Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
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Generalization of pain-related fear using a left-right hand judgment conditioning task
Ann Meulders1, 2, Daniel S. Harvie3, G. Lorimer Moseley3, & Johan W.S. Vlaeyen1, 2, 4
1
2
Research Group on Health Psychology, University of Leuven, Leuven, Belgium
Center for Excellence Generalization on Research in Health and Psychopathology, University of
Leuven, Leuven, Belgium
3
Sansom Institute for Health Research, University of South Australia, Adelaide, Australia
4
Department of Clinical Psychological Science, Maastricht University, The Netherlands
Key words: pain-related fear; fear conditioning; fear generalization; motor imagery; laterality
judgment
Number of figures/tables: 6 figures, 1 table
Correspondence concerning this article should be addressed to Ann Meulders, Ph.D, Department of
Psychology, University of Leuven, Tiensestraat 102, box 3726, 3000 Leuven, Belgium. E-mail:
ann.meulders@ppw.kuleuven.be, T: +32 (0)16 32 60 38, F: +32 (0)16 32 61 44. Ann Meulders is
supported by a Postdoctoral Research Grant of the Research Foundation-Flanders, Belgium (FWOVlaanderen) – ID: 12E3714N, and an EFIC-Grünenthal Research Grant – E-G-G ID: 169518451.
G. Lorimer Moseley is supported by an NHMRC Principal Research Fellowship – ID: 1045322.
Johan W.S. Vlaeyen is supported by an Odysseus Grant ‘‘The Psychology of Pain and Disability
Research Program’’ of the Research Foundation-Flanders, Belgium, (FWO-Vlaanderen) – ID:
G090208N. This study was also supported by an NHMRC Grant – ID: 1047317. The authors would
like to thank Jeroen Clarysse for his technical assistance.
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
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Abstract
Recent research suggests that the mere intention to perform a painful movement can elicit painrelated fear. Based on these findings, the present study aimed to determine whether imagining a
movement that is associated with pain (CS+) can start to elicit conditioned pain-related fear as well
and whether pain-related fear elicited by imagining a painful movement can spread towards novel,
similar but distinct imagined movements. We proposed a new experimental paradigm that integrates
the left-right hand judgment task (HJT) with a differential fear conditioning procedure. During
Acquisition, one hand posture (CS+) was consistently followed by a painful electrocutaneous
stimulus (pain-US) and another hand posture (CS-) was not. Participants were instructed to make
left-right judgments, which involve mentally rotating their own hand to match the displayed hand
postures (i.e. motor imagery). During Generalization, participants were presented with a series of
novel hand postures with six grades of perceptual similarity to the CS+ (generalization stimuli;
GSs). Finally, during Extinction, the CS+ hand posture was no longer reinforced. The results
showed that (1) a painful hand posture triggers fear and increased US-expectancy as compared to a
non-painful hand posture, (2) this pain-related fear spreads to similar but distinct hand postures
following a generalization gradient, and subsequently, (3) it can be successfully reduced during
extinction. These effects were apparent in the verbal ratings, but not in the startle measures.
Because of the lack of effect in the startle measures, we cannot draw firm conclusions about
whether the “imagined movements” (i.e. motor imagery of the hand postures) gained associative
strength rather than the hand posture pictures itself. From a clinical perspective, basic research into
generalization of pain-related fear triggered by covert CSs such as intentions, imagined movements
and movement-related cognitions might further our understanding of how pain and fear avoidance
spread and persevere.
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
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Introduction
According to contemporary fear-avoidance models, pain-related fear plays a pivotal role in the
development and maintenance of chronic pain and disability (Crombez, Eccleston, Van Damme,
Vlaeyen, & Karoly, 2012; Vlaeyen & Linton, 2000, 2012). Accumulating evidence, mostly from
studies in patients with musculoskeletal pain, demonstrates that fear of movement-related pain is
associated with restricted physical performance, more functional disability, sickness absence, and
work loss, and that pain-related fear is often more disabling than the pain itself (Crombez, Vlaeyen,
Heuts, & Lysens, 1999; Zale, Lange, Fields, & Ditre, 2013). In addition, systematic reviews of the
literature suggest that avoidance of feared movements and activities is involved in the maintenance
of chronic pain rather than it is linked to poor prognosis in early stages of musculoskeletal pain
(Pincus, Burton, Vogel, & Field, 2002; Pincus, Vogel, Burton, Santos, & Field, 2006). Recent
evidence suggests that pain-related fear can be acquired through associative learning (Meulders,
Vansteenwegen, & Vlaeyen, 2011). That is, by virtue of the acquired propositional knowledge
between initially neutral stimuli (conditioned stimulus; CS) and pain (unconditioned stimulus; US)
(Rescorla & Wagner, 1972), these stimuli may start to elicit defensive responses such as fear and
avoidance (conditioned response; CR). For example, movements associated with (increased) pain
tend to be avoided, leading to increasing disability in the long run.
Interestingly, a recent study has shown that even the mere intention to perform a painful
movement can elicit pain-related fear (Meulders & Vlaeyen, 2013b). The intention to move (i.e.
motor intent) and imagined movement (i.e. motor imagery) share common cortical neural
mechanisms (i.e. pre-motor and pre-frontal activation) and measurable physiological responses (i.e.
changes in heart rate) (Decety, 1996; Jeannerod, 1994). It seems reasonable to predict then, that
imagining a painful movement might evoke pain-related fear. Support for this idea comes from
research in patients with complex regional pain syndrome (CRPS), showing that imagined
movements increased pain and swelling in the painful limb, even though there was no measurable
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
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movement or muscle activity (Moseley, 2004b; Moseley et al., 2008). We contend that such an
observation implies that pain-related fear may become conditioned to imagined movements, just as
it does to the intention to move.
The idea that Pavlovian conditioning may contribute to the development and maintenance of
chronic pain is not new. Fordyce (Fordyce, 1976) was the first to propose its role; however the
focus quickly shifted to the effect of reinforcement on pain behavior (operant conditioning). That
is, successful escape or avoidance of situations, movements, and activities that induce fear and
possibly pain can be instrumentally reinforced, and as a consequence the occurrence of these
behaviors will be intensified and maintained (Fordyce et al., 1973; Fordyce, Shelton, & Dundore,
1982; McCracken & Samuel, 2007; Philips, 1987).
Under normal circumstances pain-related fear would extinguish after healing, when individuals
learn that the CS is no longer followed by the painful US. The power of operant conditioning and
learned non-use/avoidance, however, may prevent this extinction from occurring (Philips, 1987;
Taub, Uswatte, Mark, & Morris, 2006). That is, when avoidance/non-use is established,
spontaneous exposure to the CS, which might disconfirm the CS-US association, is prevented.
Furthermore, it is clinically apparent that highly fearful chronic pain patients avoid not only
movements and activities that were associated with (increased) pain, through direct experience, but
also movements and activities that have not been associated with an initial pain episode.
Contemporary models of classical fear conditioning offer a possible explanation for this
observation. That is, under certain circumstances, novel stimuli that have features in common with
the original fear-eliciting CS may come to evoke a similar CR. By and large, this mechanism,
referred to as stimulus generalization (Ghirlanda & Enquist, 2003; Honig & Urcuioli, 1981; Kalish,
1969), is highly adaptive because a healthy balance between discrimination and generalization may
assist in avoiding harm in a dynamic environment. Yet, a disturbed balance may give rise to
maladaptive defensive behaviors, which is consistent with the persistent and undesired avoidance
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
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behavior observed in chronic pain. In our opinion, research into generalization of pain-related fear
triggered by covert CSs such as intentions, imagined movements and movement-related cognitions
might further our understanding of how pain and fear avoidance spread and persevere.
In order to investigate the acquisition and generalization of fear of imagined movements, we
integrated the left-right hand judgment task (HJT) with a differential fear conditioning procedure.
During the acquisition phase, one hand posture picture (CS+) was consistently followed by a
painful electrocutaneous stimulus (pain-US) and another hand posture picture (CS-) was not.
Participants were instructed to judge whether the hand was a left or a right hand. This task involves
mentally moving one’s own hand to match the posture of the hand shown in the image (Parsons,
2001). CS hand posture pictures were presented in four different orientations to maximize the
chances that the imagined hand postures, and not the geometric features of the picture, would be
associated with the painful outcome. During the generalization phase, participants were presented
with a series of novel hand postures with six grades of perceptual similarity to the CS+
(generalization stimuli; GSs), which were presented in the same four orientations. During the HJT,
we collected anticipatory US-expectancy ratings, anticipatory pain-related fear ratings, and response
latency for the laterality judgments. We also measured eyeblink startle responses while participants
made judgments (i.e. motor imagery) and in between judgments (inter-trial interval; ITI). We
predicted (a) higher US-expectancy and pain-related fear ratings, as well as higher startle responses
for the CS+ than the CS- hand postures and, (b) faster response latencies for left-right judgments for
the CS+ hand postures than for the CS- hand postures (indicative of an attentional threat bias)
during acquisition. We further predicted (c) that these differences in conditioned responding would
disappear during the extinction phase, and (d) generalization gradients characterized by higher USexpectancy and pain-related fear ratings for the novel hand pictures that are more similar to the
original CS+ than to the original CS-, and a similar gradient for the startle eyeblink and response
latency.
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
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Methods
Participants
Fifty healthy participants (41 females; Mage = 22 years, SDage = 4.23, rangeage = 18–46) were
recruited by means of flyers and through the university “Experimental Management System”
(EMS). Volunteers were paid 12€ or given course credit where applicable and preferred.
Participants were psychology students (n=23), non-psychology university students (n=25) and
working members of the community (n=2). Participants completed a health checklist to ensure they
did not suffer from respiratory, cardiovascular or neurological disease and that they were free from
chronic pain, psychiatric disorders, other minor or major illnesses or pregnancy. Additional
exclusion criteria were uncorrected hearing problems and hand pain. The experimental protocol was
approved by the Ethical Committee of the Faculty of Psychology and Educational Sciences of the
University of Leuven (registration number: S-55840) and the Medical Ethical Committee of the
University Hospital of the University of Leuven (registration number: ML9745). All participants
signed the informed consent form and participants were informed that they were allowed to
withdraw from the experiment at any time.
Stimulus materials and measures
The experiment was programmed in Affect 4.0 (Spruyt, Clarysse, Vansteenwegen, Baeyens,
& Hermans, 2010) and run on a Windows XP (Microsoft Corporation Redmond, WA, USA)
computer (Dell Optiplex 755; Dell Inc., Round Rock, TX, USA) with 2GB RAM and an Intel Core
2 Duo processor (Intel, Santa Clara, CA, USA) at 2.33 GHz and an ATI Radeon 2400 graphics card
(Advanced Micro Devices, Sunnyvale, CA, USA) with 256 MB of video RAM. We used
(implicitly) imagined movements as conditioned stimuli (CS). To create these imagined
movements, we employed a computerized left-right judgment task (HJT) (Parsons, 1987; Parsons et
al., 1995), a task in which participants are prompted to judge whether a certain hand picture created
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
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with Poser (Smith Micro Software, Productivity and Graphics Division, Watsonville, CA, USA), a
3D animation program, depicts a left or a right hand. To make this judgment, (healthy) people use a
set of mental rotations that closely match the operations required for actual hand movements, a
process known as “motor imagery”. Evidence has accumulated pointing to a tight similarity
between properties of motor imagery and actual movement execution ((Parsons, Gabrieli, Phelps, &
Gazzaniga, 1998). Furthermore, evidence stemming from neuroimaging studies suggests that
comparable brain activation is observed during mental rotation and motor execution (Decety et al.,
1994; Gerardin et al., 2000). When participants judge whether the depicted hand is left or right, they
typically 1) make an initial judgment, 2) mentally rotate their own body part into the postures of the
image, 3) and then confirm or reject their initial judgment. As a result, we can assume that the
imagined movement and resulting imagined end posture is unique to the posture of the depicted
hand. Based on this knowledge, we decided to use such picture-specific motor imagery to create the
distinct covert conditioned stimuli (CS+ and CS-), generalization stimuli (GS) and distractor stimuli
(DS) (see Figure 1). The CS+ and CS- were hand postures at the extremes of hand flexion and
extension. Whether the flexed or extended hand acted as the CS+ was counterbalanced amongst
participants. Distractor hands were included to prevent the task from being too simple. The GS hand
postures were six hand pictures with decreasing perceptual similarity with the CS+ and increasing
similarity with the CS- hand postures, whereas the DS were functionally distinct hand postures. In
order to associate the imagined movement with the pain-US while restricting the salience of the
mere visual (i.e. geometric) properties of the hand picture, each hand picture was presented in four
different (3-dimensional) orientations (two medial and two lateral orientations, with each
orientation of the CS+ and CS- presented once within each experimental block). The US was a
painful electrocutaneous stimulus (2-ms duration), which was administered via a commercial
constant current stimulator (DS7A, Digitimer, Welwyn Garden City, England) through 8 mm
surface electrodes (Sensor Medics, Homestead, FL, USA), which were filled with K-Y gel
(Johnson & Johnson, New Brunswick, NJ, USA). The stimulation electrodes were attached to the
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
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right ankle, so that participants could operate the response box and computer mouse freely with
their hands. The electrocutaneous stimulus was set using a calibration procedure consisting of a
series of electrical stimuli of increasing intensity. Participants were asked to indicate how painful
each electrical stimulus was on a 1–10 numerical rating scale where 1 means: ‘‘you feel something
but this is not painful, it is merely a sensation’’; 2 means: ‘‘this sensation starts to be painful, but it
is still a very moderate pain’’; up to 10, which means: ‘‘the worst tolerable pain’’. A subjective
stimulus intensity of 8, which refers to a stimulus that is ‘‘significantly painful and demanding some
effort to tolerate’’ was targeted. The mean physical stimulus intensity chosen during the calibration
procedure was 33.94 mA (SD = 15.92, range = 8–70); participants rated this stimulus intensity as
8.02 (SD = 0.14, range = 8–9) on the painfulness scale from 1–10 confirming that the selected
stimulus was “significantly painful and demanding some effort to tolerate”.
Conditioned fear of pain-related imagined movement was measured through startle eyeblink
reflex modulation and self-reports. The startle reflex is a full-body reflex involved in defensive
response mobilization. It is very short latency reflex triggered by startle-evoking stimuli (e.g.,
acoustic startle probe) and is mediated by a brainstem and spinal cord pathway, which is directly
and indirectly connected to the amygdala. Electromyographic (EMG) activity of the orbicularis
oculi, the muscles underneath the eye, triggered by an acoustic startle probe is often used to
measure the eyeblink component of the startle response. Startle modulation refers to the increase or
potentiation of the startle reflex during fear states elicited by the anticipation of an aversive stimulus
(e.g., an electrocutaneous stimulus). In the present setup, the startle probe was a 100 dB(A) burst of
white noise with instantaneous rise time presented binaurally for 50 ms through headphones. The
magnitude of the eyeblink startle responses elicited by the startle probe during imagined movements
(i.e., while the participant mentally rotated their hand in in order to make the left-right judgment)
served as an index of stimulus-specific pain-related fear. The magnitude of the eyeblink startle
responses elicited by startle probes during the inter-trial interval (ITI) served as an index of
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
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contextual pain-related fear. Note that in this experiment no pain-USs were delivered during the ITI
and thus the context was technically safe. Therefore, we expected low startle responses during the
context and thus little or a lack of contextual fear. We measured latency and accuracy of the leftright hand judgments using a custom-made response box with two buttons connected via the
parallel port of the computer.
Procedure
In a within-subjects experimental design, the left-right hand judgment task (HJT) was
combined with a differential human fear conditioning procedure. The experiment was conducted
during a single 80-minute session. The experiment consisted of several phases: Preparation,
Practice, Habituation, Acquisition, Generalization, and Extinction. During Acquisition, participants
were presented with hand pictures in different postures and they were told that their main task was
to judge whether the depicted hand was a left hand or a right hand. They gave their judgments by
pressing the corresponding button on the response box. During Acquisition, one of these hand
postures was consistently followed by the pain-US (CS+), and another hand posture (CS-) was not.
The CS+ and CS- hand postures were at opposite ends of the physiological range of the hand
flexion-extension continuum. For half of the participants the extreme flexed hand posture was the
CS+ and the extreme extended hand posture as the CS-. For the other half of the participants, these
postures were reversed.
Preparation
Participants were informed (orally and in writing) that painful electrocutaneous stimuli
(pain-US) and loud noises (acoustic startle probes) would be administered during the experiment.
After providing informed consent, participants entered the experimental room. The electrodes for
eyeblink startle responses were placed on the left side of the face according to the site specifications
proposed by Blumenthal et al.(Blumenthal et al., 2005). Prior to the attachment of electrodes, the
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
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skin was scrubbed using exfoliating peeling cream to reduce inter-electrode resistance. Following
this, the electrical stimulation electrodes were attached to outside of the right ankle (lateral
malleolus) using adhesive collars and the stimulus intensity was set using the previously described
procedure (see section “Stimulus materials and measures”).
Practice
Before starting the combined left-right hand judgment conditioning task, we included a
practice phase to train participants to determine “as quickly and accurately as possible” whether a
certain hand picture displayed on screen was a left hand or a right hand. During this phase,
participants were shown two blocks of 20 hand pictures that were distinct from those used during
the experiment. No acoustic startle probes or pain-USs were presented. Participants who failed to
achieve 80% accuracy in the second block, repeated the practice blocks (each time consisting of 20
different hand pictures) until they achieved 80% or better. 94% of the participants went through 2
practice blocks (of 20 trials) to fulfill the task performance requirements (Mblock1 = 16.02, SDblock1 =
3.04, range = 4–20; Mblock2 = 17.44, SDblock2 = 1.79, range = 12–20); whereas 6% needed one extra
practice block (Mblock3 = 17.33, SDblock3 = 1.53, range = 16–19).
Habituation
Since the first acoustic startle probes typically elicit disproportionately high startle
responses, a habituation phase, consisting of eight trials of 15s with an ITI of 5s, was included.
During each 15-s trial, the acoustic startle probe was presented at a random moment between 2-7s
(4 trials) or between 8-13s (4 trials). During this phase, the participants wore headphones and the
lights in the lab were dimmed.
Acquisition
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
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The acquisition phase comprised three blocks of 16 trials, each block consisted of 4 CS+
presentations, 4 CS- presentations, and 8 DS presentations. Before starting the experiment, the
participants received written instructions about the left-right hand judgment task. Each trial began
with the presentation of a fixation cross “+”, prompting the participant to focus his/her attention.
After 2500 ms, a hand picture was presented in the middle of the computer screen until a left-right
judgment was made. If no judgment was made within 5000 ms after the presentation of the picture,
a “no response” judgment was recorded and the trial was aborted. Once the hand picture had
disappeared, the 10000 ms ITI commenced. During acquisition blocks 1 and 2, one startle probe
was presented on each trial, either during the mental rotation of the hand picture or during the ITI.
Normative data suggests that a left-right judgment response takes on average 1.5-2s (Wallwork et
al., 2013). Thus, in order to ensure fear was measured during the imagined movement (and not
during decision making and motor responding), startle probes were delivered 500 ms after picture
onset. In trials containing an ITI probe, the probe was delivered 5000 ms after the end of the
previous trial (when the picture disappeared from the screen). In half of the trials, participants were
asked to give US-expectancy (“How much do you expect the shock to occur?”) and fear ratings
(“How fearful are you at this moment?”). These questions were presented on the screen
immediately after the left-right judgment and participants responded on an 11-point (0-10)
numerical rating scale anchored at left with “not at all” and at right with “very much”. On such
question trials, the hand picture remained on screen until the questions were answered. After
participants gave their fear and US-expectancy ratings, the picture disappeared and the ITI was
initiated. On CS+ trials without any question, the pain-US was delivered immediately after the
laterality judgment (100% reinforcement). If a “no response” was recorded on a CS+ trial, the hand
picture automatically disappeared and the pain-US was administered. On CS+ trials with questions,
the pain-US was delivered immediately when the questions were answered and the image was
withdrawn. Within each block hand pictures were presented in semi-randomized order, with the
restriction that no more than two hand pictures of the same stimulus type (CS+, CS- or DS) could
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
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be presented successively and hand pictures, startle probes and fear and US-expectancy ratings were
presented with the restriction that each hand laterality (left and right) and stimulus type was equally
distributed in the EMG startle data and self-report measures. Participants were not informed about
the contingencies between motor imagery of the hand postures pictures (CSs) and the pain-US. In
the third acquisition block fear and US-expectancy ratings were presented on each trial in order to
prepare the participants for the generalization phase in which anticipatory ratings were collected
during each stimulus presentation as well.
Generalization
During the generalization phase, the procedure was largely identical to the last acquisition
block. The difference was that participants now had to perform mental rotations of hand pictures in
six novel hand postures. These hand postures varied in perceptual similarity between the CS+ and
the CS- and again were presented in four orientations. The generalization phase consisted of 2
blocks of 10 trials consisting of presentations of the original CS+ and CS-, each GS (1-6) as well as
two DS presentations. These stimuli were presented in a semi-randomized order with the restriction
that no more than two consecutive trials could be of the same laterality (left or right), stimulus type
(CS+, CS-, GS and DS) and orientation (medial or lateral) across the two phases.
Extinction
The procedure during the extinction phase was exactly the same as during acquisition with
the exception that the CS+ was no longer followed by the pain-US.
Manipulation checks
Response accuracy
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
13
Response accuracy provides a method of checking participants were not merely guessing.
We set the criterion a priori, that the 95% CI of response accuracy was greater than 50%, which
would occur due to chance.
Primary outcome variables
Anticipatory US-expectancy and fear of pain ratings
Online US-expectancy and fear of pain were assessed by asking participants to rate to what
extent they expected the painful stimulus to occur, and how fearful they were at a given moment.
Responses to the questions were given on an 11-point (0-10) numerical rating scale with the
anchors “not at all” to “very much”.
Eyeblink startle modulation
Orbicularis oculi EMG activity was recorded with 3 Ag/AgCl electrodes (4 mm diameter;
Sensor Medics) filled with electrolyte gel. The raw signal was amplified by a Coulbourn isolated
bioamplifier (Coulbourn Instruments, Whitehall, PA, USA) with bandpass filter (LabLinc v75–04).
The recording bandwidth of the EMG signal was between 90 Hz and 1 kHz (±3 dB). The signal was
rectified online and smoothed by a Coulbourn multifunction integrator (LabLinc v76–23 A) with a
time constant of 20 ms. The EMG signal was digitized at 1000 Hz from 500 ms before the onset of
the auditory startle probe until 1000 ms after it.
Response latency
Response latency, a marker of attentional threat bias, was defined as the time elapsed from
the presentation of the hand picture until a key press (i.e. left or right button) on the response box
was recorded. “No response” trials (i.e. reaction time > 5000 ms) were discarded.
Experimental setting
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
14
Participants were seated in an armchair 60cm from the screen in a sound-attenuated and
dimly lit room, adjacent to the experimenter’s room. Further verbal communication was possible
through an intercom system and the participants and their physiological responses were observed in
real time by means of a closed-circuit TV installation and computer monitors.
Data extraction and statistical analysis overview
We calculated the peak startle amplitudes, defined as the maximum of the response curve within
21-175 ms after the startle probe onset, using psychophysiological analysis (PSPHA)(de Clercq,
Verschuere, de Vlieger, & Crombez, 2006), a modular script-based program. All startle waveforms
were visually inspected prior to analysis, and technical abnormalities and artifacts were eliminated
using the PSPHA software. Each peak amplitude was scored by subtracting its baseline score
(averaged EMG level between 1 ms and 20 ms after the probe onset). The raw scores were
transformed to z-scores to account for inter-individual differences in physiological reactivity. In
order to optimize the visualization of the startle data and avoid negative values on the Y-axis, Tscores – a linear transformation of the z-scores – were used in the figures. Averages were calculated
for the startle responses elicited during the CSs, DS, GS (1-6) and the ITI per block.
Response latencies from the practice phase were not analyzed. Trials with reaction times < 500
ms (because then the probe presentation would not have been reliably during the motor imagery)
and “no response” trials (i.e. reaction time > 5000 ms) were discarded. Mean response latencies
were calculated for each stimulus type per block.
We carried out a series of repeated measures ANOVAs to test our a priori hypotheses, and we
further scrutinized the effects using planned comparisons. The effect size indication ηp2 is reported
for significant effects. Greenhouse-Geisser corrections were carried out when appropriate.
Uncorrected degrees of freedom and corrected p-values are reported together with ε. All statistical
analyses were run using Statistica 12 (StatSoft, Inc, Tulsa, Okla).
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
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Results
Manipulation checks
Response accuracy
We calculated the number of correct answers per phase for the CS+, CS-, DSs and GSs
(when appropriate). During Acquisition, accuracy was 85% for CS+ postures, 95% CI [74.69,
95.06], 84% for CS- postures, 95% CI [74.05, 94.70], and 83% for DS postures, 95% CI [72.01,
93.49]. During Generalization, accuracy was 89% for the CS+, 95% CI [80.09, 97.91], 89% for the
CS-, 95% CI [80.09, 97.91], 85% for the DS, 95% CI [74.20, 94.80], and 89% for the GSs, 95% CI
[80.13, 97.91]. During Extinction, accuracy was 92% for the CS+, 95% CI [84.04, 99.62], 94% for
the CS-, 95% CI [87.50, 100.83], and 90% for the DS postures, 95% CI [81.24, 98.43].
Primary outcome variables
Anticipatory US-expectancy ratings
Acquisition effects. We conducted a 3 × 3 [Stimulus Type (CS+/CS-/DS) x Block (a1-3)]
RM ANOVA on the US-expectancy ratings for the different hand postures, averaged per acquisition
block (see Figure 3, panel A). There was a significant main effect of stimulus type, F(2, 98) = 5.81,
p < .05, ε = .61, ηp2 = .11, and a significant main effect of block, F(2, 98) = 6.19, p < .01, ε = .75,
ηp2 = .11, indicating that US-expectancy ratings differed depending on whether stimuli where
followed by pain and changed across blocks. Of crucial importance, there was a significant stimulus
type x block interaction, F(4, 196) = 5.84, p < .01, ε = .50, ηp2 = .11, suggesting that the differences
in US-expectancy ratings for both CSs developed differently during the acquisition phase. Planned
comparisons confirmed that participants expected the pain-US more to occur after the CS+ hand
postures than after the CS- hand postures, t(49) = -3.49, p < .01, 95% CI [0.72, 2.69]. In addition,
participants also reported to expect the pain-US to occur more after the CS+ picture than after the
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
16
DS pictures, t(49) = 3.18, p < .01, 95% CI [-2.42, -0.55]. As expected, no significant differences in
US-expectancy ratings were observed between the CS- and the DS, t(49) = -1.31, p = .20, 95% CI [0.12, 0.56].
Generalization effects. To examine generalization of US-expectancy to the novel GS hand
postures, we ran a 2 × 9 [Block (g1-2) x Stimulus Type (CS+/GS1-6/CS-/DS) RM ANOVA (see
Figure 3, panel B). From this analysis a significant main effect of stimulus type, F(8, 392) = 13.47,
p < .001, ε = .28, ηp2 = .22, and a significant main effect of block emerged, F(1,49) = 13.74, p < .01,
ηp2 = .22. There was no block x stimulus type interaction, F < 1. Planned comparisons were used to
further test our a priori hypotheses. In line with our hypothesis, there was a significant linear
decrease in the US-expectancy ratings with decreasing GS similarity to the CS+ in the first
generalization block (g1), F(1, 49) = 15.03, p <.001, as well as in the second generalization block
(g2), F(1, 49) = 18.62, p <.001. The generalization gradient was further supported by multiple
planned comparisons (see Table 1). These comparisons revealed that during both generalization
blocks, the difference in US-expectancy between the CS+ and CS- remained significant, g1: t(49) =
-3.97, p < .001, 95% CI [1.21, 3.71]; g2: t(49) = 4.39, p < .001, 95% CI [1.41, 3.79], as well as the
difference in US-expectancy between the CS+ and DS, g1: t(49) = 4.11, p < .001, 95% CI [1.17,
3.43]; g2: t(49) = 4.36, p < .001, 95% CI [1.31, 3.57]. Again, no such differences were observed
between the CS- and the DS in either of the generalization blocks, g1: t(49) = -0.78 , p = .43, 95%
CI [-0.56, 2.44]; g2: t(49) = -0.66, p = .51, 95% CI [-0.64, 0.32]. Furthermore, during the first
generalization block, the US-expectancy reported in response to the GS1 did not differ from the
CS+ , t(49) = 1.54, p = .13, 95% CI [-0.15, 1.15], and during the generalization second block, there
was no significant difference in US-expectancy ratings between the CS+ and GS1, t(49) = 1.86, p =
.07, 95% CI [-0.06, 1.59] and, the CS+ and the GS2, t(49) = 1.65, p = .11, 95% CI [-0.17, 1.73].
Extinction effects. We carried out a 3 × 3 [Stimulus Type (CS+/CS-/DS) x Block (e1-3)] RM
ANOVA on the US-expectancy ratings for the different hand postures averaged per extinction block
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
17
(see Figure 3, panel A). There was a significant main effect of stimulus type, F(2, 98) = 19.80, p <
.001, ε = .56, ηp2 = .29, and a significant main effect of block, F(2, 98) = 41.64, p < .001, ε = .77,
ηp2 = .46, indicating that US-expectancy ratings differed depending on stimulus type and decreased
across blocks. In line with our expectations, the crucial stimulus type x block interaction emerged,
F(4, 196) = 3.54, p < .05, ε = .67, ηp2 = .07, suggesting that the differences in US-expectancy ratings
for both CSs developed differently during the extinction phase. Furthermore, there was a significant
decline in the differences in US-expectancy for the CS+ vs. CS- from the beginning of the
extinction phase compared with the end of the extinction phase, F(1, 49) = 5.95, p < .05. Planned
comparisons revealed at the beginning of the extinction phase (e1), (a) participants still expected the
pain-US more to occur after the CS+ hand postures than after the CS- hand postures, t(49) = -4.58,
p < .001, 95% CI [1.33, 3.41], (b) they reported to expect the pain-US to occur more after the CS+
picture than after the DS pictures, t(49) = 4.14, p < .001, 95% CI [-3.22, -1.12], and (c) no
significant differences in US-expectancy ratings were observed between the CS- and the DS, t(49) =
-1.24, p = .22, 95% CI [-0.12, 0.52]. Planned comparisons at the end of the extinction phase (e3)
further showed that (a) contrary to our expectations, participants still expected the pain-US more to
occur after the CS+ hand postures than after the CS- hand postures, t(49) = -3.48, p < .01, 95% CI
[0.56, 2.08], (b) they reported to expect the pain-US to occur more after the CS+ picture than after
the DS pictures, t(49) = -3.51, p < .001, 95% CI [-1.89, -0.51], and (c) no significant differences in
US-expectancy ratings were observed between the CS- and the DS, t(49) = -0.85, p = .40, 95% CI [0.17, 0.41].
Anticipatory fear of pain ratings
Acquisition effects. We ran a 3 × 3 [Stimulus Type (CS+/CS-/DS) x Block (a1-3)] RM
ANOVA on the pain-related fear ratings for the different hand postures, averaged per acquisition
block (see Figure 4, panel A). There was a significant main effect of stimulus type, F(2, 98) = 3.52,
p < .05, ε = .66, ηp2 = .07, but no main effect of block, F(2, 98) = 1.76, p = .19, ε = .75. Of crucial
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
18
importance, there was a significant Stimulus Type x Block interaction, F(4, 196) = 7.07, p < .01, ε =
.58, ηp2 = .13, suggesting that pain-related fear developed differently in response to both CSs during
the acquisition phase. Planned comparisons confirmed that participants were more afraid of the CS+
hand postures than the CS- hand postures, t(49) = -3.32, p < .01, 95% CI [0.50, 2.04]. In addition,
participants also were more afraid of the CS+ hand postures than the DS postures, t(49) = 2.68, p <
.01, 95% CI [-1.79, -0.26]. As expected, no significant differences in pain-related fear ratings were
observed between the CS- and the DS, t(49) = -1.80, p = .08, 95% CI [-0.03, 0.52].
Generalization effects. To examine generalization of fear towards the novel GS hand
postures, we ran a 2 × 9 [Block (g1-2) x Stimulus Type (CS+/GS1-6/CS-/DS) RM ANOVA (see
Figure 4, panel B). This analysis yielded a significant main effect of stimulus type, F(8, 392) =
7.86, p < .001, ε = .26, ηp2 = .14, and a significant main effect of block emerged, F(1.49) = 13.74, p
< .01, ηp2 = .22. There was no block x stimulus type interaction, F(8, 392) = 1.22, p = .30. Planned
comparisons were used to further test our a priori hypotheses. In line with previous research using
movements as generalization stimuli, there was a significant linear decrease in the pain-related fear
ratings with decreasing GS similarity to the CS+ in the first generalization block (g1), F(1, 49) =
9.14, p <.01, as well as in the second generalization block (g2), F(1, 49) = 13.42, p <.001. The
generalization gradient was further supported by multiple planned comparisons (see Table 3). These
comparisons revealed that during both generalization blocks, the difference in pain-related fear
between the CS+ and CS- remained significant, g1: t(49) = 2.82, p < .01, 95% CI [0.44, 2.64]; g2:
t(49) = 3.41, p < .01, 95% CI [0.72, 2.76], as well as the difference in pain-related fear reported
between the CS+ and DS, g1: t(49) = 2.99, p < .01, 95% CI [0.46, 2.34]; g2: t(49) = 3.30, p < .01,
95% CI [0.63, 2.61]. Again, no such differences were observed between the CS- and the DS in
either of the generalization blocks, g1: t(49) = -0.66 , p = .51, 95% CI [-0.57, 0.29]; g2: t(49) = 0.63, p = .53, 95% CI [-0.50, 0.26]. Furthermore, during the first generalization block, the painrelated fear in response to the GS1 did not differ from the CS+, t(49) = 0.78, p = .44, 95% CI [-0.28,
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
19
0.64]. There was also no significant difference in fear reported to the GS2, t(49) = 1.29, p = .20,
95% CI [-0.24, 1.12], and the GS3, t(49) = 1.69, p = .10, 95% CI [-0.15, 1.75], as compared with
the CS+. During the generalization second block, contrary to our expectations, there was a
significant difference in pain-related fear triggered by the CS+ and GS1, t(49) = 2.59, p < .05, 95%
CI [0.19, 1.54] but the difference between the pain-related fear elicited by the CS+ and the GS2 did
not differ, t(49) = 0.94, p = .35, 95% CI [-0.50, 1.38].
Extinction effects. We performed a 3 × 3 [Stimulus Type (CS+/CS-/DS) x Block (e1-3)] RM
ANOVA on the pain-related fear ratings for the different hand postures, averaged per extinction
block (see Figure 4, panel A). There was a significant main effect of stimulus type, F(2, 98) =
14.34, p < .001, ε = .55, ηp2 = .23, and a significant main effect of block, F(2, 98) = 45.82, p < .001,
ε = .86, ηp2 = .48, indicating that US-expectancy ratings differed depending on stimulus type and
decreased across blocks. The crucial stimulus type x block interaction was significant, F(4, 196) =
3.09, p = .048, ε = .52, ηp2 = .06, suggesting that the pain-related fear ratings for both CSs
developed differently during the extinction phase. Furthermore, there was a significant decline in
the differences fear elicited by the CS+ and CS- from the beginning of the extinction phase
compared with the end of the extinction phase, F(1, 49) = 4.19, p < .05. Planned comparisons
revealed that at the beginning of the extinction phase (e1), (a) participants were still more afraid of
the CS+ hand postures than of the CS- hand postures, t(49) = -3.87 , p < .001, 95% CI [0.80, 2.52],
(b) they reported more fear of pain for the CS+ hand postures than for the DS hand postures, t(49) =
3.58, p < .001, 95% CI [-2.38, -0.67], and (c) there were no significant differences in pain-related
fear ratings between the CS- and the DS, t(49) = -1.05, p = .30, 95% CI [-0.12, 0.39]. Planned
comparisons at the end of the extinction phase (e3) further showed that (a) contrary to our
expectations, participants were still more afraid of the CS+ hand postures than of the CS- hand
postures, t(49) = -2.79, p < .01, 95% CI [0.25, 1.51], (b) they reported more pain-related fear in
response to the CS+ hand postures than in response to the DS hand postures, t(49) = 3.21, p < .01,
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
20
95% CI [-1.30, -0.30], and (c) there were no significant differences in fear of pain ratings between
the CS- and the DS, t(49) = -0.68, p = .50, 95% CI [-0.16, 0.32].
Eyeblink startle modulation
Acquisition effects. We analyzed the mean startle responses during acquisition using a 3 × 4
[Block (a1-3) x Stimulus Type (CS+/CS-/DS/ITI)] RM ANOVA (see Figure 5). The analysis
comparing psychophysiological fear responding elicited during the mental rotation of the different
hand postures and the ITI revealed significant main effects for stimulus type, F(3, 147) = 14.65, p <
.001, ε = .63, ηp2 = .23, and for block, F(2, 98) = 37.90, p < .001, ε = .78, ηp2 = .44, indicating
habituation - that is, startle responses declined gradually across blocks. As expected, there was a
significant stimulus type x block interaction, F(6, 294) = 3.72, p < .01, ε = .83, ηp2 = .07. In contrast
with our predictions, planned comparisons did not reveal the expected difference between startle
responses elicited during the mental rotation of the CS+ hand postures and those elicited during
mental rotation of the CS- hand postures, F < 1. Based on the visual inspection of Figure 5, we
conducted a post-hoc comparison trying to capture what was driving the interaction effect.
Throughout the acquisition phase, startle responses elicited during the ITI were elevated as
compared to the startle responses elicited during motor imagery (irrespective of the specific
stimulus type: CS+, CS- or DS), F(1, 49) = 21.40, p < .001.
Generalization effects and extinction effects. Because there were no reliable acquisition
effects in the startle eyeblink measures, generalization and extinction effects will not be further
reported.
Response latency
24 of the 50 participants failed to give a left-right judgment within 5000 ms at least once
during the experiment (in total 152 trials). In total, 134/7600 trials were no response trials, which
corresponds with 1.8% of the total trial set. Of these 134 no response trials, 18 were CS- trials
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
21
(±13%), 16 CS+ trials (±12%), 66 DS trials –including 4 different DSs and thus corresponding with
±16% per DS type– (±49%), 6 GS1-2-4-5-6 trials (±4.5% per GS type, ±23% in total), and 4 GS3
trials (±3%). 6 of the 50 participants gave a left-right judgment quicker than 500 ms after the picture
onset at least once during the entire experimental task (in total 152 trials). In total 23/7600 trials
were premature response trials, which corresponds with 0.3 % of the total trial set. Of these 23
trials, 8 were CS- trials (±35%), 6 CS+ trials (±26%), 7 DS trials (±30%), and 2 GS2trials (±9%).
Acquisition effects. We analyzed the mean response latency during acquisition using a 3 × 3
[Block (a1-3) x Stimulus Type (CS+/CS-/DS)] RM ANOVA (see Figure 6). The analysis
comparing response latencies of the laterality judgments for the different type of hand postures
showed a significant main effect for block, F(2, 98) = 5.99, p < .01, ε = .87, ηp2 = .11, but no
significant main effect for stimulus type, F(2, 98) = 3.19, p = .06, ε = .84. The anticipated stimulus
type x block interaction was also not significant, F < 1. Notwithstanding the absence of a significant
interaction, we continued to test our a priori hypothesis. Planned comparisons did not confirm our
hypothesis that participants would be quicker to judge the laterality of the hand postures that
predicted the painful outcome (CS+) than the one that was not predicting the pain-US (CS-), F < 1.
Generalization and extinction effects. Because there were no reliable acquisition effects in
the response latency measure, generalization and extinction effects will not be further reported.
Discussion
Previous research showed that fear of movement-related pain emerges after repeated
pairings of a neutral joystick movement (CS+) with pain (Meulders et al., 2011) and that fear
generalizes selectively to novel joystick movements that resemble the original CS+ movement, but
not to those that resemble the original CS- movement (Meulders, Vandebroek, Vervliet, & Vlaeyen,
2013; Meulders & Vlaeyen, 2013a). Finally, fear of movement-related pain can subsequently be
reduced using a Pavlovian extinction procedure (Meulders & Vlaeyen, 2012). Interestingly, it has
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
22
been demonstrated that even the mere intention to perform a painful movement can function as a
covert conditioned stimulus and can start to elicit pain-related fear and that this fear can
subsequently be reduced through Pavlovian extinction (Meulders & Vlaeyen, 2013b). Based on
these previous findings and the well-documented observation that motor intention and motor
imagery are closely related, it can be argued that even without motor intention or preparation,
imagining a painful movement, might similarly evoke pain-related fear.
First of all, the verbal ratings showed that participants expected the pain-US to occur more after
the CS+ hand posture than after the CS- hand posture. In addition, they also reported being more
afraid of the CS+ hand posture than the CS- hand posture. These results indeed seem to suggest that
pain-related fear can be acquired in response to the hand postures presented in different
orientations. Further, we successfully demonstrated a generalization gradient in both verbal ratings.
More specifically, there was a linear decrease in US-expectancy and self-reported pain-related fear
for the novel generalization hand postures (GSs) approaching the original CS-, with novel hand
postures more similar to the original CS+ eliciting more pain-related fear and US-expectancy than
those more similar to the CS-. Finally, we also found successful extinction of pain-related fear in
both verbal measures. That is, the difference in US-expectancy and pain-related fear ratings
between the CS+ hand posture and the CS- hand posture significantly decreased during extinction.
However, at the end of the extinction phase, participants still expected the pain-US to occur more
and reported more fear of the CS+ hand posture than of the CS- hand posture. These results seem to
suggest that pain-related fear, triggered by hand postures presented in different orientations, was
significantly reduced, but not fully extinguished.
Second, we did not observe acquisition of pain-related fear during motor imagery of hand
postures in the startle eyeblink measures. These results were unexpected and are clearly dissociated
from the findings in the verbal measures. In contrast with our expectations, we observed elevated
startle eyeblink responses elicited by probes during the ITI (i.e. context alone) as compared with the
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
23
responses during mental imagery irrespective of the stimulus type. These results seem to suggest
that instead of affective startle potentiation (Vrana, Spence, & Lang, 1988), our procedure produced
startle inhibition. Previous research on affective modulation of the startle eyeblink response
suggests that an acoustic startle probe, presented at 500 ms after the picture presentation, as we did
here, should not generate inhibition but facilitation of the startle response (Bradley, Codispoti, &
Lang, 2006). However, attentional processes and cognitive load have been shown to affect affective
startle modulation as well (Acocella & Blumenthal, 1990; Filion, Dawson, & Schell, 1993; Schell,
Wynn, Dawson, Sinaii, & Niebala, 2000). As such, it is possible that the cognitive load of the leftright hand judgment task (i.e. participants were mentally rotating their hand into the displayed hand
postures) interfered with the startle modulation and produced inhibition of the startle response. The
observation that the startle responses during the context alone (ITI) were consistently larger than
those occurring during mental imagery of all hand postures is consistent with this possibility.
Because of the lack of effect in the startle measures, we cannot draw firm conclusions about
whether the “imagined movements” (i.e. motor imagery of the hand postures) gained associative
strength rather than the hand posture pictures themselves .
Third, we did not observe any differences in reaction times to give laterality judgments for the
CS+ hand posture as compared with the CS- hand posture. A recent meta-analysis on attentional
bias towards pain-related information revealed an attentional bias of medium effect size (d=0.676)
(Crombez, Van Ryckeghem, Eccleston, & Van Damme, 2013) towards signals of impending
experimental pain in healthy volunteers. The present results do not corroborate those findings. One
possible explanation for the absence of the attentional bias is that left-right judgments typically
consist of different processes (initial judgment, mental imagery and decision making) that sum up to
the total response latency. Therefore, even if the initial identification of the CS+ hand picture was
facilitated, but no differences occur during mental imagery and decision making, the attentional
threat bias might still not be picked up by assessing the complete reaction time of the laterality
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
24
judgment. Of further relevance to this issue is a previous finding that experimentally induced pain
in one hand (Moseley, Sim, Henry, & Souvlis, 2005) , and experimentally induced expectation of
pain in one hand, are associated with a longer response latency for left-right judgments of the other
hand (Hudson, McCormick, Zalucki, & Moseley, 2006). This is the opposite pattern to that
observed in people with complex regional pain syndrome, who take longer to make the left-right
judgments when the picture corresponds with their painful hand (Moseley, 2004a, 2004c, 2005).
These opposing patterns of delay have been attributed to an information processing bias associated
with ambiguous stimuli, such that the bias triggers an erroneous first decision, which is not
confirmed by the motor imagery and a second decision is made, which is then confirmed. Thus,
although there is a side to side delay, it reflects not a slowing down of CNS processing, but an
interpretation bias manifesting in the first stage of the left-right judgment task. It may be then, that,
in the present study, the CS+ and CS- pictures were sufficiently different to avoid such an
interpretation bias and, thus, there was no delay.
Some interesting findings deserve further attention. First, it should be noted that the acquisition
training itself can be interpreted as a type of generalization learning, because the CS+ consisted of
the same hand posture presented in four orientations. As mentioned before, this procedure was
applied to induce motor imagery that is required to perform the task (Decety et al., 1994; Gerardin
et al., 2000; Parsons et al., 1995; Stephan et al., 1995). As a consequence, participants had to
integrate this information and generalize this knowledge across the four orientations of each
stimulus type. Therefore, it is unlikely that the visual image, per se, was conditioned to elicit painrelated fear because the four orientations provide distinct visual images that are difficult to match
without performing the left-right task. Therefore, it is possible that even though participants
engaged in motor imagery, the “imagined movements” themselves did not become conditioned
stimuli, but that participants simply identified the end point hand posture as the predictor of the
painful stimulus. Second, using several orientations offers a likely explanation for the incomplete
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
25
extinction. It is possible that generalization of inhibitory learning (during extinction) from one
orientation to another orientation is more difficult than generalizing the excitatory learning (during
acquisition). Closely related is the well-known dissociation between first and second learned
associations: acquisition learning (first learned association) normally generalizes easily, whereas
extinction learning (second learned association that inhibits the behavioral expression of the first
learned association) does not, although it is more context-dependent (Bouton, 1984, 1988, 1994,
2002).
Interpretation of the current study results should consider some limitations. First of all, there was
no explicit measure to confirm that participants actually engaged in motor imagery to generate the
left-right hand judgments. We only measured response accuracy as an implicit measure of motor
imagery, that is, participants in general gave more correct left-right judgments than expected at
chance level suggesting that they most likely did mentally rotate their own hand in the displayed
hand postures. Future research might include more explicit manipulation checks. Second, because
our startle measures did not replicate the findings observed in the verbal ratings, we cannot firmly
conclude that the US-expectancy and pain-related fear ratings relate to the motor imagery of the
hand postures rather than the visual aspects of the displayed hand postures (unrelated to imagined
movements). As a consequence it should be concluded that the present paradigm is not suitable to
study conditioning of pain-related fear of imagined movements with startle eyeblink measures as a
main outcome. Future research might register event-related potentials (ERP) as a central index of
fear perception during motor imagery (Williams et al., 2004). The recording of event-related
potentials (ERPs) indeed can provide millisecond resolution of the perceptual and decision making
processes that follow stimulus onset (Lim et al., 1999; Ugland, Dyson, & Field, 2013). In general,
previous research has shown that early neural responses (P1, N1 (Wong, Bernat, Bunce, & Shevrin,
1997) and P2 (Wong, Bernat, Snodgrass, & Shevrin, 2004)) may all index aspects of fear
conditioning . Larger amplitudes appear to be broadly characteristic of the CS+ relative to the CS-
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
26
and these effects appear to be robust for later components related to discrimination (N1 and P2)
relative to an earlier P1 component that is often associated with physical stimulus features, attention
and arousal (Olofsson, Nordin, Sequeira, & Polich, 2008). Because these ERP components emerge
in less than 500 ms after stimulus onset, a set-up including such ERP measures might be more
sensitive to pick up differences between the CS+ and CS- in the further study of pain-related fear of
imagined movements.
To conclude, we showed that (1) a painful hand posture triggers fear and increased USexpectancy as compared to a non-painful hand posture, (2) this pain-related fear spreads to similar
but distinct hand postures following a generalization gradient, and subsequently, (3) it can be
reduced using an extinction procedure. These effects were apparent in the verbal ratings, but not in
the startle measures. Additionally, we failed to observe an attentional threat bias towards the painful
hand postures in the response latency of the laterality judgments.
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
27
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Disclosure statement
The authors report no conflict of interest.
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
32
Acknowledgments
Ann Meulders is supported by a Postdoctoral Research Grant of the Research Foundation-Flanders,
Belgium (FWO-Vlaanderen) – ID: 12E3714N, and an EFIC-Grünenthal Research Grant – E-G-G
ID: 169518451. G. Lorimer Moseley is supported by an NHMRC Principal Research Fellowship –
ID: 1045322. Johan W.S. Vlaeyen is supported by an Odysseus Grant ‘‘The Psychology of Pain and
Disability Research Program’’ of the Research Foundation-Flanders, Belgium, (FWO-Vlaanderen)
– ID: G090208N. This study was also supported by an NHMRC Grant – ID: 1047317. The authors
would like to thank Jeroen Clarysse for his technical assistance.
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Figure Captions
Figure 1. Hand pictures used as conditioned stimuli, distractors and generalization stimuli.
Figure 2. Overview of an illustrative trial timing of a CS+ trial. Note that the
represents the
white noise signal used as the acoustic startle probe, the lightning bolt represents the pain-US.
During acquisition and extinction, only one startle probe was delivered per trial, either during
mental rotation of the picture (i.e. cued pain-related pain) or in the ITI (i.e. contextual pain-related
fear). On 50% of the trials, participants rated their anticipatory pain-related fear and US-expectancy
before the pain-US was delivered and/or the ITI was initiated. During the generalization phase, two
startle probes were presented per trial (one during the mental rotation of the picture and one during
the ITI) and pain-related fear and US-expectancy ratings were asked on each trial (100%).
Figure 3. Mean anticipatory US-expectancy ratings A. for the CS+, CS- and distractor stimuli (DSs)
separately during the three acquisition blocks (a1-3), and B. for the CS+ , CS-, the DSs and the six
generalization stimuli (GS1-6) separately during both the generalization blocks (g1-2) (lower
panel). Vertical bars denote standard errors.
Figure 4. Mean anticipatory pain-related fear ratings A. for the CS+, CS- and distractor stimuli
(DSs) separately during the three acquisition blocks (a1-3), and B. for the CS+ , CS-, the DSs and
the six generalization stimuli (GS1-6) separately during both the generalization blocks (g1-2).
Vertical bars denote standard errors.
Figure 5. Mean eyeblink startle amplitudes during the respective hand pictures and the intertrial
interval (ITI) separately during the acquisition phase (a1-3) and the extinction phase (e1-3). Vertical
bars denote standard errors. Note that for graphic purposes T-scores were used.
Figure 6. Mean response latency for the laterality judgments for the respective hand pictures (CS+,
CS- and DS) separately during the acquisition phase (a1-3) and the extinction phase (e1-3). Vertical
bars denote standard errors.
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Table 1.
Effect
t
df
US-expectancy – Generalization Block 1
CS+ vs. CS3.97
49
CS+ vs. DS
4.11
49
CS+ vs. GS1
1.54
49
CS+ vs. GS2
2.86
49
CS+ vs. GS3
3.62
49
CS+ vs. GS4
3.93
49
CS+ vs. GS5
3.73
49
CS+ vs. GS6
3.85
49
US-expectancy – Generalization Block 2
CS+ vs. CS4.39
49
CS+ vs. DS
4.36
49
CS+ vs. GS1
1.86
49
CS+ vs. GS2
1.65
49
CS+ vs. GS3
3.69
49
CS+ vs. GS4
4.44
49
CS+ vs. GS5
4.45
49
CS+ vs. GS6
4.10
49
Fear of pain – Generalization Block 1
CS+ vs. CS2.82
49
CS+ vs. DS
2.99
49
CS+ vs. GS1
0.78
49
CS+ vs. GS2
1.29
49
CS+ vs. GS3
1.69
49
CS+ vs. GS4
2.78
49
CS+ vs. GS5
2.73
49
CS+ vs. GS6
2.33
49
Fear of pain – Generalization Block 2
CS+ vs. CS3.41
49
CS+ vs. DS
3.30
49
CS+ vs. GS1
2.59
49
CS+ vs. GS2
0.94
49
CS+ vs. GS3
3.30
49
CS+ vs. GS4
3.38
49
CS+ vs. GS5
3.50
49
CS+ vs. GS6
3.14
49
Figure 1.
p
95% CI
< .001
< .001
= .13
< .01
< .001
<.001
<.001
< .001
[1.21. 3.71]
[1.17. 3.43]
[-0.15. 1.15]
[0.33. 1.87]
[0.76. 2.64]
[1.06. 3.30]
[1.00. 3.32]
[1.14. 3.62]
< .001
< .001
= .07
= .11
< .001
< .001
< .001
< .001
[1.41. 3.79]
[1.31. 3.57]
[0.06. 1.59]
[0.17. 1.73]
[0.90. 3.06]
[1.36. 3.60]
[1.43. 3.78]
[1.26. 3.70]
< .01
< .01
= .44
= .20
= .10
< .01
< .01
< .05
[0.44, 2.64]
[0.46, 2.34]
[-0.28, 0.64]
[-0.24, 1.12]
[-0.15, 1.75]
[0.37, 2.27]
[0.37, 2.43]
[0.18, 2.46]
< .01
< .01
< .05
= .35
< .01
< .01
< .01
< .01
[0.72, 2.76]
[0.63, 2.61]
[0.19, 1.54]
[-0.50, 1.38]
[0.63, 2.61]
[0.68, 2.68]
[0.76, 2.83]
[0.59, 2.69]
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
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Note – Two hand pictures in 4 distinct presentation angles (2 medial orientations and 2 lateral orientations)
were used as the reinforced (CS+) and the unreinforced (CS-) conditioned stimulus (upper panel) and 4 hand
pictures in 4 presentation angles functioned as distractor (DS1-4) stimuli (middle panel); CS+ and CSpictures were counterbalanced across participants. Six hand pictures of varying similarity with the CS+ to the
CS- served as the generalization (GS1-6) stimuli.
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
36
Figure 2.
0 ms presentation of the fixation cross
2500 ms presentation of hand picture followed by initial left-right judgment;
mental rotation of own hand into target position to verify initial judgment
3000 ms presentation of startle probe (index for cued pain-related fear)
How fearful are you at this moment?
totally not
> 7500 ms participant confirms or rejects initial left-right judgment and presses the
corresponding button on the response box; on question trials (50%) two rating scales
assessing fear of pain-related fear and US-expectancy are presented and responses
registered
very much
After the laterality judgment, the hand picture is withdrawn and pain-US
delivered
After reinforcement on CS+ trials or after the laterality judgment, a 10-s ITI starts
5000 ms presentation of startle probe (index for contextual pain-related fear)
t(ms)
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
37
Figure 3.
A. Anticipatory US-expectancy during acquisition and extinction
7
Mean anticipatory US-expectancy ratings
6
5
4
3
2
CS-
1
CS+
DS
0
a1
a2
a3
e1
e2
e3
B. Anticipatory US-expectancy during generalization
7
Mean anticipatory US-expectancy ratings
6
5
4
3
2
1
g1
g2
0
CS+
GS1
GS2
GS3
GS4
GS5
GS6
CS-
DS
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
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Figure 4.
A. Anticipatory fear of pain during acquisition and extinction
6
Mean anticipatory fear of pain ratings
5
4
3
2
CS-
1
CS+
DS
0
a1
a2
a3
e1
e2
e3
B. Anticipatory fear of pain during generalization
6
Mean anticipatory fear of pain ratings
5
4
3
2
1
g1
g2
0
CS+
GS1
GS2
GS3
GS4
GS5
GS6
CS-
DS
Running head: FEAR GENERALIZATION AND MOTOR IMAGERY
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Figure 5.
65
Mean startle eyeblink amplitudes (T-scores)
CS-
CS+
DS
ITI
60
55
50
45
a1
a2
a3
e1
e2
e3
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Figure 6.
2000
1900
Mean response latency
1800
1700
1600
1500
1400
1300
1200
CS-
CS+
DS
1100
1000
a1
a2
a3
e1
e2
e3