.  2.3.3. Startle habituation phase Ahabituationphasewasincludedtopreventpossibleconfoundsin the databecause the responses to the first startleprobes usuallyare relatively large. The habituation phase included 12 trials, eachlasting for 24seconds (with a variable ITI of, on average, 5seconds[±2seconds]). During each trial, one startle probe is presented(100-dBA burst of white noise), either between the 1 st and the2 nd second (4 trials), at the 10 th second (4 trials), or between the15 th and17 th second(4trials)ofthetrial.Thetimingofprobesdur-ing trials was randomized across participants. During this phase,the participants wore headphones, and only dimmed light wasavailable. Note that no pain-USs were delivered during this phase.  2.3.4. Acquisition phase This phase was largely identical to the practice phase, with theexception that (1) pain-USs and startle probes were presented, (2)8blocks(4predictableand4unpredictable)of8trialswererunin-steadof2blocks,and(3)instructionsnowemphasizedtopaycloseattentiontothestartingsignal ‘‘+’’ andtorespondasfastandaccu-rately as possible upon its presentation. Although a CS movementwas of variable length depending on the participants’ movementspeed, a trial typically included an ITI consisting of a pre-CS inter-val of 3.5seconds and a post-CS interval of 8seconds. The pain-USwas presented within each CS p + trial in the predictable context(100%contingency) andinhalf of thetrials duringITI intheunpre-dictablecontext.Inthepredictablecontext,theUSoccurredimme-diately after the CS p + movement. In the unpredictable context, thepain-US occurred 1-3seconds before the presentation of the start-ing signal ‘‘+,’’ or 0.5-2.5seconds after the CS movement. In eachblockwith8CSmovements, 4of thestartleprobes werepresentedduring the CS movements (2 during CS p + or CS u1 , and 2 duringCS p   or CS u2 ), and 4 during the ITI (2 probe positions before theCS and 2 probe positions after the CS). To avoid startle facilitationduring ITI being confounded by direct responses to presentationsof the pain-US in the unpredictable context, startle probes werepresented before the CS when the pain-US was presented afterthe CS, and after the CS when the pain-US was presented beforetheCS. Notethat wedidnotinformtheparticipantsaboutthecon-tingencies betweenthe joystickmovements (CSs) and the pain-US.Aftereachconditioningblock,theparticipantsratedthecuedpain-related fear elicited by each of the CS movements.  2.3.5. Transfer of acquisition Trials during the transfer of acquisition phase were basicallybuilt up the same way as during the acquisition phase. Yet, CSmovements were no longer voluntarily initiated but signaled. Thatis, 50ms after trial onset, a red asterisk ( ⁄ ) appeared for 500ms atoneoftheCSmovementdirections(left/rightinahorizontalblock;top/bottom in a vertical block), indicating in which direction par-ticipants had to move. Before actually performing the signaledmovement, participants rated their US-expectancy and cuedpain-related fear. After completing the ratings, they waited forthe ‘‘+’’ starting signal to start moving into the signaled direction.After successfully performing the signaled CS movement, a post-CS ITI of 8seconds followed (cfr. timing acquisition). During thetransfer phase, 2 blocks (one predictable and one unpredictable)  Table 1 Experimental design summary. Context Practice Habituation Acquisition Transfer of acquisition GeneralizationPredictable 4  CS p + only 6 probes 12  CS p + 4  CS p + 2  GS p + u1 4  CS p – 12   CS p – 4  CS p – 2  GS p – u1 2  GS p + u2 2  GS p – u2 Unpredictable 4  CS u1  6 probes 12  CS u1 – 4  CS u1 – 2  GS p + u1 4  CS u2  12  CS u2 – 4  CS u2 – 2  GS p – u1 12  US (during ITI) 4  US (during ITI) 2  GS p + u2 2   GS p – u2 CS,conditionedstimuli;GS,generalizationstimuli;US,unconditionedstimulus. Note: Conditionswererunwithinsubjects.CS p+  andCS p –,respectively,refertothemovementthat is followed by the pain-US and the movement that is never followed by the pain-US in the predictable context, whereas CS u1  and CS u2  both refer to movements that arenever followed by the pain-US in the unpredictable context. GS movements are novel diagonal movements that have either one feature in common with the srcinal CS p +[GS p + u1  and GS p + u2  ] or the srcinal CS p – [GS p – u1  and GS p – u2 ]. GSs are never reinforced (ie, generalization test under extinction). The suffix ‘‘only’’ is used to indicatenonreinforcement of the CS p + movement (ie, during the practice phase).274  A. Meulders, J.W.S. Vlaeyen/PAIN   154 (2013) 272–282  Author's personal copy of 8 trials were run. Startle probes were delivered following thesame timing as during acquisition.  2.3.6. Generalization phase Theprocedureof the generalizationphase wasmainlythesameas the transfer of acquisitionphase. The difference was that partic-ipants now had to perform 4 novel diagonal movements (GSs),which each have a feature in common with either the srcinalCS p + or the srcinal CS p  , namely left-top, right-top, left-bottom,orright-bottom.Again,50msaftertrialonset,aredasterisk( ⁄ )ap-peared for 500ms in one of the corners of the screen to signalwhich movement had to be performed in randomized order. Aftersuccessfully performing a movement, a post-GS ITI of 8secondsfollowed (cfr. timing acquisition). On each trial, a startle probewas delivered during the GS movement and no pain-USs weredelivered. The 4 GS movements were performed 2 times in eachexperimental context (predictable vs. unpredictable); the orderwas randomized across participants.  2.4. Manipulation checks and outcome variables 2.4.1. Manipulation checks 2.4.1.1. Retrospective US-expectancy.  As a manipulation check, weassessed retrospective US-expectancy after the entire experiment.Participants indicated for both CS movements in each context howmuch they expected the painful stimulus to occur on an 11-pointLikert scale (range 0-10) with labels  not at all  to  very much .  2.4.1.2. Online US-expectancy during transfer of acquisition.  Dur-ing the transfer-of-acquisition phase, participants indicated before each movement   to what extent they expected the pain-ful stimulus to occur when performing the ‘‘ signaled ’’ move-ments (CSs) on an 11-point Likert scale (range 0-10) withlabels  not at all  to  very much . That way, we could assesswhether the contingencies learned during the acquisitionphase using the  voluntary movement set-up  transfer to the  sig-naled movement set-up .  2.4.1.3. SAM ratings of unhappiness, arousal, and control.  After theexperiment,theparticipantsalsofilledout3Self-AssessmentMan-ikin scales (SAM) [3], measuring (un)happiness, arousal, and thecontrol they experienced when performing the respective CSmovements. These self-assessment scales each consisted of 5 dif-ferent pictographs and were accompanied by the following ques-tions: ‘‘ How (un)happy did you feel when performing the left/right/ upward/downward movement?,’’ ‘‘How excited/calm where you when performing the left/right/upward/downward movement?,’’   and  ‘‘Towhat extent did you feel in control of the situation when performing  Fig. 1.  Schematic overview of the experimental task in the (A) predictable context and (B) unpredictable context during the acquisition, the transfer of acquisition and thegeneralization phases.  Note:  The white ‘‘+’’ serves as the starting signal to initiate the voluntary movements during the acquisition phase. During the transfer of acquisitionand the generalization phases, the order of the movements is no longer chosen freely, a red ‘‘ ⁄ ’’indicates which CS/GS (diagonal) movement ought to be performed. Blue-coloredsegmentsofthecounterbarsrepresentthenumberofperformedmovementsandwhite-coloredsegmentsofthecounterbarsindicatethemovementsthatstilloughttobeperformed.CSp+andCSp,respectively,refertothemovementthatisfollowedbythepain-US(ie,left)andthemovementthatisneverfollowedbythepain-US(ie,right)in the predictable condition, whereas CSu1 and CSu2 both refer to movements that are never followed by the pain-US in the unpredictable condition (ie, upwards anddownwards). GS movements are novel diagonal movements that have either one feature in common with the srcinal CSp+ [GSp+u1 and GSp+u2 ] or the srcinal CSp  [GSp  u1 and GSp  u2]. CS, conditioned stimuli; GS, generalization stimuli.  A. Meulders, J.W.S. Vlaeyen/PAIN   154 (2013) 272–282  275
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