Gender differences in the processing of standardized emotional visual

stimuli in humans: a functional magnetic resonance imaging study

Jana Wrasea, Sabine Kleinb, Sabine M. Gruesserc, Derik Hermannb, Herta Florb, Karl Mannb,Dieter F. Brausb, Andreas Heinza,*

aDepartment of Psychiatry, Charite-University Medicine Berlin, Campus Charite Mitte, Schumannstrasse 20/21, 10117 Berlin, GermanybCentral Institute of Mental Health, Mannheim, Germany

cDepartment of Psychology, Humboldt-University of Berlin, Berlin, Germany

Received 19 February 2003; received in revised form 15 April 2003; accepted 5 May 2003

Abstract

Pictures from the International Affective Picture System were used in a functional magnetic resonance imaging study to assess gender

differences in brain activation in ten male and ten female volunteers. The affectively positive, negative and neutral pictures were presented

for 750 ms in a single event design and were carefully matched for arousal, valence and stimulus content. Men and women showed no

significant difference in valence, arousal, skin conductance response and startle modulation. Only in men was amygdala activation observed

in the pleasant condition. Furthermore, men showed a stronger brain activity for positive visual stimuli than women in the frontal lobe

(inferior and medial frontal gyrus). In women, stronger brain activation for affectively negative pictures was observed in the anterior and

medial cingulate gyrus. These results indicate that it is crucial to take gender differences into account when emotional paradigms are used in

functional brain imaging.

q 2003 Elsevier Science Ireland Ltd. All rights reserved.

Keywords: Gender differences; International Affective Picture System; Emotion; Pictures; Functional magnetic resonance imaging

Although several studies have suggested that gender

differences in emotional processing may have neuroanato-

mical correlates [8,9], so far only few brain imaging studies

based on faces and erotic visual stimuli are available [13,14,

18]. There is no study that directly tested this hypothesis

with standardized visual stimuli. Emotions can readily be

classified with respect to arousal and valence [2]. A

frequently used, standardized method to evoke and assess

emotions with respect to these dimensions is the Inter-

national Affective Picture System (IAPS) [4]. In this

paradigm, a large series of pictures with emotional content

were rated and validated in different cultural contexts. In

spite of the frequent clinical use of this paradigm [6], so far

only few brain imaging studies have been published that

used the IAPS to elicit emotions and to compare the

associated brain activation in men and women [3]. Canli

et al. demonstrated stronger right amygdala activation in

men and left amygdala activation in women, when subjects

remembered unpleasant pictures. However, this study did

not use positive stimuli and did not report gender differences

when subjects viewed the pictures directly [3]. We

examined brain activation directly elicited by positive and

negative IAPS and assessed gender differences.

Ten men (mean age 43.2 years, SD 7.32) and ten women

(mean age 40.0 years, SD 6.70), all right-handed, partici-

pated in the study after providing informed written consent

according to the Declaration of Helsinki. The Ethics

Committee of the University of Heidelberg approved the

study. Standardized clinical assessment with the Structured

Clinical Interview I was performed to exclude axis I

psychiatric disorders according to DSM IV and ICD 10.

Women were tested for pregnancy and drug abuse with

regular urine drug tests.

For emotion induction affectively negative, positive and

neutral pictures were used. Each category consisted of 18

pictures. Positive and negative cues were taken from the

IAPS and are standardized for the basic dimensions of

emotion: arousal and valence, as rated with the Self-

Assessment Manikin (SAM) on a scale from 1 to 9 [2,4].

Since both genders respond to the same affective pictures

differently [4], we matched affective pictures that have been

0304-3940/03/$ - see front matter q 2003 Elsevier Science Ireland Ltd. All rights reserved.

doi:10.1016/S0304-3940(03)00565-2

Neuroscience Letters 348 (2003) 41–45

www.elsevier.com/locate/neulet

* Corresponding author. Tel.: þ49-30-450517153; fax: þ49-30-

450517921.

E-mail address: andreas.heinz@charite.de (A. Heinz).

reported to elicit the same level of valence and arousal in

men and women [4]. The pictures were also matched for

content, since we chose the same number of pictures for the

themes: family, nature, sports and erotic. In a second step,

we used SAM ratings [2], skin conductance response and

the affect-modulated eye blink startle reaction [11] to

confirm that these pictures indeed elicit the same level of

self-reported arousal, valence, skin conductance and startle

response in men and women (Table 1).

The stimuli were presented in an event-related design for

750 ms and were arranged in an individually randomized

order for each subject. To reconstruct the BOLD (blood

oxygen level dependence) event-related time-course, we

sampled data points at different peristimulus time points

using a random jitter between the intertrial interval and the

acquisition period. This resulted in an equal distribution of

data points after each single stimulus. The intertrial interval

was randomized between 9.9 and 19.8 s. During the

intertrial interval a fixation cross was presented.

A 1.5 T clinical whole-body tomograph (Magnetom

VISION; Siemens, Erlangen, Germany) equipped with a

standard quadrature head coil and the automatic Siemens

MAP shim were used. For fMRI, 24 slices were acquired

every 3.3 s (4 mm thickness, 1 mm gap) using a standard

EPI-Sequence (TR ¼ 1:8 ms, TE ¼ 66 ms, a¼ 908) with an

in-plane resolution of 64 £ 64 pixels (FOV 220 mm). A

morphological 3D T1-weighted MPRAGE (magnetization

prepared rapid gradient echo) image data set (1 £ 1 £ 1

mm3 voxel size, FOV 256 mm, 162 slices, TR ¼ 11:4 ms,

TE ¼ 4:4 ms, a¼ 128) covering the whole head was

acquired for anatomical reference.

Data were analyzed with Statistical Parametric Mapping

(SPM99; Welcome Department of Neurology, London,

UK). The structural 3D data set was co-registered to the first

T2* image and was spatially normalized to a standard

template using a 12-parameter affine transformation with

additional nonlinear components. A nonlinear transform-

ation was subsequently applied to the T2* data. The

functional data were smoothed using an isotropic Gaussian

kernel for individual analysis (6 mm Full Width Half

Table 1

Subjective ratings of valence, arousal, skin conductance response (SCR) and affect-modulated startle reaction to different affective pictures in women and men

Women Men t P Women Men t P Women Men t P

Valence 7.7 ^ 1.0 7.0 ^ 2.5 20.8 0.4 2.0 ^ 0.7 1.5 ^ 1.2 21.1 0.3 5.6 ^ 0.9 5.9 ^ 2.4 0.3 0.8

Arousal 3.8 ^ 1.3 4.4 ^ 1.7 0.8 0.5 4.9 ^ 1.4 4.6 ^ 3.5 21.9 0.9 2.0 ^ 1.6 2.0 ^ 1.5 21.9 0.9

SCR 0.2 ^ 0.2 0.2 ^ 0.1 0.04 0.9 0.3 ^ 0.2 0.3 ^ 0.0 20.2 0.8 0.1 ^ 0.1 0.2 ^ 0.1 20.8 0.4

Startle 73 ^ 37 101 ^ 91 20.7 0.5 76 ^ 56 129 ^ 151 20.8 0.4 90 ^ 48 85 ^ 74 0.1 0.9

Values are given as the mean ^ SD.

Table 2

Increased activation elicited by emotionally positive vs. neutral visual stimuli in (a) men, (b) women and (c) men compared to women (P , 0:001, uncorrected)

Areas Side Talairach coordinates t value

x y z

(a) Men

Amygdala Left 221 29 212 6.89

Right 24 24 215 4.46

Inferior frontal gyrus BA 47 Left 245 28 217 4.60

BA 47 Right 56 26 21 8.41

Temporo-parietal junction BA 39/22 Left 250 269 20 7.98

BA 39/22 Right 59 243 8 5.89

(b) Women

Temporo-parietal junction BA 39/22 Left 253 266 12 4.68

BA 39/22 Right 62 240 19 4.37

Middle temporal gyrus BA 39 Right 53 264 6 5.79

(c) Men . women

Amygdala Left 221 29 27 3.91

Inferior frontal gyrus BA 47 Left 242 28 214 3.65

Right 33 28 217 4.73

Medial frontal gyrus BA 10 Left 29 56 14 3.98

Right 12 56 11 5.49

Fusiform gyrus BA 37 Left 227 239 213 3.67

BA 37 Right 30 250 210 4.07

J. Wrase et al. / Neuroscience Letters 348 (2003) 41–4542

Maximum (FWHM)) and for group analysis (12 mm

FWHM).

Statistical analysis was performed by modeling the

different conditions (positive, negative, neutral; delta

functions convolved with a synthetic hemodynamic

response function and its time derivative) as explanatory

variables within the context of the general linear model on a

voxel-by-voxel basis. Data were analyzed for each subject

individually (threshold P , 0:001, uncorrected). To detect

between-group differences, the contrast images of all

subjects of each group (male and female subjects) were

included in a second level random effects analysis

(threshold P , 0:001, uncorrected).

In men, positive compared to neutral pictures bilaterally

activated the amygdalae, the inferior frontal gyrus (BA 47)

and the temporo-parietal junction (BA 22/39). The amyg-

dala activation was more pronounced on the left side.

Women showed a significant BOLD-response only in the

temporo-parietal junction (BA 22/39) (Table 2, Fig. 1).

In a direct comparison of the brain activation between

men and women the inferior frontal gyrus (BA 47) and the

left amygdala remained significant. Additionally the

interaction analysis revealed differential bilateral activation

in the medial frontal gyrus (BA 10) and the fusiform gyrus

(BA 37) for men vs. women when positive pictures were

presented (Table 2, Fig. 1).

Negative emotional pictures elicited a significant acti-

vation of the right inferior frontal gyrus (BA 45, 47) and the

temporo-parietal junction (BA 22/39) in women and men.

Due to a priori hypotheses of amygdala activation in

response to aversive stimuli [10], we tested brain activation

at a very liberal significance threshold of P , 0:05; both

genders exhibited right amygdala activation. When we

corrected for region of interest, amygdala activation

remained significant only in women. Furthermore, only

female subjects showed activation in the medial (BA 24)

and the anterior cingulate (BA 33) (Table 3). The direct

comparison between women and men revealed no signifi-

cant differences at a significance level of P , 0:001.

One of the fundamental issues in emotion and gender

research is that the same visual stimuli elicit different levels

of arousal and valence in men and women [15]. As a

consequence, both genders were presented with pictures of

similar contents matched for arousal, valence, skin con-

ductance response and startle reactivity. When exposed to

pleasant pictures, men displayed more amygdala and

prefrontal activation compared to age-matched women.

Women demonstrated more cingulate activation when

looking at unpleasant pictures. Other studies that assessed

gender differences used emotional faces or erotic scenes

[13,14,18]. We used pictures from the IAPS that are

internationally standardized for arousal and valence [4].

To the best of our knowledge, there is only one study in

which brain activation elicited by negative IAPS stimuli was

measured in women and men separately [3]. When the

volunteers in this study remembered affectively negative

pictures, men showed a stronger activation in the right and

women in the left amygdala [3]. In accordance with this

study men showed a trend to activate the right amygdala

when confronted with aversive visual stimuli. In contrast to

Fig. 1. Positive vs. negative pictures in women and men. The left column shows brain activation in the inferior frontal gyrus, the temporo-parietal junction and

the amygdalae in ten men. The middle column demonstrates no activation in these regions in ten women except for the temporo-parietal junction. The right side

represents the group comparison (two sample t-test) for the contrast men . women. The amygdala is visible in the coronar slice. The medial and the inferior

frontal gyrus can be seen in the 3D brains. For the purpose of presentation the significance threshold in the 3D rendered pictures was set to P , 0:005. The

amygdala activation in the contrast men . women (coronar slice) is shown with a significance level of P , 0:001.

J. Wrase et al. / Neuroscience Letters 348 (2003) 41–45 43

Canli et al. [3] we observed not left but right amygdala

activation in women. However, the right amygdala

activation found in women in our study is in accordance

with other studies measuring the direct response to aversive

stimuli [20].

The orbitofrontal and medial frontal cortex respond to

the reward value in a nonlinear way: the response is

enhanced for the lowest and highest reward [7,12,16]. In this

study, only men showed orbitofrontal cortex activation to

positive and negative pictures.

When affectively negative visual stimuli were presented,

only women activated the anterior cingulate, a region

known to integrate attention and emotion [19]. The anterior

cingulate was also activated during the presentation of

noxious thermal and aversive gustatory stimuli [1,20] and

plays an important role in pain processing [1,5]. Recent

studies showed that females are more sensitive to painful

experience than males [17]. Our study may indicate that

women show a more sensitive central processing to aversive

material in general. This finding could contribute to the

understanding of higher depression/anxiety rates in women.

Further studies are needed to address this issue.

In summary, pleasant and unpleasant visual stimuli

activated different neuronal structures in women and men.

These results emphasize that both genders may have to be

analyzed separately when fMRI paradigms including

emotional stimuli are used. This may also be important

when using IAPS in fMRI studies with patients.

Acknowledgements

This study was supported by the Deutsche Forschungs-

gemeinschaft (He 2597/4-1).

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