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Pain 136 (2008) 250–261

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Emotional control of nociceptive reactions (ECON):


Do affective valence and arousal play a role?
Jamie L. Rhudy *, Amy E. Williams, Klanci M. McCabe,
Jennifer L. Russell, Lauren J. Maynard
Department of Psychology, The University of Tulsa, 600 South College Avenue, Tulsa, OK 74104, USA

Received 30 November 2006; received in revised form 6 June 2007; accepted 25 June 2007

Abstract

Prior research suggests emotional picture-viewing modulates motoric (nociceptive flexion reflex), autonomic (skin conductance
response, heart rate acceleration), and subjective (pain rating) reactions to noxious electrodermal stimulation. The present study
sought to determine whether emotional valence and arousal contribute to nociception modulation. To do so, pictures varying in
emotional content (erotica, food, neutral, loss, attack) were chosen to manipulate emotional valence (pleasant = erotic and food;
unpleasant = loss and attack) and arousal (low = food and loss; moderate = erotica and attack). Pictures were presented in pseu-
dorandom order to elicit emotional processing while noxious electric stimulations were delivered to the sural nerve. Nociceptive flex-
ion reflex (NFR) magnitude, skin conductance response (SCR), heart rate (HR) acceleration, and subjective pain ratings to each
stimulation were measured, standardized, averaged by picture content, and analyzed. Results suggested that picture-viewing
explained 52% of the variance in the multivariate combination of the nociceptive reactions and modulated them in parallel. Pleasant
pictures inhibited reactions, whereas unpleasant pictures enhanced them. However, only erotica and attack pictures elicited signif-
icant modulation relative to neutral pictures, suggesting arousal also contributed. An exploratory multilevel analysis also supported
this conclusion. Together, these data suggest emotional control of nociceptive reactions (ECON) is associated with a valence-by-
arousal interaction. Implications of these findings for how emotional picture-viewing can be used to study supraspinal modulation
are discussed.
 2007 International Association for the Study of Pain. Published by Elsevier B.V. All rights reserved.

Keywords: Affect; Nociceptive flexion reflex; Heart rate; Skin conductance; Pain perception; Pain modulation

1. Introduction 2007b). Unfortunately, little research has been con-


ducted to elucidate factors that determine the emo-
Emotional processing influences subjective pain (e.g., tion–pain relationship.
de Wied and Verbaten, 2001; Keefe et al., 2001; Mea- We have used motivational priming theory (MPT;
gher et al., 2001; Villemure et al., 2003) and physiologi- Lang, 1995) as a conceptual framework to make predic-
cal reactions to noxious stimulation (nociceptive flexion tions about the influence of emotional processing on
reflex, skin conductance response, heart rate accelera- pain (Rhudy and Meagher, 2001). MPT purports two
tion, cortical potentials) (Kenntner-Mabiala and Pauli, central opponent motive systems are responsible for
2005; Rainville et al., 2005; Rhudy et al., 2005, 2006, emotional processing (Lang and Davis, 2006). The appe-
titive system is activated by appetitive stimuli (e.g., sex,
food) and results in positively valenced emotions. The
*
Corresponding author. Tel.: +1 918 631 2839; fax: +1 918 631
defensive system is activated by harmful or potentially
2833. harmful stimuli (e.g., threat, noxious stimuli) and results
E-mail address: jamie-rhudy@utulsa.edu (J.L. Rhudy). in negatively valenced emotion. Thus, measures of

0304-3959/$34.00  2007 International Association for the Study of Pain. Published by Elsevier B.V. All rights reserved.
doi:10.1016/j.pain.2007.06.031
J.L. Rhudy et al. / Pain 136 (2008) 250–261 251

valence/pleasure have been used to assess which motive of the experiment were described to them. Participants were
system is activated. excluded for: <18 yrs old, cardiovascular, neurological, and/
The imminence of appetitive consummation (appeti- or circulatory problems, recent use of analgesic, anxiolytic,
tive system) or threat (defensive system) determines the or antidepressant medication, psychological trauma as defined
by the DSM-IV (APA, 2000), specific phobia of snakes or spi-
strength/intensity of motive system activation and pro-
ders, or Raynaud’s disease. Twenty-five healthy participants
motes action via metabolic arousal (Bradley, 2000).
(10 male, 15 female) completed the study and were included
Thus, measures of arousal are used to assess the degree in the analyses; however, an additional male participant was
of system activation. Not surprisingly, stimuli with excluded for equipment failure and three others (2 female, 1
greater motivational-relevance, such as sexual objects male) were excluded because a nociceptive flexion reflex could
and threatening stimuli, lead to strong appetitive and not be obtained (see Section 2.6.1). Of the total 29 participants,
defensive system activation (and arousal), respectively most were female (59%), White non-Hispanic (55.2%), single
(Bradley et al., 2001). (89.7%), and unemployed (55.6%), with an average age of
MPT predicts that if a motive system is activated 21.81 yrs (SD = 5.50).
(primed), future responses emanating from that system
will be facilitated, whereas responses from the opposing 2.2. Apparatus
system will be inhibited (Lang, 1995). For example, defen-
sive system activation facilitates subsequent defensive A computer running LabVIEW software (National Instru-
responses, while inhibiting appetitive responses. Further, ments, Austin, TX) equipped with dual monitors and A/D
MPT predicts the degree of system activation determines board (National Instruments, PCI-6036E) controlled all stim-
uli, questionnaire presentation, and data acquisition, and
the degree of facilitation/inhibition (Cuthbert et al.,
was used for offline data reduction. One 1700 flat panel monitor
1996): greater activation = greater modulation. There-
was used by the experimenter to monitor physiological signals
fore, defensive reactions to nociceptive input should be and experimental timing. The other 1700 flat panel monitor
inhibited by appetitive activation (positive emotions) (positioned .5 m from the participant) presented visual stimuli
and facilitated by defensive activation (negative emo- and questionnaires. Electrodermal stimulations were delivered
tions). Moreover, nociception modulation should be by a Grass Instruments stimulator (Model S88, West Warwick,
greater when systems are strongly activated (indirectly RI), stimulus isolation unit (Model SIU8T), constant current
assessed from higher arousal). No single study, however, unit (Model CCU1), and bipolar stimulating electrode (Nico-
has tested this hypothesis by independently manipulating let, 019-401400, Madison, WI). The stimulating electrode
the system activated (valence) and the degree of activation was attached to the left ankle over the retromalleolar pathway
(arousal). Based on MPT, it is predicted that the motive of the sural nerve. The onset/offset of the stimulator was
controlled by computer, and a computer-controlled voltage
system (emotional valence) determines the direction,
regulator varied the current to the participant (max cur-
and emotional activation (arousal) determines the degree,
rent = 40 mA). All psychophysiological signals were sampled
of nociception modulation. at 1000 Hz and collected/filtered using a Grass Instruments
The present study used a picture-viewing paradigm to Model 15LT Bipolar Amplifier with Quad AC (15A54) and
study the emotion–pain relationship. Pictures varying in Dual DC (15A12) modules. Skin conductance response
content (attack, loss/grief, neutral objects, food, erotica) (SCR) was measured using an adaptor (Grass, Model SCA1)
were used to manipulate motive system activation for the 15A12 amplifier and electrodes filled with isotonic paste
(valence: unpleasant, neutral, pleasant) and activation (EC33, Grass Instruments).
level (arousal: low vs. moderate). During picture-view- To apply all EMG, ECG, and stimulating electrodes, first
ing, noxious electric stimulations were delivered to the the skin was degreased with alcohol, slightly abraded using
sural nerve and nociceptive reactions were assessed NuPrep gel to achieve impedances below 10 KX, and then con-
ductive gel (EC60, Grass Instruments) was applied. All record-
(nociceptive flexion reflex, skin conductance response,
ing electrodes were Ag–AgCl. Psychophysiological signals
heart rate acceleration, subjective pain). It was predicted
were sampled in 11 s trials: 3 s before picture presentation
that unpleasant pictures would facilitate nociceptive and 8 s after picture onset. Throughout testing, participants
reactions and pleasant pictures would inhibit them were seated in a recliner with a small pillow positioned under
(Rhudy et al., 2005, 2006, 2007b). However, modulation their left ankle to facilitate relaxation. Sound attenuating
was expected to be greatest during erotic and attack pic- headphones and a video camera allowed the experimenter to
tures because they elicit the greatest activation/arousal. communicate with and monitor the participant from an adja-
cent room.
2. Method
2.3. Emotion-induction: picture-viewing
2.1. Participants
Emotion elicited by picture-viewing has been shown to reli-
All procedures were fully approved by The University of ably alter pain and nociception (de Wied and Verbaten, 2001;
Tulsa Ethics Review Board and participants recruited from Meagher et al., 2001; Wunsch et al., 2003; Kenntner-Mabiala
the psychology department gave informed consent after details and Pauli, 2005; Rhudy et al., 2005, 2006, 2007b). Therefore,
252 J.L. Rhudy et al. / Pain 136 (2008) 250–261

60 digital pictures1 from five picture contents (12 pictures per across picture content and picture duration. Therefore, six
content) were chosen from the International Affective Picture stimulations were delivered during each picture content. To
System (CSEA, 1999; Lang et al., 1999) that should manipu- minimize conditioning to the pictures, 10 stimulations were
late emotional valence and arousal. Valence was manipulated also delivered during randomly chosen inter-picture intervals,
by two pleasant picture contents (couples in erotic poses, for a total of 40 stimulations during the picture-viewing
food), two unpleasant picture contents (depictions of loss/ procedure.
grieving, animal and human attack scenes), and neutral pic-
tures (household objects, mushrooms). Erotic and attack pic-
ture contents were chosen to elicit moderate motive system 2.4. Subjective reactions to picture-viewing
activation and arousal, whereas food and loss contents were
chosen to elicit low motive system activation and arousal. Subjective emotional evaluations of pictures were assessed
Mean normative valence/pleasure and arousal ratings for each using the Self-Assessment Manikin (SAM; Bradley and Lang,
picture content were: erotic couples (valence: M = 6.66, arou- 1994). The SAM is a two item questionnaire that consists of
sal: M = 6.10), food (valence: M = 6.88, arousal: M = 4.82), two sets of five pictographs depicting affective valence/pleasure
neutral (valence: M = 4.93, arousal: M = 2.53), loss (valence: (unpleasant–pleasant) and arousal (calm-excited). A comput-
M = 2.65, arousal: M = 4.56), and human and animal attack erized version of the SAM was used to rate affective valence
(valence: M = 3.00, arousal: M = 6.35) (See section entitled and arousal following each picture (Rhudy et al., 2005). To
‘‘Subjective reactions to picture-viewing’’ below for description respond, participants dragged an indicator on or between
of rating scales) (Lang et al., 1999). Thus, pictures containing any of the five pictographs for each scale and submitted their
erotic and food contents were roughly equivalent in normative answers by computer mouse. This yielded ratings between 1
pleasure/valence ratings, as were attack and loss contents. and 9 for each dimension, with higher scores indicating greater
Moreover, erotic and attack contents were roughly equivalent pleasure or arousal, depending on the scale. Pictures were
in normative arousal ratings, but higher than loss and food expected to vary in emotional valence, with erotic and food
contents which were roughly equivalent. Therefore, pictures pictures eliciting the greatest pleasure, neutral pictures inter-
containing erotica, food, loss, and attack contents were chosen mediate, and loss and attack pictures the least pleasure (Lang
to independently manipulate affective valence and arousal, and et al., 1999). Erotic and food pictures were expected to elicit
neutral pictures served as controls.2 Pictures were presented by equivalent pleasure, whereas loss and attack were expected
computer in a dimly lit room. The order of presentation was to elicit equivalent displeasure (low pleasure). Arousal was
randomized across participants with the limitation that not expected to be highest in response to erotic and attack pictures,
more than two pictures of similar content were shown consec- intermediate for food and loss, and lowest for neutral (Lang
utively. Picture duration was also manipulated. Half of the pic- et al., 1999).
tures were presented for 500 ms and the other half 6 s
(duration balanced across content) because these durations 2.5. Psychophysiological reactions to picture-viewing
have been shown to effectively modulate the defensive acoustic
startle reflex (Codispoti et al., 2001). Picture duration did not In paradigms using picture-viewing to evoke emotions, psy-
have a significant influence on nociceptive reactivity; thus, the chophysiological reactions are typically used in conjunction
picture duration IV was removed from the final statistical with subjective reactions to verify emotion-induction. SCR is
models predicting nociceptive outcomes. used as a physiologic correlate of subjective arousal and HR
To examine the effect of picture-viewing on nociceptive as a correlate of subjective valence (Lang et al., 1993; Bradley
reactions, electric stimulations at 120% NFR threshold (see et al., 2001). However, we have failed to observe these picture-
Section 2.6.1) were delivered randomly during 50% of pictures, evoked ANS responses when shocks are delivered throughout
with the limitation that stimulations were equally distributed picture-viewing, even from pictures not receiving a shock
(Rhudy et al., 2005, 2006). We argue this is likely due to the
masking of subtle picture-evoked ANS reactions when pictures
1
Image numbers were: erotic couples (4607, 4611, 4651, 4666, 4669, are viewed in a threatening context (i.e., during randomly
4670, 4690, 4810, 4606, 4608, 4623, 4653), food (7230, 7270, 7283, delivered shocks) (Rhudy et al., 2005, 2006). Nonetheless,
7320, 7330, 7350, 7390, 7400, 7430, 7450, 7470, 7475), neutral (7000,
these measures were recorded and analyzed to facilitate com-
7004, 7010, 7025, 7030, 7040, 7080, 7090, 7150, 7175, 7235, 5531), loss
(2141, 2205, 2276, 2455, 2700, 2800, 2810, 2900, 9000, 9001, 9220,
parisons with other picture-viewing studies. However, we do
9421), and human and animal attack scenes (1052, 1111, 1205, 1301, not predict SCR or HR will covary significantly with subjective
1525, 1932, 3500, 6230, 6242, 6250, 6550, 6560). arousal or valence, respectively.
2
Although these picture contents were chosen to independently SCR was measured by placing electrodes filled with isotonic
manipulate emotional valence and arousal, it must be pointed out that paste (EC33, Grass Instruments) on the volar surface of the
valence and arousal manipulations are by definition confounded with middle and ring fingers after participants washed and dried
picture content. Thus, it is possible that modulatory differences noted their hands (Venables and Christie, 1980). Electrocardiogram
between attack and loss, or erotic and food contents may reflect (ECG) was measured using Ag–AgCl electrodes that were
differences due to content rather than arousal/intensity. Indeed, a filled with conductive gel (EC60, Grass Instruments) and
recent study attempted to manipulate valence and arousal independent
applied to the left and right forearms. ECG was converted off-
of content and found that picture content, emotional valence, and
emotional arousal all had independent modulatory effects on the
line to heart rate (HR) in beats-per-minute in half-second bins
acoustic startle reflex (Bernat et al., 2006). Specifically, erotic and by determining the interbeat interval in milliseconds using
threat pictures had the greatest modulatory influences that appeared LabVIEW software. Picture-evoked reactions in SCR and
independent of reported arousal. HR were calculated by subtracting mean activity in the 1 s
J.L. Rhudy et al. / Pain 136 (2008) 250–261 253

prior to picture presentation from 12 half-second bins follow- .75 mA steps until a reflex was no longer detected. This up–
ing picture onset (Bradley et al., 2001). Picture-evoked SCR down procedure was repeated two more times with .5 mA
was determined by finding the maximum change that occurred steps. The average stimulus intensity of the last two peaks
1–4 s after picture onset. Picture-evoked HR was calculated in and troughs was increased 20% to generate the intensity of
two ways: (1) maximum deceleration from baseline in the first stimulation used during picture-viewing (120% NFR thresh-
3 s of picture-viewing and (2) peak acceleration during the last old). This intensity minimizes ceiling and floor effects (Danzi-
3 s of picture-viewing (Bradley et al., 2001). To eliminate stim- ger et al., 1998). Participants for which a NFR could not be
ulus artifact due to shocks, picture-evoked SCR and HR reac- reliably obtained before tolerance was achieved were given
tions were only calculated for pictures in which a shock was the choice of repeating the threshold assessment procedure
not presented. or discontinuing the experiment (three discontinued as noted
in the Section 2.1).
To examine the influence of picture-viewing on NFR,
2.6. Nociceptive reactions within-subject changes in NFR magnitude were examined.
NFR magnitude was calculated for stimulations delivered dur-
2.6.1. Nociceptive flexion reflex (NFR) ing picture-viewing by subtracting mean activity in the 60 ms
The NFR is a protective withdrawal reflex in response to a prior to electric stimulation from mean activity in the 90–
noxious stimulus (Skljarevski and Ramadan, 2002; Sandrini 150 ms post-stimulation window.
et al., 2005). Experimentally, the NFR is typically elicited by
electrodermal stimulation over the sural nerve that activates 2.6.2. Subjective pain ratings
primary nociceptors (Ad and C fibers). Nociceptor activation To rate each electric stimulation, a computer-presented rat-
results in a nociceptive signal to the spinal cord that subse- ing scale oriented vertically was used (France et al., 2002;
quently elicits a withdrawal response in the leg that can be Rhudy et al., 2005). Bottom-to-top, the scale was labeled: 0
quantified using electromyography (EMG) (Wiesenfeld-Hallin (no sensation), 1 (just noticeable), 25 (uncomfortable), 50
et al., 1984; Sandrini et al., 2005). The NFR is a spinal reflex (painful), 75 (very painful), and 100 (maximum tolerable).
because supraspinal regions are not necessary for its elicitation To respond, participants moved an indicator anywhere along
(e.g., Sandrini et al., 1999). The stimulation intensity necessary the scale and submitted their answers by computer mouse.
to reliably elicit the NFR (i.e., NFR threshold) correlates with These ratings were used as a measure of subjective pain.
subjective report of pain threshold, and the magnitude of the
NFR correlates with subjective pain intensity (Chan and Dal- 2.6.3. Autonomic reactions
laire, 1989; Guieu et al., 1992; Rhudy et al., 2005). Thus, the Research from our laboratory has found that peak auto-
NFR is used as an objective, indirect measure of spinal nomic reactions (skin conductance response [SCR]; peak heart
nociception. rate [HR] acceleration) to noxious stimulation are modulated
Two active recording electrodes were placed over the left by emotional processing (Rhudy et al., 2007b). Specifically,
biceps femoris muscle 10 cm superior to the popliteal fossa peak SCR and HR acceleration following noxious shock are
to assess EMG activity associated with the NFR. A common diminished by appetitive activation and enhanced by defensive
ground electrode was placed over the left lateral epicondyle activation. Therefore, we chose to focus only on these auto-
of the femur. Biceps femoris EMG activity 90–150 ms post- nomic measures.3 SC activity was first averaged by .5 s epochs,
stimulation was used to define the NFR. Prior research has and then the mean activity in the 1 s pre-shock interval was
shown that using the 90–150 ms timeframe avoids potential subtracted from each .5 s post-shock epoch (Bradley et al.,
contamination by the non-nociceptive RII reflex, startle 2001). SCR was defined as the maximum skin conductance
responses, and/or voluntary movements (Dowman, 1992; increase in the 1–4 s post-shock interval (Dawson et al.,
France and Suchowiecki, 2001). The raw biceps femoris signal
was amplified by 20,000, bandpass filtered (10–300 Hz), and
3
rectified. These methods of scoring SCR and HR acceleration have been
The intensity of electrodermal stimulation delivered used in previous emotion research to determine picture-evoked
throughout picture-viewing was set at 120% NFR threshold. reactions (Bradley et al., 2001). However, these scoring methods may
To determine NFR threshold, procedures were adapted from lead to artificially high values, because they base responses on peak
values in a narrow scoring window. To determine whether the
France and colleagues (France et al., 2002). During threshold
emotional modulation effects noted in this study were artifacts of
assessment, NFR was defined as a mean EMG response in the our scoring methods we also calculated HR as the mean change in the
90–150 ms post-stimulus interval that exceeded mean EMG 1–5 s post-stimulus window and SC as the mean change in the 1–4
activity during the 60 ms pre-electrical stimulus baseline inter- post-stimulus window. These change scores were then standardized
val by at least 1.0 standard deviation. Stimulation of the sural and compared to the standardized versions of our original HR
nerve for threshold determination proceeded using an up– acceleration and SCR variables. The two scoring methods were highly
down staircase method with a variable interval of 8–12 s while correlated with each other (SCR, r > .90; HR, r = .59; ps < .001).
the participant sat comfortably in a recliner with their leg out- Analyses of the effect of picture-viewing on these new variables
stretched (knee angle approximately 180; e.g., Chan and resulted in nearly identical results as those reported using the HR
Tsang, 1985). Each stimulation consisted of five rectangular acceleration and SCR variables. Picture content explained 36% of the
variance in SC change and 23% in HR change. The pattern of SC
wave pulses of 1 ms duration and 3 ms interstimulus interval
change means and HR change means for each picture content were the
(250 Hz). The threshold assessment procedure started at same as those noted for SCR and HR acceleration, thus we chose to
0 mA (current) and increased in 1.5 mA steps until a NFR keep our original variables in the manuscript to be consistent with our
was detected. Stimulus intensity was then decreased in previous study (Rhudy et al., 2007b).
254 J.L. Rhudy et al. / Pain 136 (2008) 250–261

2000). Therefore, the .5 s post-shock epoch (in the 1–4 s post- verting to z scores.4 Standardizing has the effect of eliminating
shock interval) with the greatest positive change was used as between-subject variability (by setting each participant’s mean
the response definition (Bradley et al., 2001). ECG was con- response to zero), while retaining within-subject variability due
verted offline to HR in beats-per-minute from interbeat inter- to picture-viewing, and is common in psychophysiological
vals and visually inspected for errors. Like SC, the HR studies (e.g., Blumenthal et al., 2005). Therefore, individual
waveform was first averaged by .5 s epochs and the mean activ- differences in the absolute magnitude of each variable are
ity in the 1 s pre-shock interval was subtracted from each .5 s removed and the effect of picture-viewing (a within-subject
post-shock epoch. Peak HR acceleration was defined as the effect) is retained. Furthermore, standardizing has the benefi-
.5 s post-shock epoch (in the 1–5 s post-shock interval) with cial effect of placing all nociceptive reactions in a common met-
the greatest positive change. ric (standard deviation units) thus facilitating the
interpretation of analyses that collapse across reaction type
2.7. Procedure (analyzing all reactions simultaneously, see below).
Although analyses were conducted to examine the indepen-
Health status of all participants was determined using a dent influence of affective valence and arousal, a single inde-
brief health questionnaire and interview to determine eligibil- pendent variable (picture content) was used to model the
ity. If eligible, electrodes were applied, the participant was influence of valence and arousal rather than separate indepen-
seated comfortably in a reclining chair, and then familiarized dent variables. This allowed statistical models to make com-
with the rating scales used throughout testing (SAM, pain parisons to neutral pictures (which could not be done if
rating scale). Ratings were made using a computer mouse valence and arousal were separate independent variables).
positioned on a lap desk. Participants were told that there Analyses on manipulation checks for emotion-induction were
were two phases to the experiment. Phase 1 (NFR threshold conducted using a 5 (Picture Content) · 2 (Picture Dura-
assessment) involved sending electric pulses to the ankle to tion) · 2 (Participant Sex) repeated measures MANOVA. To
determine the stimulus intensity necessary to elicit the examine the influence of picture-viewing on nociceptive reac-
NFR. During this phase, the participant viewed the pain rat- tions, a 4 (Reaction Type) · 5 (Picture Content) repeated mea-
ing scale positioned next to a digital green light (both were sures MANOVA was conducted. Initially, participant sex and
continuously displayed on the computer monitor). The light picture duration were also included as independent variables in
indicated when the participant was to make a rating (follow- the model predicting nociceptive reactions, but these effects
ing every stimulus). The participant was told to make a rating were not significant (Fs < 2.10, ps > .16). Thus, for parsimony,
whenever the light came on, regardless of whether the stimu- they were dropped from the final model. Follow-up compari-
lus was perceived. During phase 2, the participant was sons were conducted with Bonferroni adjusted means tests to
instructed to view every picture presented on the computer control for Type I error rate, except a priori hypotheses of
monitor, and told that electric stimuli would be delivered ran- nociceptive outcomes were one-tailed Fisher LSD tests. Unless
domly during and in between pictures. Picture duration was noted, analyses were conducted using the GLM procedure
varied in a pseudorandom manner, with half of the pictures within SPSS 14.0. Partial eta-squared (g2) was used as the effect
having 500 ms duration and the other half 6 s duration. Pic- size for F tests and Cohen’s d was used for mean comparisons.
ture durations were equally distributed across picture con- Cohen (1977) provides guidelines for interpreting g2
tents. Inter-picture intervals varied randomly from 12 to (small = .01, medium = .06, large = .14) and d (small = .2,
22 s. Electric stimuli (at 120% NFR threshold) were delivered medium = .5, large = .8). Wilks’ k are the multivariate statis-
during 50% of the pictures (six for each picture content, bal- tics interpreted but are not presented given the redundancy
anced across picture duration) and 10 inter-trial intervals. with partial eta-squared.
Thus, a total of 40 stimulations were delivered during phase
2. During phase 2, electric stimuli were randomly delivered 3– 2.8.1. Hypotheses
5 s after picture onset and 11–21 s after inter-picture interval It was predicted that nociceptive reactions would be modu-
onset to reduce predictability (shock onset intervals were lated in parallel and influenced by emotional valence and arou-
always an integer). The 3–5 s post-picture-offset interval was sal (valence-by-arousal interaction). Specifically, nociceptive
chosen because it has been shown to produce the largest emo- reactions were expected to be facilitated by unpleasant pictures
tional modulation effects on the acoustic startle reflex (Brad- and inhibited by pleasant pictures. However, pictures eliciting
ley et al., 1993; Codispoti et al., 2001). Following each greater arousal were expected to show stronger modulation –
picture, the SAM was administered to assess emotional attack pictures were expected to elicit the greatest facilitation
responses to the pictures. The pain rating scale was adminis- and erotic pictures the greatest inhibition. Therefore, only a
tered following pictures and inter-picture intervals in which main effect of picture content was predicted to be significant
an electric stimulus was delivered. At the end of the experi- in the analysis of nociceptive reactions. Reactions during
ment, the participant was debriefed and thanked for their
participation. 4
It is important to note that within-subject z transformations can
have the beneficial effect of minimizing the impact of outlier values,
2.8. Data reduction and analyses
because means are centered at zero and the within-subject variability is
put on a common metric (in this case standard deviation units).
All self-report and psychophysiological variables were aver- Therefore, the standardized means will ‘‘rein in’’ the outlier. At times,
aged across pictures with similar content (attack, loss, neutral, this can cause a mean to change its magnitude relative to other means.
food, erotic). Before averaging, SCR, HR acceleration, NFR, This is most obvious when comparing unstandardized means to
and pain ratings were standardized within-individuals by con- standardized means.
J.L. Rhudy et al. / Pain 136 (2008) 250–261 255

attack and erotic pictures were expected to be significantly dif- For unpleasant contents, loss (p = .001, d = .89) and
ferent (higher and lower, respectively) than reactions during attack pictures (p < .001, d = 1.74) were more arousing
neutral pictures, whereas reactions during loss and food pic- than neutral, and attack pictures were more arousing
tures were not expected to differ significantly from reactions than loss (p < .001, d = .92). For pleasant contents, food
during neutral pictures.
(p = .001, d = .93) and erotic (p < .001, d = 1.46) pic-
tures were more arousing than neutral, but the compar-
3. Results ison between erotic and food pictures eluded significance
(p = .10, d = .57). The main effect of picture duration
3.1. Subjective reactions to picture-viewing suggested 6 s pictures elicited greater arousal than
500 ms pictures, albeit a small difference in subjective
Table 1 depicts subjective valence and arousal ratings arousal. Together, these data suggest that valence and
by picture content, picture duration, and participant sex. arousal were independently manipulated, although ero-
Analysis of valence/pleasure ratings found a main effect tic pictures evoked less subjective arousal than expected.
of picture content, F(4, 20) = 35.13, p < .001, g2 = .88.
Erotic and food pictures elicited similar pleasure 3.2. Psychophysiological reactions to picture-viewing
(p = 1.00, d = .13) that was greater than neutral pictures
(ps < .001, ds > 2.24). Attack and loss pictures were sim- Table 2 depicts psychophysiological reactions to pic-
ilar in pleasure (p = 1.00, d = .11) and lower than neu- ture-viewing by picture content and picture duration. As
tral pictures (ps < .001, ds > 1.41). However, this main predicted, picture contents did not lead to differential
effect was qualified by significant interactions of Picture psychophysiological reactions. For picture-evoked
Content · Participant Sex [F(4, 20) = 3.45, p = .027, SCR, only the main effect of picture duration was signif-
g2 = .41] and Picture Content · Picture Duration icant [F(4, 23) = 7.07, p = .01, g2 = .24], but not the
[F(4, 20) = 8.01, p = .001, g2 = .62]. To decompose the main effect of picture content (p = .42) or the Picture
Picture Content · Participant Sex interaction, the simple Content · Picture Duration interaction (p = .23). Brief
effect of sex was examined. Only the simple effect of sex pictures led to slightly greater SCR (0.13 lS vs.
for the neutral pictures was significant. Men rated neu- 0.18 lS). For picture-evoked HR deceleration, the main
tral pictures as slightly less pleasurable than women effects of picture content (p = .14) and picture duration
(Ms = 4.54 vs. 4.88; p = .036, d = .63). To decompose (p = .63) and the Picture Content · Picture Duration
the Picture Content · Picture Duration interaction, the interaction (p = .23) were all non-significant. For pic-
simple effect of picture duration was examined for each ture-evoked HR acceleration, the main effects of picture
picture content. The only effect of duration noted was content (p = .10) and picture duration (p = .06), and the
for ratings of loss content, with 6 s pictures eliciting Picture Content · Picture Duration interaction (p = .10)
greater displeasure than 500 ms pictures (Ms = 2.45 vs. were all marginally significant. HR acceleration tended
3.13; p < .001, d = .81). to be higher during brief pictures. However, exploratory
Analysis of arousal ratings revealed main effects of Bonferroni comparisons for the main effect of picture
picture content [F(4, 20) = 12.99, p < .001, g2 = .72] content and the simple effects of picture duration were
and picture duration [F(1, 23) = 7.18, p = .01, g2 = .24]. all non-significant (ps > .05). Thus, these data are con-
Table 1
Means and standard deviations of picture-evoked subjective reactions by picture content, picture duration, and participant sex
Attack Loss Neutral Food Erotica
Mean SD Mean SD Mean SD Mean SD Mean SD
Valence ratings
500 ms Male 3.08 0.73 3.18 0.55 4.57 0.25 6.03 0.73 6.43 1.36
Female 2.44 0.96 3.09 0.94 4.84 0.34 6.10 1.53 5.50 1.28
Total 2.70 0.92 3.13 0.80 4.73 0.33 6.07 1.25 5.87 1.37
6s Male 2.88 0.91 2.37 0.67 4.52 0.64 6.33 1.20 6.58 1.25
Female 2.37 1.09 2.51 1.01 4.92 0.46 6.28 1.34 5.58 1.28
Total 2.57 1.03 2.45 0.88 4.76 0.57 6.30 1.26 5.98 1.34

Arousal ratings
500 ms Male 5.60 1.11 3.87 0.95 3.24 1.57 4.89 1.80 5.79 1.32
Female 6.16 1.96 5.11 1.57 3.22 1.42 4.31 0.86 4.95 1.32
Total 5.93 1.67 4.61 1.47 3.23 1.45 4.54 1.31 5.29 1.36
6s Male 6.05 0.76 4.60 1.21 3.70 1.80 5.03 1.58 5.83 1.07
Female 6.51 1.95 5.08 1.85 3.22 1.39 4.40 1.26 4.96 1.43
Total 6.33 1.58 4.89 1.61 3.41 1.55 4.65 1.40 5.31 1.34
256 J.L. Rhudy et al. / Pain 136 (2008) 250–261

Table 2
Means and standard deviations of picture-evoked psychophysiological reactions by picture content and picture duration
Attack Loss Neutral Food Erotica
Mean SD Mean SD Mean SD Mean SD Mean SD
SCR (DlS)
500 ms 0.20 0.32 0.17 0.28 0.16 0.21 0.17 0.32 0.22 0.27
6s 0.16 0.23 0.13 0.17 0.18 0.32 0.10 0.18 0.13 0.17
Total 0.18 0.23 0.15 0.18 0.17 0.21 0.13 0.20 0.17 0.19
HR deceleration (Dbpm)
500 ms 5.84 4.27 4.18 2.80 3.83 2.90 4.13 2.90 4.94 4.19
6s 5.20 3.44 4.02 2.40 4.87 4.37 4.16 2.97 5.47 3.09
Total 5.52 3.01 4.10 1.92 4.35 3.06 4.14 2.20 5.21 2.64
HR acceleration (Dbpm)
500 ms 4.00 5.40 2.27 2.23 4.07 3.31 4.69 3.63 3.70 4.19
6s 4.37 6.52 2.45 2.54 3.06 2.55 3.30 2.90 2.39 2.81
Total 4.19 5.54 2.36 1.90 3.57 2.48 3.99 2.70 3.05 3.07
SCR, skin conductance response; HR, heart rate; bpm, beats-per-minute.

sistent with our previous research suggesting subtle and food pictures were in the predicted directions, these
physiological responses to pictures are not observed pictures did not lead to significant modulation relative
when shocks are randomly delivered during picture- to neutral pictures (ps > .16, ds < .30). Importantly, the
viewing (Rhudy et al., 2005, 2006). Reaction Type · Picture Content interaction was not
significant (F = .45, p = .91). This suggests reactions
3.3. The effect of picture-viewing on nociceptive reactions were modulated in parallel by picture contents. None-
theless, to provide a more stringent test of parallel mod-
As predicted, only a significant main effect of picture ulation, the simple effect of reaction type was examined
content was found that explained 52% of the variance in at each level of picture content using exploratory Bon-
the multivariate combination of the standardized ferroni comparisons. Reactions were not significantly
reactions [F(4, 21) = 5.76, p = .003, g2 = .52]. Fig. 1 different during attack (ps > .12), loss (ps > .70), neutral
depicts standardized nociceptive reactions by picture (ps > .35), food (ps > .30), or erotic (ps > .26) pictures.
content. Standardized reactions during attack pictures To determine the variance explained by picture content
were significantly larger than during neutral (p = .032, in each separate reaction, partial g2 was calculated from
d = .59), but not loss pictures (p = .10, d = .38). Alter- the simple effect of picture content. Picture content
natively, standardized reactions during erotic pictures explained 15% of the variance in NFR, 42% of the var-
were significantly smaller than all other picture contents iance in pain ratings, 37% of the variance in SCR, and
(ps < .02, ds = .68–1.55). Although reactions during loss 32% of the variance in HR acceleration. For reference
purposes, Table 3 presents unstandardized means for
each nociceptive reaction by picture content. However,
0.4 NFR
it is important to point out that standardization of vari-
0.3 Pain ables can cause changes in the relative magnitude of the
Response Magnitude

0.2
SCR means and are thus not directly comparable to unstan-
HR
dardized variables.
(z score)

0.1
0.0
-0.1 3.4. Exploratory analyses
-0.2
-0.3 3.4.1. Potential confounds
-0.4
Attack Loss Neutral Food Erotic Given that NFR, SCR, and HR reactions are all cal-
culated as a change from baseline, there is the potential
Fig. 1. The influence of picture content on nociceptive flexion reflex
(NFR), pain ratings (pain), skin conductance response (SCR), and
for picture-viewing to alter baseline physiological activ-
heart rate acceleration (HR) following noxious stimulation of the sural ity, and thus confound the interpretation of these vari-
nerve. Generally, unpleasant pictures enhanced nociceptive reactions, ables (even though prior analyses suggested pictures
whereas pleasant pictures inhibited them. However, the degree of did not lead to differential psychophysiological
modulation was determined by the emotional intensity (arousal) responses). For example, an incorrect inference of
elicited by the pictures – only the most arousing pictures (attack,
erotic) elicited modulation that was significantly different from the
SCR inhibition could result if erotic pictures, but not
neutral pictures. This suggests that valence and arousal both contrib- attack pictures, significantly increased baseline skin con-
ute to the modulation of nociception and pain. Error bars are SEM. ductance level, causing the response magnitude to
J.L. Rhudy et al. / Pain 136 (2008) 250–261 257

Table 3
Means and standard deviations of unstandardized nociceptive reactions by picture content
ITI Attack Loss Neutral Food Erotic
Mean SD Mean SD Mean SD Mean SD Mean SD Mean SD
NFR magnitude (DlV) 5.49 3.24 7.16 8.09 6.59 6.22 6.88 7.53 6.30 5.40 5.65 4.58
Pain rating (0–100) 43.49 23.46 47.45 24.73 47.29 25.41 45.81 23.06 45.17 24.93 43.51 24.38
SCR (DlS) 1.26 1.20 1.32 1.32 1.21 1.07 1.20 1.16 1.14 1.23 1.06 1.09
HR acceleration (Dbpm) 7.90 3.82 8.41 4.04 7.88 4.43 7.22 4.45 7.30 4.63 6.20 4.95
Note: NFR, nociceptive flexion reflex; SCR, skin conductance response; HR, heart rate; bpm, beats-per-minute.

appear smaller after the baseline activity is subtracted 4. Discussion


(although the actual response magnitude might not have
changed). To ensure that this was not the case, the aver- The present study used picture-viewing to study
age local baselines used to calculate the change scores supraspinal modulation of objective (NFR magnitude,
for each physiological reaction were analyzed using 5 SCR, HR acceleration) and subjective (pain ratings)
(Picture Content) · 2 (Picture Duration) ANOVAs. reactions to noxious sural nerve stimulation – a para-
Fig. 2 depicts local baselines averaged by picture content digm referred to as emotional control of nociceptive
for each of the physiological reactions as well as post- reactions (ECON). Extending prior research, this study
shock waveforms of each reaction averaged by picture used different picture contents to vary valence and arou-
content. No significant effects were found, suggesting sal. Moreover, this was the first study to evaluate the
baselines were not significantly altered by the content influence of picture-viewing on four nociceptive reac-
or duration of pictures. Therefore, change scores are a tions simultaneously. Pictures effectively manipulated
valid method of quantifying the magnitude of these valence, with erotic and food pictures eliciting the great-
responses. est pleasure, attack and loss pictures the lowest pleasure,
and neutral intermediate. Pictures also manipulated
3.4.2. The relationship between self-reported emotion and emotional arousal, with erotic and attack pictures elicit-
nociceptive reactions ing the greatest arousal, loss and food pictures interme-
Although it is assumed that subjective emotion diate arousal, and neutral pictures the lowest arousal.
(valence, arousal, Valence · Arousal interaction) at least Surprisingly, erotic pictures did not elicit significantly
partially mediates the relationship between picture con- greater arousal than food pictures, as was predicted
tent and nociceptive reactivity, MANOVA models do from normative ratings. It is tempting to speculate that
not directly test the relationship between subjective emo- sexual arousal may have been underreported in our sam-
tion and nociception. To examine this relationship, a ple due to geographic social norms. However, there is no
multilevel model (hierarchical) correlational approach way to verify this given that objective picture-evoked
was conducted using the SPSS 14.0 MIXED procedure psychophysiological reactions are masked when pictures
to examine covariation between trial-by-trial valence are viewed in a threatening context (Rhudy et al., 2005,
and arousal ratings and trial-by-trial nociceptive reac- 2006).
tions. Thus, a benefit of this approach is that it takes Analyses suggested valence and arousal contributed
into account inter- and intra-individual variability in to modulation of nociceptive reactions. Reactions were
reactions to each picture and each shock. A custom larger during unpleasant pictures and smaller during
model with REML estimation was built that included pleasant pictures. But, only reactions elicited during ero-
reaction type, valence, arousal, Valence · Arousal inter- tic and attack pictures were significantly modulated rel-
action, and a Valence · Arousal · Reaction Type inter- ative to neutral pictures. This was supported by an
action as fixed effects and subject number as a random exploratory multilevel analysis suggesting self-reported
effect. Significant effects of arousal [F(1, 2967)=11.48, arousal and the valence-by-arousal interaction were sig-
p = .001] and a Valence · Arousal interaction [F(1, nificant predictors of nociceptive reactions.
2967)=9.76, p = .002] were found. The effect of valence Consistent with prior research (Rhudy et al., 2005,
just eluded significance [F(1, 2967)=3.47, p = .063]. The 2006, 2007b), the present study found nociceptive reac-
main effect of reaction type [F(3, 2967)=.93, p = .42] tions were modulated in parallel. To test this, all reac-
and the interaction of Valence · Arousal · Reaction tions were placed on a common metric and analyzed
Type [F(1, 2967)=1.27, p = .28] were non-significant. using a Reaction Type · Picture Content interaction
This suggests that subjective emotion does covary with within MANOVA (minimizing Type I error). The inter-
nociception modulation. Further, the analysis provides action effect, exploratory simple effects tests of reaction
additional evidence that a valence-by-arousal interac- type, as well as the multilevel analysis all suggested reac-
tion is associated with nociception modulation, and that tions were modulated in parallel. Importantly, picture
reactions were modulated in parallel. content explained 52% of the variance in the multivari-
258 J.L. Rhudy et al. / Pain 136 (2008) 250–261

6 NFR 13 NFR
12
Attack
Neutral

Change in Biceps Femoris EMG


11
Baseline Biceps Femoris EMG 5
Erotica
10
9
4
(micro Volts)

(micro Volts)
8
7
3
6
5
2
4
3
1 Nociceptive
2
Flexion
1 Reflex Window
0 0
Att Loss Neu Food Ero 30 60 90 120 150 180 210 240
Time from Shock (ms)

1.75 Attack
10 SCR SCR
Loss
1.50 Neutral
Skin Conductance Change

9
Baseline Skin Conductance

Food
1.25
(microSiemens)

Erotic
(micro Siemens)

8
1.00
7
0.75

6
0.50

5 0.25

4 0.00
Att Loss Neu Food Ero 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0 4.5 5.0
Time from Shock (s)

74 12 Attack
HR HR
Loss
72 10 Neutral
Food
Baseline Heart Rate

Heart Rate Change

70 8 Erotic
(bpm)

(bpm)

68 6

66 4

64 2

62 0
Att Loss Neu Food Ero 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0 4.5 5.0

-2
Time from Shock (s)

Fig. 2. Local baselines used to calculate physiological nociceptive reactions and the time course of physiological nociceptive reactions following
noxious sural nerve stimulation. Panels on the left depict local baselines averaged by picture content for each of the physiological reactions (Att,
attack; Neu, neutral; Ero, erotic). Panels on the right are the post-shock waveforms of each reaction averaged by picture content (NFR waveforms
for loss and food pictures are not depicted in the top right panel to improve readability). The top panels are the nociceptive flexion reflex (NFR), the
middle panels are skin conductance response (SCR), and the bottom panels are heart rate (HR). Erotic pictures reduced physiological reactivity and
attack pictures enhanced physiological reactivity. (Note: Individual trials depicting NFR waveforms are characterized by a phasic response in the 90–
150 ms post-stimulation interval. In the present figure, however, the waveforms in the upper right panel appear ‘‘plateau-like,’’ with activity
beginning in the 90–150 ms interval and extending beyond it. This is due to grand averaging across individuals and trials that obscures the ‘‘silent
period’’ that typically occurs after the NFR (RIII component), but before startle and voluntary movements in individual trials. In the present graph,
this averaging artifact is particularly prominent, because there were participants who demonstrated large absolute EMG responses after the 90–
150 ms interval, and grand averages (means) are heavily influenced by outliers. This large individual variability in response magnitude is an important
reason for standardizing biceps femoris EMG (NFR magnitude) when the effect of interest is a within-subject effect, i.e., emotional modulation.)
J.L. Rhudy et al. / Pain 136 (2008) 250–261 259

ate combination of the reactions, and considerable var- 2007b). Skin conductance and heart rate had been
iance in individual reactions (15% NFR, 42% pain rat- recorded in the prior experiments as a physiological
ings, 37% SCR, 32% HR acceleration). manipulation check for emotion-induction. These sig-
As noted here, picture content generally explains nals were rescored to calculate shock-evoked change
more variance in pain report than other nociceptive (nociceptive reaction), rather than picture-evoked (emo-
reactions (Rhudy et al., 2005, 2006, 2007b). One poten- tion-induction). As predicted, autonomic nociceptive
tial explanation could be report bias, because pain rat- reactions were also modulated by emotion. Shock-
ings and picture (emotion) ratings are made together. evoked SCR and HR acceleration were smaller during
Contrary to this hypothesis, the picture content IV pleasant pictures than during unpleasant pictures. Thus,
explains greater variance in pain than emotion ratings converging evidence suggests ECON can be used to
(Rhudy et al., 2005, 2006). Alternatively, different noci- study modulation of nociceptive reactions assessed from
ceptive responses may be modulated by different pro- multiple response systems (motoric, autonomic, subjec-
cesses. Supporting this, emotional modulation of the tive), mediated by circuits at spinal (NFR) and supraspi-
NFR is abolished when noxious shocks are predictable, nal (SCR, HR) levels.
despite intact modulation of subjective pain (Rhudy
et al., 2006). Thus cortico-cortical circuits may continue 4.2. The emotion–pain relationship
to modulate subjective pain even when brain-to-spinal
cord circuits are disengaged. This would explain why This study provides preliminary support for the
some cognitive-emotional factors (catastrophizing, self- hypothesis that the emotion–pain relationship is deter-
efficacy) modulate subjective pain but not NFR (France mined by a valence-by-arousal interaction. Specifically,
et al., 2002; Brant et al., 2007; Rhudy et al., 2007a). valence determines the direction of the modulation and
Although compelling, the reason for modulatory differ- arousal the magnitude. This hypothesis may not extend
ences across responses cannot be determined at this time. to highly arousing emotions, however. Animal and
human studies (e.g., Fanselow, 1994; Rhudy and Mea-
4.1. Relation to prior research gher, 2000) suggest nociceptive reactions are inhibited
by events that elicit intense defensive activation (highly
This is the fourth study from our laboratory to exam- arousing negative emotion) – a reversal of the direction
ine the influence of emotional picture-viewing on noci- of modulation compared to negative emotions with low-
ceptive reactions. Rhudy and colleagues (2005) were to-moderate arousal. However, the direction of modula-
the first to demonstrate emotional processes can activate tion does not appear to reverse during highly arousing
descending circuits that influence spinal nociception. In positive emotions. The current study suggests positive
that study, erotic, neutral, and attack pictures modu- emotions with low-to-moderate arousal inhibit pain,
lated the spinally-mediated NFR and subjective pain. whereas other studies suggest intense appetitive activa-
NFR magnitudes and pain ratings were greater during tion (e.g., genital stimulation) that elicits highly arousing
attack pictures and smaller during erotic pictures. As a positive emotion (e.g., orgasmic bliss) leads to profound
result, we argued ECON procedures represent novel, pain inhibition (Komisaruk and Whipple, 1986). When
non-invasive methods for engaging descending modula- all data are considered, a valence-by-arousal interaction
tion in humans. may still characterize the emotion–pain relationship
Rhudy et al. (2006) examined whether reactions to (Fig. 3). Picture-viewing would not be expected to
predictable noxious shocks were also modulated by pic- induce negative emotions capable of producing pain
ture-viewing. Hypothetically, if nociceptive reactions to inhibition, however. Inhibition is expected only when
predictable shocks were also modulated, then employing negative emotions accompany imminent threat (Fanse-
predictable shocks could reduce participant stress given low, 1994) and pictures are only likely to represent an
the preference for noxious events to be predictable imminent threat for certain clinical populations (e.g.,
(Miller, 1981; Mineka and Henderson, 1985). In that specific phobia of snakes).
study, half of the participants received cued (predict-
able) shocks during picture-viewing, and the other half 4.3. Limitations
received uncued (unpredictable) shocks. Data from the
uncued shock group replicated the first study. However, The present study was limited by a small sample. For-
pain ratings, but not NFR, were modulated in the cued tunately, picture-viewing exerts a large statistical effect on
shock group. Thus, it was concluded that unpredictable nociceptive reactivity. However, other predictors in the
shocks should be used to observe NFR modulation (and model (participant sex, picture duration) may have
ensure brain-to-spinal cord circuitry is activated). achieved significance with a larger sample. Although the
The third study combined data from the first two Reaction Type · Picture Content interaction did not
studies to examine the impact of picture-viewing on achieve significance, exploratory simple effects tests pro-
autonomic reactions to noxious shocks (Rhudy et al., vided some confidence low power was not responsible.
260 J.L. Rhudy et al. / Pain 136 (2008) 250–261

Defensive Activation (negatively valenced emotions)


independent influence of arousal. Indeed, a recent study
Appetitive Activation (positively valenced emotions) found that valence, arousal, and picture content all con-
tributed uniquely to emotional modulation of the acous-
Nociception Modulation
Facilitation

tic startle reflex (Bernat et al., 2006). Despite our


confounding between picture content and arousal,
exploratory multilevel analysis of subjective emotion
ratings suggested that a valence-by-arousal interaction
did significantly predict nociceptive reactions.
Inhibition

4.4. Implications
Arousal (Emotional Intensity)
This represents the third independent test of ECON
Low Arousal Moderate High Arousal
Arousal procedures. Nociception modulation has been reliably
elicited across all three samples, and picture content
Range of arousal elicited by
picture-viewing consistently explained large proportions of variance in
nociceptive outcomes. Thus, ECON appears to be a
Fig. 3. A hypothetical figure depicting the influence of emotional
valence and arousal on nociception. Negative emotions with low-to-
valid method of engaging supraspinal modulation.
moderate arousal facilitate nociception, with the degree of facilitation Although it is important that future studies determine
determined by arousal level. However, highly arousing negative whether individual differences (e.g., participant sex)
emotions inhibit nociception. In contrast, positive emotions always influence which pictures elicit greatest modulation, these
inhibit nociception, with the degree of inhibition determined by results suggest the greatest modulation is evoked by ero-
arousal level. Thus, an interaction of emotional valence and arousal
characterizes the emotion–pain relationship. Emotion-induction by
tic and attack pictures. Thus, researchers should be cau-
picture-viewing would not be expected to elicit intense, highly arousing tious when averaging reactions across pictures of similar
negative emotions indicative of active defense. Therefore, negative valence (but that vary in content/arousal) as this may
emotions would not be expected to inhibit nociceptive reactions in the attenuate the modulation observed.
current study. (This figure is adapted from Rhudy and Williams (2005),
reprinted by permission of the publisher; Rhudy and Williams: Gender
differences in pain: do emotions play a role? Gender Medicine;2:208– 4.5. Summary
26. Copyright 2005 by Excerpta Medica Inc.).
This study found emotional valence and arousal con-
tribute to modulation of nociceptive reactions (NFR,
It is noteworthy that modulation of subjective pain
subjective pain, SCR, and HR acceleration), with mod-
was a clinically small effect, despite being a statistically
ulation being associated with a valence-by-arousal inter-
large effect. Thus, emotional picture-viewing may prove
action. The combined influence of valence and arousal
better for studying nociceptive processing than for cop-
had a coordinating effect, with picture content explain-
ing with chronic pain (Seminowicz and Davis, 2007).
ing 52% of the variance in the four reactions. Together,
Before this conclusion can be drawn though, the effects
these data suggest the ECON paradigm is a reliable tool
of picture-viewing on clinical pain must be established
for studying supraspinal modulation.
(c.f., Montoya et al., 2005).
In the present study respiration rate was not measured.
Thus, picture-evoked breathing changes may have modu-
Acknowledgements
lated shock-evoked HR (respiratory sinus arrhythmia)
rather than pain modulatory circuits. However, given that
The first author would like to acknowledge the Henry
ANS reactions may contribute to pain perception (Chap-
Kendall College of Arts and Sciences and the Office of
man et al., 2002), respiration may represent another
Research at The University of Tulsa for partial financial
mechanism by which emotion can indirectly influence
support of this research through a faculty development
pain and nociceptive reactions. Nonetheless, our HR out-
summer fellowship. The authors thank Carl P. Latti-
comes should be interpreted with caution.
more III for help with data processing, as well as Emily
A final limitation is due to the method of manipulat-
Bartley and two anonymous reviewers for their com-
ing arousal. Given the arousal manipulation is con-
ments on earlier drafts of this paper.
founded with picture content, we are unable to
determine whether quantitative differences in activa-
tion/arousal are responsible for our results, or whether
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