Men fear other men most: Gender specific brain activations in. perceiving threat from dynamic faces and bodies. An fmri. study.

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1 Men fear other men most: Gender specific brain activations in perceiving threat from dynamic faces and bodies. An fmri study. Kret, ME, Pichon, S 2,4, Grèzes, J 2, & de Gelder, B,3 Cognitive and Affective Neurosciences Laboratory, Tilburg University, Tilburg, the Netherlands. 2 Laboratoire de Neurosciences Cognitives, U960 INSERM & Département d Etudes Cognitives, Ecole Normale Supérieure, Paris, France. 3 Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA, USA. 4 Laboratory for Neurology and Imaging of Cognition, Department of Neuroscience, Medical School, University of Geneva Switzerland Correspondence: Beatrice de Gelder Department of Radiology-Massachusetts General Hospital Athinoula A. Martinos Center, Building 36, Room 409 First Street Charlestown, MA 0229 Telephone 67/ degelder@nmr.mgh.harvard.edu

2 We report a functional magnetic resonance imaging experiment showing different activation patterns as a function of threatening signals from facial or bodily expressions and these differed between male and female participants as a function of male and female actors. Male observers showed a clear motor preparation response to threatening male body language. Facial and bodily expressions are among the most salient affective signals regulating our daily interactions and they have a strong biological basis -3. Therefore it stands to reason that gender figures prominently among factors that determine affective communication. For example, activation in superior temporal sulcus (STS) is stronger in men than women in response to faces denoting interpersonal superiority 4. We tend to view a physically strong male expressing threat with his body language as dangerous. Others will say that there is nothing scarier than an angry woman. But it is not yet known whether gender effects depend on the gender of the observed stimulus as well as on that of the observer. We used functional magnetic resonance imaging (fmri) to investigate whether () female and male observers respond differently or not to observed threatening facial or body expressions (2) this putative gender difference depends or not on the gender of the observer; and whether (3) male actors trigger the threat system and the motor preparation system more than female actors depending or not on the gender of the observer. Twenty-eight healthy right handed adults (4 females, mean age 9.8 years old, range 8-27 years old; 4 males; mean age: 2.6 years old, range 8-32 years old) who gave informed consent took part in the experiment. Half of the participants viewed neutral and angry and the other half neutral and fearful face and body expressions (see Supplementary Methods). All stimuli have been validated previously 5. The videos had a duration of

3 ms. An oddball task was used to control for attention and required participants to press a button each time an inverted video-clip appeared so that trials of interest were uncontaminated by motor responses. Imaging data were analyzed in SPM2. Face- and body-sensitive voxels in the extrastriate body area (EBA), fusiform face/body area (FFA/FBA), STS, amygdala (AMG), temporo-parietal junction (TPJ) and pre supplementary motor area (pre-sma) were identified using a separate localizer scan session in which participants performed a one backward task on face, body, house and tool stimuli and regions of interest were created by using a 5mm sphere around the peak activation (see Supplementary Table ). Beta values were extracted and served as factors in an ANOVA: face threat male and female, face neutral male and female, body threat male and female, and body neutral male and female. Gender of the observer was included as a between subjects variable (see Supplementary Methods). As indicated by recognition data obtained afterwards, male and female participants recognized all expressions equally well (see Supplementary Figure ). Overall, a higher BOLD response in pre-sma, EBA and STS was found when participants observed male versus female actors expressing threat. But interestingly, in these regions, as well as in FFA/FBA, we observed an interaction between category, emotion and observer; more activation for male threatening versus neutral body stimuli in the male participants was observed. Threatening bodies and not faces triggered highest activity in STS, specifically in male observers. In male monkeys, STS was also most active for conspecific threatening body postures 6 (see Figure 2). The AMG was more active for facial than bodily expressions, independent of emotion, yet specifically for male observers watching female faces. This is consistent with findings that AMG activity in male observers was increased for viewing female faces with relatively large pupils indicating an index of interest 7. 3

4 Possibly, female faces provide more information to relevant males than male faces, whereas the distinction at the level of the face between male and female faces is less important for female observers 8. Other studies have reported that AMG is face but not emotion specific 9. But the striking fact here is that the other areas that reflect sensitivity of the male observers are all emotion sensitive. This disjunction between AMG face-gender and STS, EBA, pre- SMA gender-emotion sensitivity indicates that AMG indeed plays a different role than being at the service of emotion encoding and fits with the notion that it encodes salience and modulates recognition and social judgment 0, hence the face-gender effect. Common belief is that men express emotion because the situation warrants it, whereas females express emotions because they are just being emotional. Our results belie this intuition. So, if we see an emotional male, something real must be going on and the observer has to decide whether to flight or fight, explaining the enhanced responses to male threatening body expressions in EBA, STS and pre-sma. While our results are similar to previous reports that show male observers to be more reactive to threatening signals than females 4, 2, previous studies used faces and did not take the gender of the actor into account. Whereas EBA and STS showed a main effect of emotion, pre-sma specifically showed increased activation for threatening versus neutral male actors as observed in male participants. (see Supplementary Results). It is well known that activity in the pre-sma increases with action preparation to generate an escape response 3 and it has been found responsive to threatening body expressions before 4. This is the first study that shows that males show a strong preparation to move or act as measured by the pre-sma response when they are confronted with another males threatening body expression. Insert Figure 2 4

5 Acknowledgments - Supported by Nederlandse Organisatie voor Wetenschappelijk Onderzoek, (NWO, ), Human Frontiers Science Program RGP54/2004 and European Commission (COBOL FP6-NEST ).. de Gelder, B. Nat. Rev. Neurosci. 7, (2006). 2. Darwin, C. The expression of the emotions in man and animals (John Murray, London, 872). 3. De Waal, F.B. No imitation without identification. Behav. Brain. Sci. 2, 689 (998). 4. Aleman, A. & Swart, M. PLoS One 3, e3622 (2008). 5. Kret, M., Pichon, S., Grèzes, J. & de Gelder, B. NeuroImage (in press). 6. de Gelder, B. & Partan, S. Neuroreport 20, (2009). 7. Demos, K.E., Kelley, W.M., Ryan, S.L., Davis, F.C. & Whalen, P.J. Cereb. Cortex 8, (2008). 8. Andersson, M. Sexual selection (Princeton: Princeton University Press, 994). 9. van der Gaag, C., Minderaa, R.B. & Keysers, C. Soc. Cogn. Affect. Neurosci. 2, (2007). 0. Tsuchiya, N., Moradi, F., Felsen, C., Yamazaki, M. & Adolphs, R. Nat. Neurosci 2, (2009).. Barrett, L.F. & Bliss-Moreau, E. Emotion 9, (2009). 2. Fine, J.G., Semrud-Clikeman, M. & Zhu, D.C. Behav. Brain. Res. 20, (2009). 3. Kwan, C.L., Crawley, A.P., Mikulis, D.J. & Davis, K.D. Pain 85, (2000). 4. Grèzes, J., Pichon, S. & de Gelder, B. Neuroimage 35, (2007). 5

6 Figure 2. Threatening facial and bodily expressions as a function of gender differences Extrastriate Body Area MNI ; Superior Temporal Sulcus MNI ; x F M F M F M F M observer Pre-Supplementary Motor Area MNI ; F M F M F M F M observer -0.5 F M F M F M F M observer Blood oxygenation level-dependent response measured by functional magnetic resonance imaging face female actor face male actor body female actor body male actor p <.05 p <.0 p <.005 p <.00 Fig. 2. The figures represent difference scores between cortical activations elicited by threatening and neutral videos. The superior temporal sulcus, extrastriate body area and pre-supplementary motor area were active following bodily expressions, especially when threatening, even more so when expressed by a male actor and above all when observed by a male participant. Whereas the extrastriate body area and the superior temporal sulcus showed main effects for threat and bodily signals, the pre-sma showed a very specific action preparation response in male observers when watching male threatening body expressions.

Supporting Information

Supporting Information Lingnau et al. 10.1073/pnas.0902262106 Fig. S1. Material presented during motor act observation (A) and execution (B). Each row shows one of the 8 different motor acts. Columns in