Behavioral modulation by mutilation pictures in women

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Braz J Med Biol Res 37(3) 2004

Behavioral modulation by mutilation pictures in womenBrazilian Journal of Medical and Biological Research (2004) 37: 353-362ISSN 0100-879X

Behavioral modulation by mutilationpictures in women

1Departamento de Neurobiologia, Instituto de Biofísica,Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brasil2Departamento de Fisiologia e Farmacologia, Universidade Federal Fluminense,Niterói, RJ, Brasil3National Institute of Mental Health, Bethesda, MD, USA

M.G. Pereira1, E. Volchan1,L. Oliveira2,

W. Machado-Pinheiro2,J.A. Rodrigues2,

F.V.P. Nepomuceno2

and L. Pessoa3

Abstract

Previous studies have shown that women are more emotionally ex-pressive than men. It is unclear, however, if women are also moresusceptible to the emotional modulation of behavior imposed by anaffective stimulus. To investigate this issue, we devised a task inwhich female subjects performed six sequential trials of visual targetdetection following the presentation of emotional (mutilation anderotic) or neutral pictures (domestic utensils and objects) and com-pared the data obtained in the present study with those described in aprevious study with male subjects. The experiment consisted of threeblocks of 24 pictures and each block had an approximate duration of4 min. Our sample consisted of 36 subjects (age range: 18 to 26 years)and each subject performed all blocks. Trials following the presenta-tion of mutilation pictures (283 ms) had significantly slower reactiontimes than those following neutral (270 ms) pictures. None of the trialsin the “pleasant block” (271 ms) was significantly different from thosein the “neutral block”. The increase in reaction time observed in theunpleasant block may be related in part to the activation of motiva-tional systems leading to an avoidance behavior. The interferenceeffect observed in this study was similar to the pattern previouslydescribed for men. Thus, although women may be more emotionallyexpressive, they were not more reactive to aversive stimuli than men,as measured by emotional interference in a simple reaction time task.

CorrespondenceM.G. Pereira

Departamento de Neurobiologia

Instituto de Biofísica, UFRJ

CCS, Bloco G

21949-900 Rio de Janeiro, RJ

Brasil

Fax: +55-21-2280-8193

E-mail: [email protected]

Research supported by PRONEX/MCT,

CNPq and FAPERJ.

Received March 14, 2003

Accepted November 10, 2003

Key words• Emotion• Behavior• Reaction time• Sex differences• Affective stimulus

Introduction

The fast, effortless processing of poten-tially threatening stimuli is highly advanta-geous and may be critical for survival. Sev-eral researchers have proposed that the pro-cessing of a negative stimulus may be “auto-matic” (1,2). Psychophysical studies haveshown that observers exhibit fast, involun-tary responses to emotional stimuli, such asfaces with fearful expressions or aversive

pictures (3-5) . However, many studies sug-gest that there are sex differences in theresponses to emotional stimuli. Conventionalwisdom (at least in some cultures) suggeststhat women are more “emotional” than men(6). Does this mean that women express,experience or have stronger physiologicalresponses than men? In fact, a substantialbody of research has demonstrated thatwomen are more emotionally expressive thanmen (for a review, see Ref. 7). However,

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Kring and Gordon (8) stated that women donot report experiencing more emotion thanmen and their skin conductance activity isdifferent but not directly consistent with theview that women are more emotional. Ac-cording to those investigators, differencesbetween men and women in the physiologi-cal response, at least for skin conductanceactivity, varied according to type of emotion,particularly for negative emotions. In theseexperiments, men showed greater reactivityto fear and anger films, and women hadgreater reactivity to sad and disgustingfilms.

Other studies suggest that women aremore reactive to unpleasant events, espe-cially those that are threatening or traumatic(9). Bradley et al. (10) investigated sex dif-ferences in emotional picture processing andobtained results consistent with the idea thatwomen are more reactive to aversive stimu-lation. In their study, they compared theresponses of men and women to pleasantand unpleasant pictures (of varied contents)and demonstrated that women were morereactive to unpleasant materials, rating thepictures as more arousing and more unpleas-ant, and also reacted with more markedchanges in electromyographic recordings ofcorrugator activity. Women also respondedwith greater fear bradycardia (cardiac decel-eration) when viewing unpleasant pictures.According to the investigators, these datasuggest that symbolic picture cues activatethe defensive motivational system more in-tensely in women than in men. In contrast,men tended to be marginally more reactivethan women when viewing pleasant pictures,rating these pictures slightly more pleasantand more arousing, and reacting with moreskin conductance activity (10).

In addition to the wide range of directemotional responses evoked by affective pic-tures (3,11) the processing of emotionalstimuli by human subjects can also interferewith the performance of non-emotionalattentional tasks (12,13). On the basis of the

statement made by Bradley et al. (14,15)that, among others, erotic and attack-mutila-tion pictures most strongly activate the pri-mary motivational states (i.e., appetitive anddefensive states, respectively), we tested theeffects of viewing these categories of pleas-ant and unpleasant pictures in a subsequentsimple detection task in a male sample. Inthis study (16) we demonstrated that emo-tional pictures induced a sustained interfer-ence with a simple detection task. Subjectsperformed six sequential trials of simple tar-get detection following the offset of eachpicture. Reaction times for trials presentedafter mutilation pictures were significantlyslower than those presented after erotic orneutral pictures. As discussed above, manystudies have measured direct physiologicalor evaluative responses evoked by affectivestimuli and have suggested that women ap-pear to be more emotionally expressive thanmen, and there is also some evidence fortheir hyperreactivity to aversive pictures.Would this mean that women are more sus-ceptible to the emotional modulation of be-havior imposed by affective stimuli (at leasthighly arousing stimuli)?

To investigate this issue, we repeated thesame paradigm as used in our previous study,but now applied to a group of women. Bycomparing the data obtained in the presentstudy to the results described previously formen, we can assess if emotional modulationof a behavioral task has a similar pattern forboth sexes. Evaluative judgments were alsoperformed in order to check for sex differ-ences in rating reports (10) in our sample.

Subjects and Methods

Subjects

Thirty-six female volunteers participatedin the experiment (age range: 18-26 years).Subjects were college students from the Fed-eral Fluminense University, Rio de Janeiro,RJ, Brazil, who reported no neurological or

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psychiatric disorders, and none were takingmedication. All of them were right-handedaccording to the Edinburgh Inventory (17)and had normal or corrected vision. Thelocal Ethics Committee approved the exper-imental protocol and each subject gave writ-ten informed consent to participated in thestudy.

Apparatus and stimulus selection

Subjects were tested in a sound-attenu-ated room under dim ambient light. Stimulustiming and presentation, as well as collec-tion of responses, were controlled by a com-puter. Stimulus presentation was pro-grammed using MEL software (PsychologySoftware Tools Inc., Pittsburgh, PA, USA).The subjects’ head was positioned on a head-and-chin rest 57 cm from the screen.

Ninety pictures were used in the wholeexperiment. Seventy-nine were selected fromthe International Affective Picture System, acollection of standardized color photographicmaterial (18,19). Eleven additional eroticmale pictures were obtained on the Internet.We divided these pictures into four sets.Three sets of 24 pictures each were used intest blocks: pleasant (erotic males or eroticcouples), neutral (household and inanimateobjects) and unpleasant (mutilated bodies).One set of 18 pictures with wide-rangingvalence and arousal ratings was selected fora practice block (see below).

Design and procedure

The experimental session consisted of aninitial practice block followed by three testblocks. During each test block, 24 picturesof a single type were used (erotic, neutral, ormutilation). The serial position of each testblock was counterbalanced across partici-pants using all six possible orders. Pictureswere presented in a fixed order within ablock for all participants. We carefullyaligned the pictures in a manner as unbiased

as possible according to the valence andarousal ratings (18).

For all blocks, each picture was presentedfor 2 s, followed by six trials of target detec-tion. Subjects were instructed to attend to thepicture as long as it was displayed. Afterpicture offset, a fixation spot was presentedin the center of the screen for 500 to 700 msand then the target (a small annulus) ap-peared around it (see Figure 1). Both thefixation spot and the target were presented inwhite on a black screen and remained onuntil the subject’s response. Subjects wererequired to press a button with the rightindex finger as soon as they detected thetarget. The next trial began 500 ms after thesubject’s response, with the onset of thefixation spot. After six trials, a new pictureappeared on the screen. Trials with responseslonger than 1000 ms or shorter than 100 ms

Picture 24

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Figure 1. Schematic representation of the experimental design. Neutral, unpleasant, andpleasant blocks consisted of 24 pictures. Each picture was followed by six trials of a simpletarget detection task. The lower part of the figure presents the temporal structure associ-ated with each picture and subsequent detection trials.

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were considered errors and were discarded(less than 5% of the trials).

The choice for a blocked presentation ofpictures was based on the study by Bradleyet al. (20), who reported that emotional modu-lation in the interpicture interval is only elic-ited under a blocked paradigm.

During the practice block a visual feed-back of the response latency (in millisec-onds) appeared on the screen for 1 s. Afterthe offset of the display with reaction time, anew trial began. Errors were displayed onthe screen as “anticipation” or “slow re-sponse”, also for 1 s. There was no visualfeedback of the response latency in testblocks.

Statistical analysis

Data from two subjects who had a meanreaction time slower than the group average

minus 3 standard deviations were not in-cluded in the analysis of the test blocks. Themean reaction time for each block was sub-mitted to a repeated-measures ANOVA test.Valence (pleasant, neutral or unpleasant)and trial number (1-6) were used as within-subject factors. Post hoc tests were carriedout by the Newman-Keuls method. The levelof significance adopted was P < 0.05.

Rating session

After the end of the behavior experimen-tal session, an evaluative report of the previ-ously presented pictures began. The picturesused in the rating session were presented inthree sets of 30 pictures each. They were thesame 90 pictures as described before, butrandomly distributed. The rating session be-gan with a preparation slide (“Get ready torate the next image”), which was presentedfor 5 s. Then images were presented for 6 s.During the 10-s interval between pictures,participants were asked to rate the picture (ina ratings booklet) on the dimensions of va-lence and arousal using the paper and pencilversion of the self-assessment manikin, anaffective rating system devised by Lang et al.(18,21). In this system, ratings of valence areindicated by 5 graphic representations offacial expressions ranging from a severefrown (most negative) to a broad smile (mostpositive). For arousal, the manikin variesfrom a state of low to high agitation. Partici-pants may select any of the five figures com-prising each scale, or the boxes between anytwo figures, which results in a nine pointrating scale for each dimension. In the va-lence dimension, 9 represents the extreme ofpleasantness and 1 the extreme of unpleas-antness. For the arousal dimension, ratingsare such that 9 represents a high rating and 1represents a low rating. Before the rating ofthe pictures, 9 pictures were used in order todemonstrate the rating scales. Additionally,subjects practiced their ratings on 3 practicepictures.

Figure 2. Ratings of women (closed symbols) and men (open symbols). Each symboldepicts the mean valence and arousal ratings for pleasant, unpleasant and neutralpictures. The data for women are from the present study and the data for men weretaken from a previous study (16).

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Results

Valence ratings of erotic (mean = 6.9)pictures were significantly higher and va-lence ratings of mutilation pictures (mean =1.9) were significantly lower than valenceratings of neutral pictures (mean = 5.1).Arousal ratings were greater for pleasant(mean = 4.7) and mutilation (mean = 6.3)pictures than for neutral ones (mean = 1.8);mutilation and erotic pictures differed sig-nificantly in arousal level (see in Figure 2).As proposed by Bradley et al. (10), by com-puting the correlation between pleasure andarousal ratings it is possible to determine the“vectors” that describe appetitive and defen-sive motivation. To assess these motivationvectors, we computed the correlation be-tween pleasure and arousal ratings for eachgroup of pictures separately. There was asignificant correlation between ratings ofpleasure and arousal for erotic (r = 0.73, P <0.001) and mutilation (r = -0.60, P = 0.002)pictures, but no correlation was found forneutral pictures (r = 0.02, P = 0.92).

The analysis of reaction times revealed amain effect of valence (F[2,66] = 4.06, P =0.02). Mean reaction times to targets weresignificantly slower following mutilation pic-tures (283 ms) than those following neutralpictures (270 ms) and erotic pictures (271ms). There was no significant difference inreaction time between erotic and neutralblocks (P = 0.93).

There was also a main effect of trialnumber (F[5,165] = 3.5, P = 0.004), with afaster reaction time for the second trial (262ms) following picture offset compared to allother trials (P < 0.05), except for trial 3 (271ms), for which only a trend was observed (P= 0.08). Post hoc analyses revealed that thesecond, third, fifth and sixth trials duringunpleasant blocks were significantly slowerthan those during neutral blocks. This sus-tained effect is illustrated in Figure 3A. Dur-ing erotic blocks, none of the trials weresignificantly different from those during neu-

Figure 3. Sustained interference effect. Data are reported as means ± SEM. A, Asignificant slowing down of manual reaction time following unpleasant picturescompared to neutral pictures was observed for trials 2, 3, 5 and 6. B, None of thetrials involving pleasant blocks differed significantly from those involving neutralblocks.

tral blocks (Figure 3B).

Discussion

Evaluative judgments confirmed that theaffective pictures used in this experimentwere associated with reports of pleasure ordispleasure. Moreover, there was a correla-tion between pleasure and arousal ratingsindicating that as pictures were rated as in-creasingly more pleasant or more unpleas-

Rea

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ant, arousal ratings tended to increase aswell. We compared the ratings of the femalegroup with the men’s ratings obtained in ourprevious study (16) to determine if therewere significant differences in evaluativejudgments between groups. The pictures usedin the previous study were the same, exceptfor the pleasant pictures that were eroticphotos of females instead of males. Table 1presents the mean ratings of pleasure andarousal for women (present study) and men(16) when viewing erotic, neutral and muti-lation pictures. Values reported by Lang etal. (18) for North Americans are presented inTable 2. The Brazilians’ ratings for each ofthe 72 pictures used in the test blocks arepresented in Figure 2 separately for men andwomen. Women rated negative pictures assignificantly more unpleasant than men and

positive pictures as significantly less pleas-ant than men. There was no difference be-tween groups in valence ratings for neutralpictures. Men’s arousal ratings for erotic andneutral pictures were significantly higherthan for women. In our samples women didnot find the mutilation pictures more arous-ing than men which is different from datareported by Bradley et al. (10) and Lang et al.(18). A comparison between the vectors de-scribing appetitive and defensive motivationrevealed that women showed a stronger cou-pling between increased arousal and unpleas-antness (r = -0.6 vs r = -0.13 for women andmen, respectively; P = 0.04). Previous stud-ies also described stronger linear defensemotivation vectors for women than for menwhen subjects rated pictures (10), sounds orwords (22,23). On the other hand, these

Table 2. International Affective Picture System (IAPS) ratings of valence and arousal for women and menwhen viewing pleasant, neutral and unpleasant pictures.

Valence Arousal

Women Men Significance Women Men Significance

Erotic nudes 6.5 ± 0.5 7.5 ± 0.5 P < 0.0001 5.9 ± 0.4 6.8 ± 0.5 P < 0.0001

Objects 5.0 ± 0.3 4.8 ± 0.2 P = 0.0793 2.6 ± 0.4 2.4 ± 0.4 P = 0.0529

Mutilated bodies 1.5 ± 0.3 2.1 ± 0.4 P < 0.0001 6.9 ± 0.7 6.1 ± 0.6 P < 0.0001

Data are reported as mean ± SD. The statistical test used to compare men to women was the t-test. Thedata for both females and males were taken from IAPS (18). The ratings for the 13 erotic pictures wereselected from IAPS (19).

Table 1. Ratings of valence and arousal when viewing pleasant, neutral and unpleasant pictures for womenand men.

Valence Arousal

Women Men Significance Women Men Significance

Erotic nudes 6.9 ± 0.5 7.5 ± 0.5 P = 0.0002 4.7 ± 0.8 6.0 ± 0.6 P < 0.0001

Objects 5.1 ± 0.2 5.1 ± 0.2 P = 0.9055 1.8 ± 0.2 2.4 ± 0.4 P < 0.0001

Mutilated bodies 1.9 ± 0.2 2.4 ± 0.3 P < 0.0001 6.3 ± 0.5 6.5 ± 0.4 P = 0.2248

Data are reported as mean ± SD. The statistical test used to compare men to women was the t-test. The datafor females (N = 36) are from the present study and the data for males (N = 24) were taken from a previousstudy (16).

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studies described a stronger linear appetitivemotivation vector for men than for women.We did not observe any difference in linearapproach vector between women and men (r= 0.73 and r = 0.64, respectively; P = 0.54).

The data obtained in the behavioral ses-sion showed that the valence of task-unre-lated pictures affects the performance of asubsequent non-emotional reaction time taskin women. More specifically, responses fol-lowing mutilation pictures were slower thanthose following neutral or erotic pictures,and there was no difference in reaction timebetween pleasant and neutral blocks. Thisslowing down of reaction time during theunpleasant block was not a transient effectof brief duration, but rather it persisted for atleast 6 s after picture offset. This sustainedeffect may be linked to the blocked presenta-tion mode of the experiment. There was nosignificant linear trend for an increase or adecrease of the reaction time slowing downeffect across the block.

The interference effect observed in thepresent study is similar to the pattern re-ported for men by Pereira et al. (16). Thedifference in mean reaction time during un-pleasant blocks compared to neutral blockswas virtually identical for both sexes, i.e.,13.7 ms for men and 12.6 ms for women.These data do not provide evidence of greateremotional modulation on task performancein women compared to men. Although beingmore emotionally expressive than men (seeRef. 7), women showed equal emotionalinterference with behavior, as measured byemotional influence on reaction time to on-going tasks. Bradley et al. (10) suggest thatsymbolic picture cues activate the defensivemotivational system more intensely in womenthan in men and that they are more reactiveto aversive stimulation. At least for an indi-rect measurement of emotional influence, asused in this study, we found no support for agreater reactivity to aversive stimuli inwomen. One possibility is that women andmen differ only in the expression of emotion,

but the responses and influences of emo-tional stimulation are the same in both sexes.In fact, Gross and John (24) pointed out thatmen mask their feelings more than do women,which suggests an expressive difference, andnot necessarily an experiential difference,between men and women.

A possible explanation for the presentinterference effect of mutilation pictures isthat they are more attentionally demanding,thereby reducing available resources for thesubsequent target detection task. The capac-ity for emotional stimuli to engage attentionhas been well documented (20). Selectiveattention effects are, in general, very fast andtransient (25), with attentional dwelling timeof the order of 600-800 ms (26). In our task,the slowing down of reaction time during theunpleasant block was observed until the sixthtrial (not less than 6 s). The long duration ofthis effect does not favor explanations solelyin terms of typical selective attention effects,which, as observed above, occur within lessthan a second. Therefore, it is likely thatother processes are involved.

Bradley et al. (15) have recently used ablocked paradigm for specific emotional cat-egories in an investigation of visual cortexreactivity. The aim of their study was todetermine if emotional stimuli that stronglyengage the motivational primary states wereresponsible for the large activation of thevisual cortex seen in previous studies withmixed categories (27,28). Their choice oftesting separate blocks of erotic, attack andmutilation pictures as representative of scenesexpected to induce heavy engagement of theappetitive and defensive systems did resultin the highest activation of the visual cortex.In a recent paper, Codispoti et al. (29) usedexactly the same blocked paradigm as in thepresent study, i.e., mutilation as unpleasant,objects and utensils as neutral, and eroticpictures as pleasant to reveal neuroendo-crine changes related to primary motiva-tional stimuli. Concerning the pictures ofmutilated bodies, Marks (30) had already

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demonstrated that evidence of death, mutila-tion and blood from a conspecific member isan important fear-evoking stimulus. Indeed,in 1946 Hebb (31) had observed that pri-mates react with avoidance to signs of deathor mutilation of a species member. Stevensand Gerzov-Thomas (32) working with rats,observed strong fright reactions to conspe-cific blood and muscle and not to tissuesfrom another rodent species. Bradley et al.(14) also showed that humans present markedpsychophysiological reactions to mutilationpictures. Additionally, work from our labo-ratory recording body oscillations with aforce platform (33) showed that the visual-ization of a block of mutilation pictures de-creased the postural sway and caused amarked bradycardia, revealing a defensivereactivity.

Thus, an alternative explanation for thelong-duration effects observed in the presentstudy is based on the idea that activation ofmotivational systems prompts approach andavoidance behavioral tendencies (1). Chenand Bargh (34) tested whether automaticstimulus evaluation results directly in be-havioral predisposition towards a stimulus,such that positive evaluations would pro-duce immediate approach tendencies, andnegative evaluations would produce imme-diate avoidance tendencies. Subjects re-sponded to attitude object stimuli either bypushing or by pulling a lever. They respondedfaster to negatively valenced stimuli whenpushing the lever away (“avoid”) than whenpulling it toward them (“approach”), butresponded faster to positive stimuli by pull-ing than by pushing the lever. The results ofChen and Bargh (34) suggest that the auto-matic classification of stimuli as either posi-tive or negative appears to have direct be-havioral consequences. Duckworth et al. (35)used positive and negative novel pictures ona paradigm of simple reaction time. Theparticipants in the approach condition wereinstructed to pull a lever towards them whenthey detected the picture and responded faster

to positive than to negative stimuli. Those inthe avoidance condition responded by push-ing the lever away from them. Responseswere now faster to negative than to positivenovel stimuli. They concluded that, as foundfor familiar stimuli, the automatic evalua-tion of novel stimuli has direct and immedi-ate consequences for approach and avoid-ance behavioral tendencies. In a related studyby Wentura et al. (36), subjects participatedin a go/no-go lexical decision task in whichthey had to withdraw their finger from apressed key (“avoid”) or had to press a key(“approach”) if a word was presented. Re-sponses to negative words were relativelyfaster in the withdraw condition, whereasresponses to positive words were relativelyfaster in the press condition.

The interpretation of our data in terms ofapproach and avoidance behavior linked tomotivational systems predicts that unpleas-ant pictures should engage the subject in anavoidance-like behavior and positive pic-tures should engage the subject in an ap-proach-like behavior. The slower reactiontime for mutilation pictures is consistent withthe former. However, we did not obtain anyevidence for an approach-like behavior inthe case of pleasant pictures since the reac-tion time for positive pictures was not fasterthan that for neutral pictures. In the presentstudy, however, positive pictures consistedof photos of nude males presented to femalesubjects. Although rated as pleasant, it ispossible that they also caused some sort ofembarrassment or awkwardness to the sub-jects. This could potentially counterbalancethe “pleasantness” of the pictures. The doublenature of the affect associated with nudepictures when employed in laboratory ex-periments has been pointed out by others(37). The absence of any evidence of ap-proach-like behavior in this study was alsodescribed in our previous work with malesubjects (16). The data reported by Bradleyet al. (10) suggest that men and womendiverged in their reports of emotional expe-

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rience when viewing erotic pictures of theopposite sex, with a higher proportion ofmen reporting that they felt “sexy” and “ex-cited”, whereas women reported feeling“amused” and “embarrassed”, and with lessagreement amongst themselves. In the pres-ent study we found no evidence that eroticstimuli induce a different pattern of behav-ioral response between women and men.Bradley et al. (10) reported that when ex-posed to nude pictures of their same sex,both men and women rated them as neutraland low arousing. Interestingly, physiologi-cal measures, such as heart rate and startlereflex magnitude, showed that implicit emo-tional reactions were as strong as those forthe opposite sex pictures. This may meanthat explicit reports are more prone to be

constrained by social influences. Then, dif-ferences in evaluative judgments of emo-tional pictures do not always predict theirmodulatory effect on behavior.

Beyond the comparisons between menand women, taking individual differencesinto account has shed light on the mechan-isms underlying emotional reactions (see re-view by Kosslyn et al., Ref. 38). Measures ofaffective trait will be conducted in our futurestudies. Other issues for future investiga-tions include increasing the number of trialsafter the picture’s offset to check for theextent to which the modulation by unpleas-ant pictures is present, and employing func-tional neuroimaging techniques to unravelthe neural circuits underlying the behavioralmodulation reported here.

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