COGNITION AND EMOTION
2006, 20 (8), 1075 1091

Tracking fear in snake and spider fearful participants
during visual search: A multi-response domain study
Anders Flykt and Roberto Caldara
University of Geneva, Switzerland

In visual search tasks snake or spider fearful participants showed shorter reaction
times (RTs) to respond to their feared animal (e.g., snake) than to the nonfearedanimal (i.e., spider) (Öhman, Flykt, & Esteves, 2001). Here, we used this paradigm
with heart rate (HR), RTs, and event-related potential (ERP) measures, toinvestigate the nature of the responses to the feared animal, a nonfeared (butfear-relevant) animal, and fear-irrelevant target stimuli with snake fearful, spider
fearful, and nonfearful participants. Fearful participants showed shorter RTs andevoked larger amplitudes on a late positive potential (LPP; 500 700 ms) for theirfeared compared to the nonfeared and the fear-irrelevant targets. No relevant
significant differences were found on early ERP components and HR measures.
These findings do not support an involvement of early information processing in
the detection of the feared animal in fearful participants, they favour instead a moreelaborated analysis of these complex stimuli to achieve the detection.

When snake or spider fearful participants were exposed to pictures of theirfeared animal (e.g., a spider), a nonfeared (but fear-relevant) animal (e.g., asnake), and fear-irrelevant stimuli (e.g., a flower), they showed larger skinconductance responses (SCRs) to the exposure of their feared animal thanfor the other two types of stimuli (Öhman & Soares, 1994). A comparable
Correspondence should be addressed to Anders Flykt, Department of Social Science, Mid
Sweden University, S-831 25 Ostersund, Sweden. E-mail: Anders.Flykt@miun.se
This research was supported by the FNRS Grant No. 11-61659.00 provided by the Swiss
National Science Foundation, a grant given to Klaus Scherer and Anders Flykt for the study of
threat appraisal and its physiological correlates. The authors are grateful to Klaus Scherer forsupporting this study, to Thomas Wherle for programming both the heart rate changes analysis
program and also a program that transformed the matrix search arrays into nonfigurative
pictures with the same colours and luminance as the original search arrays for the baseline in theevent-related potential (ERP) experiment, to Lara Desire for recruiting the fearful subjects andassisting in both experiments, and to Didier Grandjean for assisting in the ERP experiment. We
would like to thank Denis Brunet for his ERP analysis software: Cartool 3.1. Anders Flykt is
now at the Mid Sweden University, Ostersund, Sweden, Roberto Caldara is currently supported
by a post-doctoral fellowship provided by the Swiss National Science Foundation. We are
grateful to Gillian Bruce for her comments on a previous version of the manuscript.
# 2006 Psychology Press, an imprint of the Taylor & Francis Group, an informa businesswww.psypress.com/cogemotion
DOI: 10.1080/02699930500381405

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phenomenon occurred when these biological stimuli were backwardly
masked to prevent conscious awareness of the picture content, a resultthat has been interpreted as evidence for preattentive processing of feared
stimuli, a processing that precedes and directs attention by focusing
resources at the crucial stimuli when awareness occurs (see Logan, 1992).
Öhman (1993; Öhman & Wiens, 2004) postulated that such processes occur
for biologically relevant threats and evoke faster responses for theseparticular visual stimuli compared to other visual stimuli.
The idea that feared and fear-relevant animals would direct attention has
been also supported by the results from a series of visual search experimentsby Öhman, Flykt, and Esteves (2001) in which randomly selected participants were instructed to indicate the presence or absence of a target stimulusin 2/2 and 3/3 matrices of objects (i.e., grid pattern). Reaction times (RTs)for a fear-relevant target stimulus among fear-irrelevant distractor stimuli
were shorter than in the opposite situation (i.e., a fear-irrelevant target
stimulus among fear-relevant distractors). In the third experiment of thisseries, individuals were selected based on their score on a questionnaire that
evaluated their fear for snakes and spiders (see Klorman, Weerts, Hastings,
Melamed, & Lang, 1974). Fearful participants had shorter reaction times(RTs) in response to their feared target animal than to the nonfeared (butfear-relevant) one. With the exception of the feared target animal, fearfulparticipants did not differ in their RTs from the low/no fear control group.
To disentangle the effects of target from distractors, two follow-up studies(Flykt, 2005, 2006) were designed using all possible combinations of targets
and distractors within random samples of participants. The results suggest
an involvement of controlled processes in this paradigm*an initial effect of
the target stimulus on heart rate (HR) measure followed by an effect of the
distractors was shown (Flykt, 2005). Furthermore, when participants wererequired to withhold their responses for a certain time after the matrix
search array off-set, the results indicated that reaction times (RTs) are afunction of the number of fear-relevant pictures in the search arrays, themore fear-relevant pictures the shorter RTs (Flykt, 2006), reflecting apreparedness to act on potential threats.
The findings based on the visual search experiments by Flykt (2005, 2006)
suggest an initial effect of the target followed by effects of the distractors andsupport the Perceptual Load Theory introduced by Lavie (1995, 2005; Lavie& Tsal, 1994). Lavie postulated that when a task required a large amount of
resources, no additional resources are available for perceptual-parallel
processing. When, however, attentional demands are low, or working
memory load is requested, stimuli besides those in the focus of attention
would influence information processing (see Lavie, 2005). In the visual
search task framework, this theoretical position suggests that a search taskthat requires a lot of resources will not be affected by distractor stimuli, orFEAR AND PHYSIOLOGY IN VISUAL SEARCH

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even by aspects of the target stimulus, until the controlled processing of thesearch has been achieved.
In a modified replication and extension of the Öhman et al. (2001) study,
Lipp, Derakshan, Waters, and Logies (2004) have also found shorter RTs,
among randomly selected participants, when snake and spider stimuli were
exchanged for nonfear-relevant animals, such as horses and domestic cats.
This finding suggests that animals per se may have more response driving
properties than flowers and mushrooms. From an evolutionary point of view
it would be functional that objects that could potentially approach oradvance away from the observer, independently of their fear-relevance,
should elicit more activation, as they might necessitate a reaction.
When required to search for a mushroom among flowers, spider fearfulparticipants showed an increase in RTs when one of the flowers was replaced
by a picture of a spider (Miltner, Krieschel, Hecht, Trippe, & Weiss, 2004).
This increase in RTs could result from an attentional capture by the spider
picture. However, an alternative or complementary explanation of suchattentional bias would result from a problem in attentional disengagement
occurring after the detection of the feared animal. Problems to disengage
attention from threat have been proposed to be a central aspect ofattentional biases toward threat (Fox, Russo, Bowles, & Dutton 2001;
Fox, Russo, & Dutton, 2002). Consequently, the idea that fear-relevant (butnonfeared) animals would have response driving properties different thanthose of other animals in visual search tasks can be questioned based on the
results from Lipp et al. (2004). Nevertheless, when the feared animal is atarget in visual search tasks such as those used by Öhman, et al. (2001), it
would appear beyond doubt that fear for snakes or spiders decrease RTs forthe feared animal.
If fear for animals has response driving properties, whether genetically
predisposed or acquired, these properties could be based either on parallelperceptual processing or on more elaborate processing that require a certain
amount of resources to be available, as would be suggested by the Perceptual
Load Theory (Lavie, 1995, 2005). In the former case, the feared animal would
be processed independently of the perceptual load of the task and effects
should be shown in the Pl/Nl complex of event related potentials (ERPs),
two electrophysiological components modulated by spatial selective attention (see e.g., Luck, Woodman, & Vogel, 2000). Alternatively, if perceptualload would block responses to feared animals, no differential Pl/Nl responses
should be expected.
Consequently, event-related potentials (ERPs) represent a suitable
technique to investigate the processes that precede the behavioural outcome
from which attentional biases are inferred. Validly cued targets evoke larger
amplitude for the PI (90 130 ms) andNl (150 200 ms) ERP components
over the extrastriate occipital area for attended stimuli as compared to1078

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unattended stimuli (e.g., Mangun & Hillyard, 1991). Vogel and Luck (2000)
suggested that the Nl could represent a discrimination process. Thus, theinvestigation of such components allows the identification of the earliest
time point at which attention could play a role in the emotional processing ofvisual images. Another robust finding in the framework of ERP inprocessing of emotional picture content relies on an increased response,
occurring between 400 ms and 700 ms over the centroparietal electrodes, forpleasant and unpleasant stimuli as compared with neutral stimuli; the latepositive potential (LPP), relating to the intensity of the emotional stimulation (Cacioppo & Berntson, 1994; Crites, Berntson, & Coles, 1993;
Cacioppo, Crites, & Gardner, 1996; Cacioppo, Crites, Gardner, &Berntson, 1994; Cacioppo, Diedrich, Naumann, Maier, & Bartussek, 1997;
Schupp et al., 2000). It has been demonstrated that the exposure to negative
pictures evokes a larger positive component over the centroparietal regions
than positive pictures at about 500 ms (Ito & Cacioppo, 2000; Dolcos &Cabeza, 2002; Ito, Larsen, Smith, & Cacioppo, 1998). According to Schupp
et al. (2004) the existing results on LPP are consistent with the hypothesisthat it reflects an elaborated perceptual processing. Ito and Cacioppo (2000)
proposed that LPP reflects a competition for processing resources. However,whether the LPP component is modulated by the fear that a stimulus elicits
remains to be clarified.
In the present study participants were selected based on their responses
on reduced versions of the spider and snake fear questionnaires (Klorman etal., 1974) to form a snake fearful group, a spider fearful group, and a group,
not fearful of spiders or snakes (the nonfearful group). In both experiments
participants were required to detect whether a target was present in thematrix search array or not. In Experiment 1, participants were engaged in a
training phase and had to search for a target stimulus without responding.
During this phase, signals were acquired for the HR measure. In the second
phase, they were required to indicate their responses by pressing one out of
two buttons. In Experiment 2 (in which the signals for the ERPs wereacquired), participants were instructed to search for a target on all trials, but
to respond uniquely when the target stimulus was followed by a question
mark, which randomly occurred after the presentation of the matrix searcharray. We hypothesised that a feared target in comparison with other targets
would result in: (1) a different HR response pattern; (2) shorter RTs;and (3) would result in modulated patterns of brain activations. Such
activations would be shown in the Pl/Nl complex if pre-attentive processing
directed attention to the feared target. In the absence of preattentive
processing, the differential responses would not occur prior to the detectionof the target stimulus.

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EXPERIMENT 1
MethodParticipants. These were recruited from a sample of 250 first semester
students in psychology at University of Geneva who had completed shortversions (see Carlsson et al., 2004) of the snake (20 items) and spider (18items) questionnaires of Klorman, Weerts, Hastings, Melamed, and Lang
(1974). The use of only some items of the questionnaires was based on an
item analysis of the responses on the 30 Snake items and the 31 Spider itemsby the approximately 130 medical students who had filled in the originalquestionnaire in the Öhman et al. (2001) study (unpublished data). All
participants were French speakers and the questionnaires were translated
and completed in French.
The nonfearful group consisted of nine participants (three males) all
right-handed, with an average age of 24 years (SD /5, range 20 35 years).
Their mean spider score was 0.3 (SD /0.5, range 0 1) and their mean snake
score was 0.7 (SD/0.5, range 0 1). The spider fearful group consisted ofnine participants (one male) all right-handed, with an average age of 21
years (SD/2, range 19 24). Their mean spider score was 12.2 (SD /1.6,
range 10 15) and their mean snake score was 1.4 (SD /1.1, range 03). The
snake fearful group consisted of nine participants (all female) four righthanded, with an average age of 23 years (SD/5, range 19 33). Their mean
spider score was 1.4 (SD /0.5, range 1 2) and their mean snake score was
15 (SD /2.8, range 1119).
Stimulus materials. The same picture materials presented in 3 x 3 items(i.e., matrix) search arrays as in the Öhman, et al. (2001) study were adopted.
Each combination of a snake among flowers, a snake among mushrooms, aspider among flowers, a spider among mushrooms, a flower among
mushrooms, and a mushroom among flowers were presented in ninedifferent search array constellations. Aside from these 54 search arrays, anadditional 54 arrays with the target (the remaining combinations of targetand distractors) and 36 arrays without the target were used as filler trials.
Apparatus. The search arrays were presented on a 17 inch. (43 cm)
screen. The size of the search arrays was approximately 23.5 cm /15.5 cm
and the viewing distance was approximately 1 metre. The Experimental Run
Time System (ERTS; see Dutta, 1995) was used for the stimulus generationand collection of RTs with the EXKEY-logic and response pad. Theinterstimulus intervals (ISIs) varied randomly between 3 s and 4 s and in thesecond-phase the RT was added to the ISIs (maximum 2000 ms). BioPac
system (see e.g., Frazier, Strauss, & Steinhauer, 2004) MP100TEL with the1080

FLYKT AND CALDARA

dedicated software, AcqKnowledge 3.5 (see e.g., Leong, Mann, Wallymahmed, MacFarlane, & Wilding, 2001), was used for recording the
ECG signal and a signal indicating the stimulus presentation. The ECG
signal was sampled at 500 Hz.
Procedure. These were informed that the task was a pretest for an ERP
experiment, in which they were encouraged to participate in later. The
experiment comprised two phases. During the first phase, which waspresented as a training period, participants were instructed that they had
to perform the search task, but not to respond. In the second phase,participants were instructed to respond by pressing a button if the target waspresent or another button if the target was absent. Participants were required
to press a button with their nondominant hand if all the items in the searcharray belonged to one of the categories spiders, snakes, flowers, ormushrooms. If one picture in the display belonged to a different category
than the rest of the pictures a button had to be pressed with their dominanthand. Before starting the experiment ECG electrodes were attached (theground to the neck, the reference electrode to the right side about 10 cm
below the armpit, and the active electrode at about the same position on theleft side).
Design. As the focus of interest was the differences between feared,
nonfeared (but fear-relevant), and fear-irrelevant targets and to reduce thecomplexity of the results in terms of the ERP experiment only, these threedifferent conditions were used for the analysis. The conditions were: (1) asnake among flowers or mushrooms; (2) a spider among flowers or
mushrooms; and (3) a flower among mushrooms or a mushroom among
flowers. The design for the ANOVA had group (Snake fearful, Spider fearful,
Nonfearful) as between variable and target as within variable (Snake, Spider,
Fear-irrelevant).
Data treatment. Only the heart rate data obtained during the first (i.e.,‘‘the training’’) phase were used for the analysis. The peaks of the R-waves
were used for the calculation of interbeat intervals (IBIs). After visualinspection, artifacts were removed on all trials. No attempts to correct for
respiratory responses were made. The baseline consisted of the two entire
IBIs before stimulus onset. For the analysis of RT data only correct
responses were used. Violation of the sphericity assumption of repeatedmeasure ANOVA was corrected by the use of Greenhouse-Geisser to adjust
all probabilities (p). The original degrees of freedom were, however, used forreadability of the results. When t-tests were used Cohen’s (1988) d wasreported as an indicator of the effect size.

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Results
No significant differences were found for HR measures (see Table 1 formeans and standard deviations). The ANOVA for the RTs showed longer
RTs for fear-irrelevant targets (1040 ms) than snake or spider targets (both817 ms), as shown by a main effect of target, F(2, 24) /52.77, pB/.01,
MSE /9339, h2 /.69. The RTs were shorter for spider than for snake
targets in the spider fearful group, and shorter for snake than spider targets
in the snake fearful group, for the nonfearful group the mean RT was shorterfor spider targets than snake targets. This was shown by the interaction effectTarget /Group, F(4, 24) /2.94, p/.04, MSE /9339, h2 /.20 and a priori
t-tests. Spider target vs. snake target: Spider fearful (one-tailed); t(8) /4.25,
p B/.01, d/0.83, Snake fearful (one-tailed); t(8) / /2.11, p /.04, d/1.13,
and Nonfearful; t(8) /2.83, p/.03, d /0.61 (see Figure 1).

Discussion
No significant difference on HR measures was found between the different
conditions. The fearful groups showed shorter RTs for the feared target
animal than the other animal or the fear-irrelevant targets, replicating theÖhman et al. (2001, experiment 3) results. The nonfearful group showed
shorter RTs to spider targets than snake targets.
The results of a previous visual search study by the first author (Flykt,2005) revealed less heart rate deceleration to fear-relevant than fearirrelevant targets. Thus, at first sight, the absence of an effect in HR
measures in the present study may appear odd. It could, however, be
explained by a difference in the population under investigation *while theprevious study (Flykt, 2005) was conducted using randomly selectedparticipants, the current study involved participants who were selected on
the basis of a questionnaire relating to their fear of the investigated
TABLE 1Means (and standard deviations) of heart rate (HR) change scores(groups in columns and targets in rows)
HR change scores
Spider fearful

Snake fearful

Non fearful

Spider target
Mean (SD)/1.00 (1.54)

/1.32 (2.73)

/0.88 (1.53)

Snake target
Mean (SD)/1.41 (2.59)

/0.72 (1.92)

/1.54 (0.94)

Fear-irrelevant target
Mean (SD)/1.70 (2.37)

/0.48 (1.28)

/0.70 (1.13)

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Figure 1.

Mean reaction times (RTs) in ms. Displayed results are based on the condition’’A target
spider among flowers or mushrooms‘‘ (black bars), the conditions ’’A target snake among flowers or
mushrooms‘‘ (grey bars), and the condition ’’A flower among mushrooms or a mushroom among
flowers" (white bars) for the three groups, Snake fearful (n /9), Spider fearful (n/9) and Nonfearful(n/9). Vertical bars report the mean standard errors, the numbers displayed above report the mean
RT values (ms).

biological stimuli. The possibility of being exposed to their feared animal
could have resulted in anticipatory strategies that modulated the nature of
the responses involved in the detection of the feared animal or the detectionof another target. This anticipatory effect could then have interfered with aspontaneous evoked heart rate changes due to the target detection.
As expected, fear-irrelevant targets resulted in longer RTs than theother targets. Spider and snake fearful participants showed shorter RTs
for their respective feared target stimulus, compared to the other target
stimuli. However, shorter RTs to spider than snake targets in thenonfearful participants were observed. This difference in RTs could
reflect a general preferential processing of spider than snake targets,
which could be associated with faster central nervous processing for
spider than snake targets. To address this question and to investigate
whether, where and when feared animals are differentially processed withrespect to a nonfeared (but fear-relevant) animal, we adopted the visual
search paradigm with a simultaneous recording of the electroencephalographical activity.

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EXPERIMENT 2
MethodParticipants.
experiment.

The same participants as in Experiment 1 took part in thisStimulus materials. The same stimuli as in Experiment 1 were used inthis experiment.
Procedure. Participants were seated in a dimly illuminated and soundattenuated electrically shielded room, facing a colour-video monitor at a
distance of 120 cm. A fixation cross was continuously visible in the centre of
the screen. The total number of matrix search arrays presented to eachparticipant was 1872. Each image subtended a visual angle of 6.688 by 4.398.
Of these 1872 search arrays, 117 were presented for each combination oftarget and distractors (e.g., a snake among flowers, a spider among
mushrooms). Each matrix search array was presented for 1500 ms, withan ISI randomised between 1500 ms and 2500 ms between the different
presentations. Participants were instructed to search for a deviant picture
among a congruous category of pictures. On 272 of the trials a question
mark followed the matrix search array exposure. Only on these trials theparticipants were required to respond by differential key pressing dependenton whether a picture from a deviant category was present or not. Theseverification trials were used to keep a high level of attention and were
excluded for the analysis. The background colour of the monitor was black.
ERP recording and averaging. The EEG was recorded from 64 silver/
silver chloride electrodes. Of these, 62 were embedded in an elasticised cap
montage (QuickCap, NeuroScan Inc., USA), arranged according to theInternational 1020 system. An electrode was placed on the tip of the noseand used as a common reference for all the cap electrodes. Ocular artifacts
were recorded and monitored by using bipolar electrodes on the outercanthus of each eye, and vertical EOG was recorded from electrodes placed
above and below the eye. Vertical blinks were corrected off-line by anautomatic algorithm (Scan 4.2, Neuroscan Inc., USA). The sampling rate
was 1000 Hz (band pass 0.15 70 Hz). Electrodes impedances were kept
under 5 kV. EEG epochs extended from 200 ms before to 1500 ms after
stimulus onset. Data were baseline corrected to the first 200 ms of the epoch.
Epochs were carefully scanned, and the epochs presenting remaining
artifacts were rejected before averaging the individual evoked potentials.
Finally, a low-pass filter of 30 Hz was applied and the data were rescaled
across the average reference.

1084

FLYKT AND CALDARAERP analysis. To investigate the emotional effect of the stimuli, for thethree groups of subjects peak amplitudes and peak latencies were computedfor the matrix search arrays with a target stimulus (snake, spider, and fearirrelevant) among fear-irrelevant stimuli (mushrooms or flowers) in threetime windows: between 90 ms and 150 ms (PI), 120 ms and 190 ms (Nl) and,after visual inspection, 500 ms and 700 ms poststimulus onset (LPP). These
values were calculated with an automatic algorithm for each selected
electrode and each condition at a single latency per component and pereach subject. The electrodes of interest for the Pl/Nl complex were P3, P03 in
the parietooccipital area of the left hemisphere, and P4, P04 for the righthemisphere. For the LPP component three Regions Of Interest (ROI) of nineelectrodes each were defined in the central part of the scalp. The left ROI
was defined by pooling and average the activity on FT7, FC5, FC3, T7, C5,
C3, TP7, CP5, CP3 electrodes; for the central ROI on the FC1, FCZ, FC2,
CI, CZ, C2, CP1, CPZ, CP2 electrodes; and finally for the right ROI on the
FT8, FC6, FC4, T8, C6, C4, TP8, CP6, CP4.
Design. Analyses of variance (ANOVAs) with group (Snake fearful,
Spider fearful, Nonfearful) as a between-subject factor and target (Snake,
Spider, Fear-irrelevant), Hemisphere (Left, Right for the Pl/Nl complexLeft, Central, and Right for the LPP) and electrodes (for the Pl/Nl complex)
as within-participant variables were conducted for peak amplitudes andlatency. Violation of the sphericity assumption with a repeated-measures
ANOVA was corrected by the use of Greenhouse-Geisser to adjust all
probabilities (p). The original degrees of freedom were, however, used forclarification of the results.

Results
For the Pl-Nl complex: The PI amplitude was larger over the P- (6.86 mV)than PO-electrodes (5.87 mV), F(l, 24)/12.11, pB/.01, MSE /6.52, h2 /.34.
The PI peak latency occurred later for the P- (114 ms) than the POelectrodes (110 ms), F(l, 24) /4.48, p B/.05, MSE /244.90, h2 /.16. The
latency for the PI was shorter for the right (111 ms) than the left hemisphere(113 ms), F(1, 24) /6.05, p/.03, MSE /95.37, h2 /.20. There was also a
Target /Electrode /Hemisphere/Group interaction effect, F(4, 48) /3.23,
p /.04, MSE /29.69, h2 /.21. No reasonable interpretation could be madefor this interaction, or for the Target /Electrode /Hemisphere /Group
interaction effect for the Nl amplitude, F(4, 48) /2.63, pB/.05, MSE /0.22,
h2 /.18. The Nl latency for the PO-electrodes (155 ms) was shorter than for
the P-electrodes (161 ms), F(1, 24) /23.26, p B/.01, MSE /146.43, h2 /.49.
The latency for the right hemisphere (156 ms) was shorter than for the left
hemisphere (160 ms), F(1, 24) /5.34, p /.04, MSE /197.45, h2 /.18.

FEAR AND PHYSIOLOGY IN VISUAL SEARCH

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A positive component between 500 ms and 700 ms from stimulus onset(LPP, see Table 2 and Figure 2a and 2b) showed larger amplitudes for spider
targets (4.42 mV) than fear-irrelevant targets (3.51 mV), F(2, 48) /3.82,
p /.03, MSE /4.38, h2 /.14, and Bonferroni corrected pairwise comparisons. In the spider fearful group spider targets resulted in larger amplitude(5.92 mV) than snake and fear-irrelevant targets (3.95 and 3.72 mV,
respectively), and in the snake fearful group the snake target resulted in alarger amplitude (4.74 mV) than spider and fear-irrelevant targets (3.61 and3.09 mV, respectively). In the non-fearful group there was no difference
between the three different targets. This was shown by an interaction effectbetween target and group, F(4, 48) /4.84, pB/.01, MSE /4.38, h2 /.29, anda priori t-tests. Spider target vs. snake target: Spider fearful (one-tailed);
t(8) / /2.70, p /.02, d/0.93, Snake fearful (one-tailed); t(8) /3.09, pB/.01,
d /0.66, and Nonfearful; t(8) / /0.40, p / .69 (see Figure 2). The central
ROI had a higher maximum amplitude (4.26 mV) than the left (3.73 mV) andthe right (3.80 mV) ROIs, F(2, 48) /13.57, pB/.01, MSE /0.56, h2 /.36.
The ANOVA for the latency of the maximum amplitude of the LPP
showed a shorter latency for the spider targets (590 ms) than for the fearirrelevant targets (604 ms), as shown by a main effect of target, F(2, 48) /
3.48, pB/.01, MSE /1253.31, h2 /.13, and Bonferroni corrected pairwise
comparisons. The latency of the maximal LPP amplitude was shorter for theleft ROI for the spider targets (586 ms) than for the central (593 ms) and theright (592 ms) ROIs, as shown by an interaction between target and ROI,
F(2, 96) /2.78, pB/.05, MSE /44.61, h2 /.10, and corrected pairwise
comparisons.
TABLE 2
Mean amplitudes (mV) and latencies (ms) values for the late positive
potential (LPP) component (groups in columns and targets in rows)
LPP (500 700 ms)
Spider fearful

Snake fearful

Non fearful

Spider target
Amplitude (mV)
Latency (ms)

5.92
588

3.61
591

3.72
592

Snake target
Amplitude (mV)
Latency (ms)

3.95
602

4.74
591

3.46
607

Fear-irrelevant target
Amplitude (mV)
Latency (ms)

3.72
610

3.09
607

3.72
596

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Figure 2a. Event-related potential (ERP) maps for the time window 500 700 ms late positive
potential (LPP) after stimuli onsets rescaled across the average reference. All maps are viewed from thetop, with the nose up and the left ear to the left (red/positive in activity in relation to the reference,
white /no difference in activity in relation to the reference, and blue/decrease in activity in relation
to the reference) for the three groups Spider fearful (n/9), Snake fearful (n/9), and Nonfearful (n/9). The upper row shows the activity over the scalp for the condition: ‘‘A target spider among flowers
or mushrooms’’. The middle row shows the activity over the scalp for the condition: ‘‘A target snake
among flowers or mushrooms’’. The lower row shows the activity over the scalp for the condition: ‘‘Atarget flower among mushrooms or a mushroom target among flowers’’. [View the Figure online to seea colour version.]

Discussion
The ERP analyses comparing the Pl/Nl component for the feared and the
not feared target animals or the fear-irrelevant targets did not reveal any
difference in terms of amplitude or latency. However, the LPP component
showed a larger amplitude for the feared animal than the nonfeared animal
and the fear-irrelevant targets.
The Nl was expected to evoke larger amplitudes for attended stimuli than
not attended stimuli (Mangun & Hillyard, 1991), representing a discrimination processing (Vogel & Luck, 2000). The absence of any differential
responding at the Pl/Nl in the present experiment indicates that no early
differentiation between the different target stimuli took part. Our data
indicate instead a more elaborated perceptual processing (Schupp et al.,2004) or a competition for resources (Ito & Cacioppo, 2000) by showing
more enhanced amplitude of the late positive potential (LPP; 500700 ms)
for the feared stimulus than for the other animal (and the fear-irrelevant)FEAR AND PHYSIOLOGY IN VISUAL SEARCH

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Figure 2b. Grand-averaged event-related potential (ERP) waveforms rescaled across the averagereference at central electrodes (C3, CPZ, C4) in response to Spider, Snake, and Neutral (flowers andmushrooms) detections, within spider fearful (top), snake fearful (middle) and Nonfearful participants(bottom). Positive values are up. Note the occurrence of an enhanced LPP in fearful participants
detecting their respective feared animal, and a similar response for all the visual categories in the
Nonfearful participants.

targets. Such modulation for the LPP component might reflect a differencein the arousal evoked by the feared animal target as compared to the othertargets. This arousal would be considered an integrated part of a fear
response (see e.g., Fanselow & Lester, 1988; Lang, Bradley, & Cuthbert,
1997) and not as a separate dimension as pr’evious’argued by Schupp et al.
(2004).
The main effect due to shorter latency of the maximum amplitude of the
LPP for spider targets than the fear-irrelevant targets might indicate thatspiders in general are faster processed than snakes. This speed difference
resonates with the difference in the RTs of the first experiment for the nonfearful participants.

GENERAL DISCUSSION
Our results are consistent with Öhman et al.’s (2001) findings, as they show
shorter RTs to the feared animal in the fearful groups. ERP data from the1088

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same participants added important information to previous findings, byshowing enhanced LPP amplitude to feared animal targets compared to thenonfeared (but fear-relevant) animal targets. Early ERP components wereshown not sensitive for discriminating between the feared and nonfearedtarget animals. As a consequence, three important results were established inour study, which we discuss in turn.
First, the larger amplitude of the LPP component observed in fearfulparticipants for the feared animal targets, compared to the nonfeared animal
targets, is in line with previous findings showing a more enhanced LPP
component for unpleasant than neutral stimuli (Cacioppo & Berntson, 1994;
Cacioppo, Crites, Berntson, & Coles, 1993; Cacioppo, Crites, & Gardner,
1996; Diedrich et al., 1997; Cacioppo, Crites, Gardner, & Berntson, 1994).
Our pattern of results is also in line with some studies that have shown amodulation of the LPP component for unpleasant compared to pleasantstimuli (e.g., Dolcos & Cabeza, 2002; Ito et al., 1998; Schupp et al., 2004).
By selecting the participants for being fearful of one particular animal(e.g., spider), but not another animal (i.e., snake), an interaction wasobserved between the feared object and the nature of the fear in theparticipants, providing the first direct evidence for fear related modulationon the LPP component. The feared animal condition elicited a larger LPP
compared to the nonfeared (but fear-relevant) animal condition. Thus, the
LPP component might reflect an elaborated perceptual processing (Schupp
et al., 2004), or a competition for resources (Ito & Cacioppo, 2000)
modulated by participants’ fearfulness of the visual stimulus. Such acompetition for resources might, with respect to a feared animal, be related
to an allocation of processing resources to handle the threat stimulus. Froman evolutionary view an efficient handling of the threat with speeded actions
would per se be more important than a fast detection of the threat per se(Flykt, 2006).
Second, the absence of an expected difference in the Pl/Nl complex
between feared and nonfeared target conditions for the fearful groups does
not favor an early perceptual-parallel process that would direct attention
towards the feared target and result in a faster detection and subsequently
shorter RTs to feared target stimuli, as suggested by Öhman et al. (2001).
However, such early fear related processing might occur in the amygdala
nuclei (see e.g., LeDoux, 1996) rather than in the activity of the extra-striate
cortex captured in the Pl/Nl complex. The activations arising from theamygdala are not directly recordable with the ERP technique. As aconsequence, any conclusion on the involvement of that particular structureof the brain in our experiment would be speculative. Our results can only
support an absence of an attentional modulation within the Pl/Nl complex.
However, an alternative interpretation would rely on the fact that an
attentional bias in processing visual information would occur only when theFEAR AND PHYSIOLOGY IN VISUAL SEARCH

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target has been detected. As demonstrated by previous findings (Flykt, 2005,
2006) and in accordance with the Perceptual Load Theory (Lavie, 1995,
2005), when excessively large resources are needed for the search of thetarget the distractors are inhibited during the search process. This inhibition
might have modulated the search process and the occurrence of theattentional bias, a bias that will not take part until the target is detected.
The paradigm and the technique that we adopted do not permit to exclude
such alternative explanation.
Third, as previously found by Öhman et al. (2001), we observed shorter
RTs for the detection of the feared animal target compared to the nonfearedanimal within the fearful groups. Critically, these RTs had a reversed relation
with the LPP amplitude (i.e. larger amplitudes-shorter RTs/smaller amplitudes-longer RTs). Another interesting aspect of our results is reflected in theabsence of a differentiation in LPP amplitude between spider and snake
targets in the nonfearful group despite the difference in RTs. However, there
was generally a shorter LPP latency for spider targets than fear-irrelevanttargets, while this difference was not present between snake targets and fearirrelevant targets. Thus, this difference in latency might have favoured
shorter RTs for spider targets and offer a possible interpretation of theshorter RTs shown for spider targets among the nonfearful participants inthe first experiment.
In conclusion, to our knowledge this is the first study that has shown a
differentiation between a feared and a nonfeared (but fear-relevant) animal
for the LPP component. This difference was reinforced by RT data, whichshowed a comparable pattern of results for fearful participants. No
significant effects were found for the HR or Pl/Nl attentional complex.
The present findings suggest that the different processing occurs when thetarget stimulus had been attended, but no indicators for that such a
differentiation would occur before the stimulus is attended were shown. The
inconsistency with previous results suggesting an early differentiation (e.g.,
Schupp et al., 2004) might be due to the more complex stimuli used in thepresent study. The emerging question is the functionality of the latedifferential responding of the LPP component.
Manuscript received 1 December 2004
Revised manuscript received 16 September 2005

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