- Email: [email protected]
Differential amygdala activation during simulated personal space intrusion by men and women
NSC 17109
No. of Pages 5
31 May 2016 Please cite this article in press as: Wabnegger A et al. Differential amygdala activation during simulated personal space intrusion by men and women. Neuroscience (2016), http://dx.doi.org/10.1016/j.neuroscience.2016.05.023 1
Neuroscience xxx (2016) xxx–xxx
3
DIFFERENTIAL AMYGDALA ACTIVATION DURING SIMULATED PERSONAL SPACE INTRUSION BY MEN AND WOMEN
4 5
ALBERT WABNEGGER, VERENA LEUTGEB AND ANNE SCHIENLE *
6
Clinical Psychology, University of Graz, BioTechMedGraz, Austria
2
7
amygdala lesion lacked any sense of PS (Kennedy et al., 2009). The amygdala is a central structure for the initiation of defense responses (LeDoux, 2014) and by that mediates self-protection. In addition, PS processing is associated with activation of visuo-tactile neurons in the parietal cortex, the putamen and the premotor cortex as demonstrated by a convergent series of studies in animals and humans (Graziano and Cooke, 2006; Brozzoli et al., 2012). These studies showed that spatial proximity recruits brain areas which are sensitive to touch. Not only actual touch, but also the observation of another person being touched, or another person coming closer, recruits touch-sensitive neurons (e.g., Schaefer et al., 2012; Schienle et al., 2015, 2016). Interestingly, PS is a dynamic perception which is influenced by different moderating variables such as the sex of the approaching person. When participants are asked to draw a PS bubble around a silhouette representing their own person it is a consistent finding that women prefer greater interpersonal distance to the opposite sex compared to men (e.g., Schienle et al., 2015). This effect can also be shown when a behavioral technique, the stop-distance task, is used (e.g., Miller et al., 2013; Holt et al., 2014). Here, the experimenter slowly approaches the participant until he/she starts to feel uncomfortable and indicates not to come closer anymore. The remaining distance indexes PS size. One method to simulate PS intrusion during neuroimaging experiments is the presentation of stimuli that are gradually enlarged. Holt et al. (2014) showed images of faces that were expanded to evoke the impression that the displayed person was coming closer. The preferred distance to a man relative to a woman in the stop-distance task was positively correlated with parietal activation during simulated intrusion. Surprisingly, gender differences (approaching men vs. women) for the simulation had not been tested directly. This was done in a functional magnetic resonance imaging (fMRI) study by Schienle et al. (2016) with exclusively male participants. Here, amygdala recruitment was only seen when the approaching person was male. To the best of our knowledge it has not been investigated whether a similar gender bias to simulated space intrusion exists in women. Therefore, in the present fMRI investigation PS intrusion by men and women was simulated. Pictures of neutral facial expressions were enlarged (zoomed-in) to make the person appear coming closer (almost touching). Half of the presented posers were women,
Abstract—Responses to personal space (PS) violations are variable and depend (besides many other factors) on the sex of the person who enters this space. The neuronal basis of this effect is still largely unknown. A previous neuroimaging investigation had shown that male participants responded with increased amygdala activation to PS violation, but only when the intruder was male. Gender-specific responses by females have not been studied yet. In the present study we recorded affective as well as hemodynamic responses of 30 women (mean age: M = 27.3 years; SD = 8.1). The participants were exposed to images of neutral facial expressions from men and women. All stimuli were once shown as photos (static), and once were zoomed in (picture enlargement by the factor 2.75) in order to simulate PS intrusion. In both conditions (‘static’ and ‘approaching’ faces) the eyes and mouth region of the depicted persons were always completely visible. Approaching faces generally provoked activation of a parietal network (e.g., intraparietal sulcus, superior/inferior parietal cortex). When the approaching person was male additional amygdala activation was detected. Because the amygdala is a central structure for the initiation of defense responses, the heightened activation might reflect that male intrusion was decoded as potential threat. Hence, we observed a similar gender bias to simulated space intrusion in women as previously in men. Ó 2016 IBRO. Published by Elsevier Ltd. All rights reserved.
Key words: personal space, fMRI, amygdala, parietal regions. 8
9
INTRODUCTION
10
The region immediately surrounding our bodies constitutes the (peri)personal space (PS; Holmes and Spence, 2004; Graziano and Cooke, 2006). It is a safety zone, and whenever a stimulus approaches or enters it, defensive reactions are primed. Neuroimaging investigations have shown that PS intrusion by another person leads to amygdala activation (e.g., Schienle et al., 2015). Moreover, a patient with a complete bilateral
11 12 13 14 15 16 17
*Corresponding author. Address: University of Graz, Universita¨tsplatz 2/III, A-8010 Graz, Austria. E-mail address: [email protected] (A. Schienle). Abbreviations: fMRI, functional magnetic resonance imaging; GM, gray matter; IPS, intraparietal sulcus; PPD, Preferred Personal Distance; PS, personal space; ROI, region of interest; WM, white matter. http://dx.doi.org/10.1016/j.neuroscience.2016.05.023 0306-4522/Ó 2016 IBRO. Published by Elsevier Ltd. All rights reserved. 1
18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 66
NSC 17109
No. of Pages 5
31 May 2016
2 67 68 69 70 71 72 73 74 75 76 77 78 79
A. Wabnegger et al. / Neuroscience xxx (2016) xxx–xxx
the other half men. The reactions to the ‘approaching’ faces were contrasted with a control condition using the same pictures, but without animation (static). Furthermore the hemodynamic responses of the participants were correlated with their preferred distance to a female and a male as indexed by a drawn PS bubble. We hypothesized that the female participants would respond with increased activation in PS-relevant brain areas (e.g., parietal cortex) toward simulated PS intrusion relatively to static pictures. The activation should be positively correlated with the preferred distance to a person. Moreover, we expected increased amygdala responses to simulated male intrusion.
EXPERIMENTAL PROCEDURES
80 81
Sample
82
91
We investigated 30 healthy women with a mean age of 27.3 years (standard deviation = 8.1); the majority were university students (70%), the rest were white-collar employees. The participants did not suffer from mental or somatic disorders and did not take medication as insured by a standardized clinical interview (Margraf, 1994). All participants provided written informed consent after receiving full explanation of the test procedure. The study had been approved by the ethics committee of the University of Graz.
92
Procedure and materials
93
During the fMRI session, the participants passively viewed pictures of facial expressions. They were instructed to lie still in the scanner and to pay attention to the presented images. We administered 32 pictures from the Karolinska Directed Emotional Faces (Lundqvist et al., 1998) that showed neutral facial expressions. Half of the posers were men, the other half women. Each picture was presented for 3000 ms once ‘static’ and once ‘approaching’ in an event-related design. In the latter condition the original picture was enlarged (factor: 2.75) up to point that only the region involving the mouth and the eyes could be seen. This gave the impression that the approaching person almost touched oneself. During the inter-stimulus interval, which was jittered between 2500 and 3000 ms, a fixation cross was presented. All images were shown twice in randomized order. The total experiment lasted approximately 6 min. Subsequent to the MRI experiment the participants rated valence and arousal (1 = calm, positive; 9 = aroused, negative) for a random selection of the presented images (half male, half female) outside of the scanner. They rated eight pictures of each condition. Finally, the participants were presented with a silhouette of a female person representing the participant (height: 50 mm; width: 13 mm). Participants were asked to draw a bubble around the silhouette (which represented herself) in order to indicate the distance she would like to maintain between herself and another man and another woman (strangers; e.g., sales woman/man). The bubble diameter (in mm) was considered the Preferred Personal Distance (PPD). A
83 84 85 86 87 88 89 90
94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123
pilot study with a two-week interval indicated retest reliabilities ranging between .79 and .84 for this measure.
124
fMRI acquisition and preprocessing
126
The fMRI session was conducted with a 3-T scanner (Skyra, Siemens, Erlangen, Germany) using a 32channel head-coil. Functional images were acquired using an echo-planar imaging protocol (number of slices: 35, descending, flip angle = 90°, slice thickness: 3 mm, distance factor: 33%, resulting in a covered volume in feet-head direction of 139 mm; TE = 30 ms; TR = 2290 ms; matrix: 64 64; FoV: 192 mm; in-plane resolution = 3.0 3.0 mm). Structural T1-weighted images were obtained using a 3D-MPRAGE sequence (number of slices: 176, ascending, TE = 2.07 ms; TR = 1560 ms; flip angle = 9°; slice thickness: 1 mm; FoV: 256 mm; distance factor: 50%). All analyses were conducted using SPM8 (Wellcome Department of Cognitive Neurology, London). Three volumes from the beginning of the time series were discarded to account for saturation effects. First functional data were motion corrected via realignment and acquisition timing was accounted in the slice timing step. Individual T1-weighted images were coregistered to their functional data. Afterward coregistered T1-weighted images got ‘segmented’ into gray matter (GM), white matter (WM) and cerebrospinal fluid. To create a study specific template and to increase inter subject alignment GM and WM images were used in a ‘Fast Diffeomorphic Registration Algorithm’ (DARTEL). Resulting images were further normalized to MNI-space (3 mm isotropic voxel), and smoothed with an 8-mm isotropic Gaussian kernel. In the first-level analysis the six movement parameters obtained during the realignment step were used as regressors of no interest.
127
Statistical analyses
159
In the first-level analysis t-contrasts of the interactions were built for each participant. We compiled vectors for each event of interest (e.g., Approaching_Neutral_Man, Static_Neutral_Female) and entered them into the design matrix to model event-related responses by the canonical hemodynamic response function in the firstlevel stage. Data were high-pass filtered (128 s). To account for serial correlations, which can result from unmodelled neuronal activity and biorhythms we applied an AR(1) process. In the second level, we computed an analysis of variance with GLM-Flex (http://mrtools.mgh.harvard.edu/ index.php/Main_Page) with the factors Motion (approaching, static) and Poser sex (male, female). Statistically significant main effects and interaction effects were followed up by one-dimensional t-contrasts. Further, PPD scores were correlated with region of interest (ROI) activation in a multiple regression analysis. The uncorrected cluster-building threshold for the analyses was set to p < 0.05, with at least 20 contiguous voxels. We conducted exploratory whole-brain voxel intensity tests as well as ROI
160
Please cite this article in press as: Wabnegger A et al. Differential amygdala activation during simulated personal space intrusion by men and women. Neuroscience (2016), http://dx.doi.org/10.1016/j.neuroscience.2016.05.023
125
128 129 130 131 132 133 134 135 136 137 138 139 140 141 142 143 144 145 146 147 148 149 150 151 152 153 154 155 156 157 158
161 162 163 164 165 166 167 168 169 170 171 172 173 174 175 176 177 178 179 180 181
NSC 17109
No. of Pages 5
31 May 2016
A. Wabnegger et al. / Neuroscience xxx (2016) xxx–xxx 182 183 184 185 186 187 188 189 190 191 192 193 194 195 196 197 198 199 200
analyses for the amygdala, the putamen, and parietal regions (intraparietal sulcus (IPS), inferior/superior parietal region, primary/secondary somatosensory cortex (SI, SII)). These regions had been selected based on previous findings on PS processing (e.g., Graziano and Cooke, 2006; Kennedy et al., 2009; Schaefer et al., 2012; Schienle et al., 2015;). The used ROI masks were taken from the Anatomy Toolbox (Eickhoff et al., 2005). Results were considered significant when p corrected for family-wise error (FWE) was <0.05 (small volume correction) on the voxel level. The ratings for the pictures were analyzed with IBM SPSS Statistics for Windows, version 22. For the affective ratings of the facial expressions (arousal, valence) we conducted analyses of variance for repeated measures with the within-subject factors Motion (approaching, static), and Poser Sex (male, female). The PPD to a man and to a woman was compared via t-test.
RESULTS
201 202
Self-report data
203
The PPD scores (means, standard deviations) were higher for a man (41.48 mm, 16.45) than for a woman (35.25 mm, 14.00; (t(29) = 4.16, p < .001). For the valence ratings we observed significant main effect for Poser Sex (F(1,29) = 15.77, p 6 .001, partial eta squared (g2p) = .35). Female faces were judged as more positive than male faces. Neither the main effect Motion nor the interaction Motion Poser Sex reached statistical significance (p’s > .05). The analysis of variance for the arousal ratings revealed a marginally significant main effect for Motion (F(1,29) = 3.31, p = .079, g2p = .10) indicating that approaching faces were judged as more arousing than static ones (see Table 1).
204 205 206 207 208 209 210 211 212 213 214 215 216
217
fMRI data
218
The conducted analysis of variance revealed a significant effect for Motion. Approaching stimuli in contrast to static stimuli recruited bilateral inferior and superior parietal cortices, intraparietal sulci, and the left SI. Male poser elicited stronger activation in the left IPS (main effect Poser Sex). Additionally, the interaction Motion Poser
219 220 221 222 223
Table 1. Mean affective picture ratings (and standard deviations) Poser sex Motion Arousal Static Approaching
Valence Static Approaching
Female
Male
1.58 (0.97) 1.93 (1.29)
1.71 (0.97) 1.98 (0.96)
1.76 (1.13)
1.85 (0.97)
3.36 (1.30) 3.45 (1.36)
4.05 (1.33) 4.05 (0.24)
3.41 (1.33)
4.05 (0.79)
1.65 (0.97) 1.96 (1.13)
3.71 (1.32) 3.75 (0.80)
3
Sex was significant. We observed enhanced recruitment of the right amygdala when approaching male faces were presented in contrast to approaching female faces (Table 2, Fig. 1). Additionally, the whole-brain analysis detected significant approach-related activation in occipital areas (main effect Motion; see: https://view. publitas.com/p222-8747/supplementary_1). The correlational analysis with the PPD scores revealed no significant results for the interaction contrast.
224
DISCUSSION
233
In the present study we were able to show that approaching male faces provoked stronger recruitment of the amygdala than approaching female faces. We identified a similar gender bias of the amygdala to simulated male intrusion in our female sample as we did before for male participants (Schienle et al., 2016). The amygdala is responsible for detecting and responding to threats in the environment (LeDoux, 2014). Men are obviously more (potentially) threatening, which seems logical from an evolutionary perspective as men are physically more aggressive than women (Archer, 2004). Moreover, ethological models of PS suggest that this imaginary zone has evolved throughout evolutionary history to reduce intra-species as well as inter-species aggression. PS is an ordering principle that helps prevent conflict within and between groups. Thus, PS can be understood as a phylogenetically acquired trait which is rooted in the brain. PS processing of the amygdala seemed to be an automatic process, which was not directly mirrored by the self-report of the participants. The rating data did not show a significant interaction Motion Poser Sex, neither for valence nor for arousal ratings. This dissociation of neuronal and subjective responses has also been described before, even in samples with clear deviations of the brain’s PS processing, such as in patients with borderline personality disorder and in violent offenders (Schienle et al., 2015, 2016). Both groups were characterized by greater limbic activation to simulated PS intrusion which was not reflected by the affective ratings. In contrast, the drawn PS bubble clearly indicated differences in preferred interpersonal distance to men and women. As in previous research, the female participants of the present study indicated a need for greater distance to men (e.g., Holt et al., 2014). Research on PS revealed that conceptions about acceptable social distance and proximity are strongly influenced by learning experiences, which explains the pronounced cultural differences. The bubble measure might rather reflect this learned aspect of PS. In line, a study by Uzzell and Horne (2006) showed that the learned gender role accounted for more variance in PS than biological sex. Replicating previous findings, we were able to demonstrate that simulated intrusion into one’s own PS mainly recruited parietal areas. In more detail, the activated regions included the inferior and the superior parietal lobule, the IPS and the primary somatosensory cortex (SI). The SI is the main receptive area for the sense of touch (Schaefer et al., 2012). The superior
234
Please cite this article in press as: Wabnegger A et al. Differential amygdala activation during simulated personal space intrusion by men and women. Neuroscience (2016), http://dx.doi.org/10.1016/j.neuroscience.2016.05.023
225 226 227 228 229 230 231 232
235 236 237 238 239 240 241 242 243 244 245 246 247 248 249 250 251 252 253 254 255 256 257 258 259 260 261 262 263 264 265 266 267 268 269 270 271 272 273 274 275 276 277 278 279 280 281 282
NSC 17109
No. of Pages 5
31 May 2016
4
A. Wabnegger et al. / Neuroscience xxx (2016) xxx–xxx
Table 2. Results of the analysis of variance for regions of interests H
x
y
z
F
Post-hoc t-tests
p(FWE)
Cluster size
Main Effect Motion Approach > Static Inferior parietal Inferior parietal Intraparietal Intraparietal SI Superior parietal Superior parietal
L R L R L L R
48 51 30 27 33 27 27
72 69 51 54 42 51 51
15 15 51 54 51 54 54
24.05 32.66 33.03 29.54 17.44 46.22 33.61
4.90 5.72 5.75 5.44 4.18 6.80 5.80
0.007 0.001 <0.001 0.001 0.022 <0.001 0.001
47 45 190 85 262 569 463
Main Effect Poser Male > Female 15.71
3.96
0.021
126
Interaction Motion Poser Sex (Approach Male > Static Male) > (Approach Female > Static Female) Amygdala R 30 0 24 15.62
Intraparietal
L
48
42
36
3.95
0.007
42
H: hemisphere, x, y, z: MNI coordinates, F-values of analyses of variance, post hoc t-contrast with p (corrected for family-wise error (FWE)); cluster size: number of voxels in associated cluster; SI: primary somatosensory cortex.
Fig. 1. Heightened amygdalar activity during the viewing of approaching male faces in contrast to approaching female faces.
283 284 285 286 287 288 289 290 291 292 293 294 295 296 297 298
parietal lobule receives input from the SI and is responsible for the integration of the sensation of touch together with the inferior parietal lobule (Clark et al., 2010). In line, the IPS contains neurons firing to tactile stimulation (Guipponi et al., 2013). The mentioned regions not only react to actual touch but also to observed touch. A recruitment of these areas has been identified when participants watched stimuli on a computer screen that entered peripersonal space (e.g., Cardini et al., 2010; Ebisch et al., 2011; Scha¨fer et al., 2011; Schienle et al., 2015). In the present fMRI investigation, the animation of the pictures (zooming-in procedure) evoked the impression that an approaching face was almost touching the participant‘s face. This imagined physical contact was able to recruit the mentioned parietal regions that are all involved in PS processing.
Additionally, we observed that the presentation of male faces provoked a heightened cerebral blood flow in the IPS relative to female faces. It has been argued that the IPS is active when salient, and especially threat-relevant stimuli are presented (Clark et al., 2010). Thus, this finding suggests that the exposure to male faces depicted a more salient stimulus relative to female faces. We have to mention the following short-comings of our study. As we only investigated faces with neutral expressions, the generalizability of the results to specific emotions still needs to be elucidated. It is possible that gender-specific aspects further amplify amygdala responses to simulated PS intrusion, for example in the context of facial expressions of anger.
299
CONCLUSION
314
This is the first fMRI study showing that female participants respond with heightened amygdala activation to simulated PS intrusion by men.
315
CONTRIBUTORS
318
Albert Wabnegger: analyzed the data; wrote the paper. Verena Leutgeb: performed the experiments; analyzed the data. Anne Schienle: wrote the paper; analyzed the data.
319
REFERENCES
323
Archer J (2004) Sex differences in aggression in real-world settings: a meta-analytic review. Rev Gen Psychol 8(4):291–322. Brozzoli C, Gentile G, Ehrsson HH (2012) That’s near my hand! Parietal and premotor coding of hand-centered space contributes to localization and self-attribution of the hand. J Neurosci 32:14573–14582. Cardini F, Costantini M, Galati G, Romani GL, La`davas E, Serino A (2010) Viewing one’s own face being touched modulates tactile perception: an fMRI study. J Cogn Neurosci 23:503–513.
324 325 326 327 328 329 330 331 332
Please cite this article in press as: Wabnegger A et al. Differential amygdala activation during simulated personal space intrusion by men and women. Neuroscience (2016), http://dx.doi.org/10.1016/j.neuroscience.2016.05.023
300 301 302 303 304 305 306 307 308 309 310 311 312 313
316 317
320 321 322
NSC 17109
No. of Pages 5
31 May 2016
A. Wabnegger et al. / Neuroscience xxx (2016) xxx–xxx 333 334 335 336 337 338 339 340 341 342 343 344 345 346 347 348 349 350 351 352 353 354 355 356 357 358 385 386 387
Clark DL, Boutros NN, Mendez MF (2010) The brain and behavior: an introduction to behavioral neuroanatomy. 3rd ed. New York: Cambridge University Press. Ebisch SJ, Ferri F, Salone A, Perrucci MG, D’Amico L, et al. (2011) Differential involvement of somatosensory and interoceptive cortices during the observation of affective touch. J Cogn Neurosci 23:1808–1822. Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25:1325–1335. Graziano MS, Cooke DF (2006) Parieto-frontal interactions, personal space, and defensive behavior. Neuropsychologia 44:845–859. Guipponi O, Wardak C, Ibarrola D, Comte J-C, Sappey-Marinier D, Pinede S, Ben Hamed S (2013) Multimodal convergence within the intraparietal sulcus of the macaque monkey. J Neurosci 33 (9):4128–4139. Holmes NP, Spence C (2004) The body schema and the multisensory representation(s): of peripersonal space. Cogn Process 5:94–105. Holt DJ, Cassidy BS, Yue X, Rauch SL, Boeke EA, Nasr S, Tootell RBH, Coombs G (2014) Neural correlates of personal space intrusion. J Neurosci 34(12):4123–4134. Kennedy DP, Gla¨scher J, Tyszka JM, Adolphs R (2009) Personal space regulation by the human amygdala. Nat Neurosci 12:1226–1227.
5
LeDoux JE (2014) Coming to terms with fear. Proc Natl Acad Sci U S A 111:2871–2878. Lundqvist D, Flykt A, O¨hman A (1998) The Karolinska Directed Emotional Faces – KDEF. CD ROM Department of Clinical Neuroscience, Psychology Section, Karolinska Institute. Margraf J (1994) Mini-DIPS: Diagnostisches Kurz-Interview bei psychischen Sto¨rungen; mit 15 Tabellen. Berlin [u.a.]: Springer. Miller HC, Chabriac AS, Molet M (2013) The impact of facial emotional expressions and sex on interpersonal distancing as evaluated in a computerized stop-distance task. Can J Exp Psychol 67:188–194. Schaefer M, Heinze H-J, Rotte M (2012) Close to you: embodied simulation for peripersonal space in primary somatosensory cortex. PLoS One 7:e42308. http://dx.doi.org/10.1371/journal. pone.0042308. Schienle A, Wabnegger A, Scho¨ngassner F, Leutgeb V (2015) Effects of personal space intrusion in affective contexts: an fMRI investigation with women suffering from borderline personality disorder. Soc Cogn Affect Neurosci 10(10):1424–1428. Schienle A, Wabnegger A, Leitner M, Leutgeb V (2016) Neuronal correlates of personal space intrusion in violent offenders. Brain Imag Behav. http://dx.doi.org/10.1007/s11682-016-9526-5. Published online 02 March 2016. Uzzell D, Horne N (2006) The influence of biological sex, sexuality and gender role on interpersonal distance. Br J Soc Psychol 45:579–597.
(Accepted 11 May 2016) (Available online xxxx)
Please cite this article in press as: Wabnegger A et al. Differential amygdala activation during simulated personal space intrusion by men and women. Neuroscience (2016), http://dx.doi.org/10.1016/j.neuroscience.2016.05.023
359 360 361 362 363 364 365 366 367 368 369 370 371 372 373 374 375 376 377 378 379 380 381 382 383 384
No. of Pages 5
31 May 2016 Please cite this article in press as: Wabnegger A et al. Differential amygdala activation during simulated personal space intrusion by men and women. Neuroscience (2016), http://dx.doi.org/10.1016/j.neuroscience.2016.05.023 1
Neuroscience xxx (2016) xxx–xxx
3
DIFFERENTIAL AMYGDALA ACTIVATION DURING SIMULATED PERSONAL SPACE INTRUSION BY MEN AND WOMEN
4 5
ALBERT WABNEGGER, VERENA LEUTGEB AND ANNE SCHIENLE *
6
Clinical Psychology, University of Graz, BioTechMedGraz, Austria
2
7
amygdala lesion lacked any sense of PS (Kennedy et al., 2009). The amygdala is a central structure for the initiation of defense responses (LeDoux, 2014) and by that mediates self-protection. In addition, PS processing is associated with activation of visuo-tactile neurons in the parietal cortex, the putamen and the premotor cortex as demonstrated by a convergent series of studies in animals and humans (Graziano and Cooke, 2006; Brozzoli et al., 2012). These studies showed that spatial proximity recruits brain areas which are sensitive to touch. Not only actual touch, but also the observation of another person being touched, or another person coming closer, recruits touch-sensitive neurons (e.g., Schaefer et al., 2012; Schienle et al., 2015, 2016). Interestingly, PS is a dynamic perception which is influenced by different moderating variables such as the sex of the approaching person. When participants are asked to draw a PS bubble around a silhouette representing their own person it is a consistent finding that women prefer greater interpersonal distance to the opposite sex compared to men (e.g., Schienle et al., 2015). This effect can also be shown when a behavioral technique, the stop-distance task, is used (e.g., Miller et al., 2013; Holt et al., 2014). Here, the experimenter slowly approaches the participant until he/she starts to feel uncomfortable and indicates not to come closer anymore. The remaining distance indexes PS size. One method to simulate PS intrusion during neuroimaging experiments is the presentation of stimuli that are gradually enlarged. Holt et al. (2014) showed images of faces that were expanded to evoke the impression that the displayed person was coming closer. The preferred distance to a man relative to a woman in the stop-distance task was positively correlated with parietal activation during simulated intrusion. Surprisingly, gender differences (approaching men vs. women) for the simulation had not been tested directly. This was done in a functional magnetic resonance imaging (fMRI) study by Schienle et al. (2016) with exclusively male participants. Here, amygdala recruitment was only seen when the approaching person was male. To the best of our knowledge it has not been investigated whether a similar gender bias to simulated space intrusion exists in women. Therefore, in the present fMRI investigation PS intrusion by men and women was simulated. Pictures of neutral facial expressions were enlarged (zoomed-in) to make the person appear coming closer (almost touching). Half of the presented posers were women,
Abstract—Responses to personal space (PS) violations are variable and depend (besides many other factors) on the sex of the person who enters this space. The neuronal basis of this effect is still largely unknown. A previous neuroimaging investigation had shown that male participants responded with increased amygdala activation to PS violation, but only when the intruder was male. Gender-specific responses by females have not been studied yet. In the present study we recorded affective as well as hemodynamic responses of 30 women (mean age: M = 27.3 years; SD = 8.1). The participants were exposed to images of neutral facial expressions from men and women. All stimuli were once shown as photos (static), and once were zoomed in (picture enlargement by the factor 2.75) in order to simulate PS intrusion. In both conditions (‘static’ and ‘approaching’ faces) the eyes and mouth region of the depicted persons were always completely visible. Approaching faces generally provoked activation of a parietal network (e.g., intraparietal sulcus, superior/inferior parietal cortex). When the approaching person was male additional amygdala activation was detected. Because the amygdala is a central structure for the initiation of defense responses, the heightened activation might reflect that male intrusion was decoded as potential threat. Hence, we observed a similar gender bias to simulated space intrusion in women as previously in men. Ó 2016 IBRO. Published by Elsevier Ltd. All rights reserved.
Key words: personal space, fMRI, amygdala, parietal regions. 8
9
INTRODUCTION
10
The region immediately surrounding our bodies constitutes the (peri)personal space (PS; Holmes and Spence, 2004; Graziano and Cooke, 2006). It is a safety zone, and whenever a stimulus approaches or enters it, defensive reactions are primed. Neuroimaging investigations have shown that PS intrusion by another person leads to amygdala activation (e.g., Schienle et al., 2015). Moreover, a patient with a complete bilateral
11 12 13 14 15 16 17
*Corresponding author. Address: University of Graz, Universita¨tsplatz 2/III, A-8010 Graz, Austria. E-mail address: [email protected] (A. Schienle). Abbreviations: fMRI, functional magnetic resonance imaging; GM, gray matter; IPS, intraparietal sulcus; PPD, Preferred Personal Distance; PS, personal space; ROI, region of interest; WM, white matter. http://dx.doi.org/10.1016/j.neuroscience.2016.05.023 0306-4522/Ó 2016 IBRO. Published by Elsevier Ltd. All rights reserved. 1
18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 66
NSC 17109
No. of Pages 5
31 May 2016
2 67 68 69 70 71 72 73 74 75 76 77 78 79
A. Wabnegger et al. / Neuroscience xxx (2016) xxx–xxx
the other half men. The reactions to the ‘approaching’ faces were contrasted with a control condition using the same pictures, but without animation (static). Furthermore the hemodynamic responses of the participants were correlated with their preferred distance to a female and a male as indexed by a drawn PS bubble. We hypothesized that the female participants would respond with increased activation in PS-relevant brain areas (e.g., parietal cortex) toward simulated PS intrusion relatively to static pictures. The activation should be positively correlated with the preferred distance to a person. Moreover, we expected increased amygdala responses to simulated male intrusion.
EXPERIMENTAL PROCEDURES
80 81
Sample
82
91
We investigated 30 healthy women with a mean age of 27.3 years (standard deviation = 8.1); the majority were university students (70%), the rest were white-collar employees. The participants did not suffer from mental or somatic disorders and did not take medication as insured by a standardized clinical interview (Margraf, 1994). All participants provided written informed consent after receiving full explanation of the test procedure. The study had been approved by the ethics committee of the University of Graz.
92
Procedure and materials
93
During the fMRI session, the participants passively viewed pictures of facial expressions. They were instructed to lie still in the scanner and to pay attention to the presented images. We administered 32 pictures from the Karolinska Directed Emotional Faces (Lundqvist et al., 1998) that showed neutral facial expressions. Half of the posers were men, the other half women. Each picture was presented for 3000 ms once ‘static’ and once ‘approaching’ in an event-related design. In the latter condition the original picture was enlarged (factor: 2.75) up to point that only the region involving the mouth and the eyes could be seen. This gave the impression that the approaching person almost touched oneself. During the inter-stimulus interval, which was jittered between 2500 and 3000 ms, a fixation cross was presented. All images were shown twice in randomized order. The total experiment lasted approximately 6 min. Subsequent to the MRI experiment the participants rated valence and arousal (1 = calm, positive; 9 = aroused, negative) for a random selection of the presented images (half male, half female) outside of the scanner. They rated eight pictures of each condition. Finally, the participants were presented with a silhouette of a female person representing the participant (height: 50 mm; width: 13 mm). Participants were asked to draw a bubble around the silhouette (which represented herself) in order to indicate the distance she would like to maintain between herself and another man and another woman (strangers; e.g., sales woman/man). The bubble diameter (in mm) was considered the Preferred Personal Distance (PPD). A
83 84 85 86 87 88 89 90
94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123
pilot study with a two-week interval indicated retest reliabilities ranging between .79 and .84 for this measure.
124
fMRI acquisition and preprocessing
126
The fMRI session was conducted with a 3-T scanner (Skyra, Siemens, Erlangen, Germany) using a 32channel head-coil. Functional images were acquired using an echo-planar imaging protocol (number of slices: 35, descending, flip angle = 90°, slice thickness: 3 mm, distance factor: 33%, resulting in a covered volume in feet-head direction of 139 mm; TE = 30 ms; TR = 2290 ms; matrix: 64 64; FoV: 192 mm; in-plane resolution = 3.0 3.0 mm). Structural T1-weighted images were obtained using a 3D-MPRAGE sequence (number of slices: 176, ascending, TE = 2.07 ms; TR = 1560 ms; flip angle = 9°; slice thickness: 1 mm; FoV: 256 mm; distance factor: 50%). All analyses were conducted using SPM8 (Wellcome Department of Cognitive Neurology, London). Three volumes from the beginning of the time series were discarded to account for saturation effects. First functional data were motion corrected via realignment and acquisition timing was accounted in the slice timing step. Individual T1-weighted images were coregistered to their functional data. Afterward coregistered T1-weighted images got ‘segmented’ into gray matter (GM), white matter (WM) and cerebrospinal fluid. To create a study specific template and to increase inter subject alignment GM and WM images were used in a ‘Fast Diffeomorphic Registration Algorithm’ (DARTEL). Resulting images were further normalized to MNI-space (3 mm isotropic voxel), and smoothed with an 8-mm isotropic Gaussian kernel. In the first-level analysis the six movement parameters obtained during the realignment step were used as regressors of no interest.
127
Statistical analyses
159
In the first-level analysis t-contrasts of the interactions were built for each participant. We compiled vectors for each event of interest (e.g., Approaching_Neutral_Man, Static_Neutral_Female) and entered them into the design matrix to model event-related responses by the canonical hemodynamic response function in the firstlevel stage. Data were high-pass filtered (128 s). To account for serial correlations, which can result from unmodelled neuronal activity and biorhythms we applied an AR(1) process. In the second level, we computed an analysis of variance with GLM-Flex (http://mrtools.mgh.harvard.edu/ index.php/Main_Page) with the factors Motion (approaching, static) and Poser sex (male, female). Statistically significant main effects and interaction effects were followed up by one-dimensional t-contrasts. Further, PPD scores were correlated with region of interest (ROI) activation in a multiple regression analysis. The uncorrected cluster-building threshold for the analyses was set to p < 0.05, with at least 20 contiguous voxels. We conducted exploratory whole-brain voxel intensity tests as well as ROI
160
Please cite this article in press as: Wabnegger A et al. Differential amygdala activation during simulated personal space intrusion by men and women. Neuroscience (2016), http://dx.doi.org/10.1016/j.neuroscience.2016.05.023
125
128 129 130 131 132 133 134 135 136 137 138 139 140 141 142 143 144 145 146 147 148 149 150 151 152 153 154 155 156 157 158
161 162 163 164 165 166 167 168 169 170 171 172 173 174 175 176 177 178 179 180 181
NSC 17109
No. of Pages 5
31 May 2016
A. Wabnegger et al. / Neuroscience xxx (2016) xxx–xxx 182 183 184 185 186 187 188 189 190 191 192 193 194 195 196 197 198 199 200
analyses for the amygdala, the putamen, and parietal regions (intraparietal sulcus (IPS), inferior/superior parietal region, primary/secondary somatosensory cortex (SI, SII)). These regions had been selected based on previous findings on PS processing (e.g., Graziano and Cooke, 2006; Kennedy et al., 2009; Schaefer et al., 2012; Schienle et al., 2015;). The used ROI masks were taken from the Anatomy Toolbox (Eickhoff et al., 2005). Results were considered significant when p corrected for family-wise error (FWE) was <0.05 (small volume correction) on the voxel level. The ratings for the pictures were analyzed with IBM SPSS Statistics for Windows, version 22. For the affective ratings of the facial expressions (arousal, valence) we conducted analyses of variance for repeated measures with the within-subject factors Motion (approaching, static), and Poser Sex (male, female). The PPD to a man and to a woman was compared via t-test.
RESULTS
201 202
Self-report data
203
The PPD scores (means, standard deviations) were higher for a man (41.48 mm, 16.45) than for a woman (35.25 mm, 14.00; (t(29) = 4.16, p < .001). For the valence ratings we observed significant main effect for Poser Sex (F(1,29) = 15.77, p 6 .001, partial eta squared (g2p) = .35). Female faces were judged as more positive than male faces. Neither the main effect Motion nor the interaction Motion Poser Sex reached statistical significance (p’s > .05). The analysis of variance for the arousal ratings revealed a marginally significant main effect for Motion (F(1,29) = 3.31, p = .079, g2p = .10) indicating that approaching faces were judged as more arousing than static ones (see Table 1).
204 205 206 207 208 209 210 211 212 213 214 215 216
217
fMRI data
218
The conducted analysis of variance revealed a significant effect for Motion. Approaching stimuli in contrast to static stimuli recruited bilateral inferior and superior parietal cortices, intraparietal sulci, and the left SI. Male poser elicited stronger activation in the left IPS (main effect Poser Sex). Additionally, the interaction Motion Poser
219 220 221 222 223
Table 1. Mean affective picture ratings (and standard deviations) Poser sex Motion Arousal Static Approaching
Valence Static Approaching
Female
Male
1.58 (0.97) 1.93 (1.29)
1.71 (0.97) 1.98 (0.96)
1.76 (1.13)
1.85 (0.97)
3.36 (1.30) 3.45 (1.36)
4.05 (1.33) 4.05 (0.24)
3.41 (1.33)
4.05 (0.79)
1.65 (0.97) 1.96 (1.13)
3.71 (1.32) 3.75 (0.80)
3
Sex was significant. We observed enhanced recruitment of the right amygdala when approaching male faces were presented in contrast to approaching female faces (Table 2, Fig. 1). Additionally, the whole-brain analysis detected significant approach-related activation in occipital areas (main effect Motion; see: https://view. publitas.com/p222-8747/supplementary_1). The correlational analysis with the PPD scores revealed no significant results for the interaction contrast.
224
DISCUSSION
233
In the present study we were able to show that approaching male faces provoked stronger recruitment of the amygdala than approaching female faces. We identified a similar gender bias of the amygdala to simulated male intrusion in our female sample as we did before for male participants (Schienle et al., 2016). The amygdala is responsible for detecting and responding to threats in the environment (LeDoux, 2014). Men are obviously more (potentially) threatening, which seems logical from an evolutionary perspective as men are physically more aggressive than women (Archer, 2004). Moreover, ethological models of PS suggest that this imaginary zone has evolved throughout evolutionary history to reduce intra-species as well as inter-species aggression. PS is an ordering principle that helps prevent conflict within and between groups. Thus, PS can be understood as a phylogenetically acquired trait which is rooted in the brain. PS processing of the amygdala seemed to be an automatic process, which was not directly mirrored by the self-report of the participants. The rating data did not show a significant interaction Motion Poser Sex, neither for valence nor for arousal ratings. This dissociation of neuronal and subjective responses has also been described before, even in samples with clear deviations of the brain’s PS processing, such as in patients with borderline personality disorder and in violent offenders (Schienle et al., 2015, 2016). Both groups were characterized by greater limbic activation to simulated PS intrusion which was not reflected by the affective ratings. In contrast, the drawn PS bubble clearly indicated differences in preferred interpersonal distance to men and women. As in previous research, the female participants of the present study indicated a need for greater distance to men (e.g., Holt et al., 2014). Research on PS revealed that conceptions about acceptable social distance and proximity are strongly influenced by learning experiences, which explains the pronounced cultural differences. The bubble measure might rather reflect this learned aspect of PS. In line, a study by Uzzell and Horne (2006) showed that the learned gender role accounted for more variance in PS than biological sex. Replicating previous findings, we were able to demonstrate that simulated intrusion into one’s own PS mainly recruited parietal areas. In more detail, the activated regions included the inferior and the superior parietal lobule, the IPS and the primary somatosensory cortex (SI). The SI is the main receptive area for the sense of touch (Schaefer et al., 2012). The superior
234
Please cite this article in press as: Wabnegger A et al. Differential amygdala activation during simulated personal space intrusion by men and women. Neuroscience (2016), http://dx.doi.org/10.1016/j.neuroscience.2016.05.023
225 226 227 228 229 230 231 232
235 236 237 238 239 240 241 242 243 244 245 246 247 248 249 250 251 252 253 254 255 256 257 258 259 260 261 262 263 264 265 266 267 268 269 270 271 272 273 274 275 276 277 278 279 280 281 282
NSC 17109
No. of Pages 5
31 May 2016
4
A. Wabnegger et al. / Neuroscience xxx (2016) xxx–xxx
Table 2. Results of the analysis of variance for regions of interests H
x
y
z
F
Post-hoc t-tests
p(FWE)
Cluster size
Main Effect Motion Approach > Static Inferior parietal Inferior parietal Intraparietal Intraparietal SI Superior parietal Superior parietal
L R L R L L R
48 51 30 27 33 27 27
72 69 51 54 42 51 51
15 15 51 54 51 54 54
24.05 32.66 33.03 29.54 17.44 46.22 33.61
4.90 5.72 5.75 5.44 4.18 6.80 5.80
0.007 0.001 <0.001 0.001 0.022 <0.001 0.001
47 45 190 85 262 569 463
Main Effect Poser Male > Female 15.71
3.96
0.021
126
Interaction Motion Poser Sex (Approach Male > Static Male) > (Approach Female > Static Female) Amygdala R 30 0 24 15.62
Intraparietal
L
48
42
36
3.95
0.007
42
H: hemisphere, x, y, z: MNI coordinates, F-values of analyses of variance, post hoc t-contrast with p (corrected for family-wise error (FWE)); cluster size: number of voxels in associated cluster; SI: primary somatosensory cortex.
Fig. 1. Heightened amygdalar activity during the viewing of approaching male faces in contrast to approaching female faces.
283 284 285 286 287 288 289 290 291 292 293 294 295 296 297 298
parietal lobule receives input from the SI and is responsible for the integration of the sensation of touch together with the inferior parietal lobule (Clark et al., 2010). In line, the IPS contains neurons firing to tactile stimulation (Guipponi et al., 2013). The mentioned regions not only react to actual touch but also to observed touch. A recruitment of these areas has been identified when participants watched stimuli on a computer screen that entered peripersonal space (e.g., Cardini et al., 2010; Ebisch et al., 2011; Scha¨fer et al., 2011; Schienle et al., 2015). In the present fMRI investigation, the animation of the pictures (zooming-in procedure) evoked the impression that an approaching face was almost touching the participant‘s face. This imagined physical contact was able to recruit the mentioned parietal regions that are all involved in PS processing.
Additionally, we observed that the presentation of male faces provoked a heightened cerebral blood flow in the IPS relative to female faces. It has been argued that the IPS is active when salient, and especially threat-relevant stimuli are presented (Clark et al., 2010). Thus, this finding suggests that the exposure to male faces depicted a more salient stimulus relative to female faces. We have to mention the following short-comings of our study. As we only investigated faces with neutral expressions, the generalizability of the results to specific emotions still needs to be elucidated. It is possible that gender-specific aspects further amplify amygdala responses to simulated PS intrusion, for example in the context of facial expressions of anger.
299
CONCLUSION
314
This is the first fMRI study showing that female participants respond with heightened amygdala activation to simulated PS intrusion by men.
315
CONTRIBUTORS
318
Albert Wabnegger: analyzed the data; wrote the paper. Verena Leutgeb: performed the experiments; analyzed the data. Anne Schienle: wrote the paper; analyzed the data.
319
REFERENCES
323
Archer J (2004) Sex differences in aggression in real-world settings: a meta-analytic review. Rev Gen Psychol 8(4):291–322. Brozzoli C, Gentile G, Ehrsson HH (2012) That’s near my hand! Parietal and premotor coding of hand-centered space contributes to localization and self-attribution of the hand. J Neurosci 32:14573–14582. Cardini F, Costantini M, Galati G, Romani GL, La`davas E, Serino A (2010) Viewing one’s own face being touched modulates tactile perception: an fMRI study. J Cogn Neurosci 23:503–513.
324 325 326 327 328 329 330 331 332
Please cite this article in press as: Wabnegger A et al. Differential amygdala activation during simulated personal space intrusion by men and women. Neuroscience (2016), http://dx.doi.org/10.1016/j.neuroscience.2016.05.023
300 301 302 303 304 305 306 307 308 309 310 311 312 313
316 317
320 321 322
NSC 17109
No. of Pages 5
31 May 2016
A. Wabnegger et al. / Neuroscience xxx (2016) xxx–xxx 333 334 335 336 337 338 339 340 341 342 343 344 345 346 347 348 349 350 351 352 353 354 355 356 357 358 385 386 387
Clark DL, Boutros NN, Mendez MF (2010) The brain and behavior: an introduction to behavioral neuroanatomy. 3rd ed. New York: Cambridge University Press. Ebisch SJ, Ferri F, Salone A, Perrucci MG, D’Amico L, et al. (2011) Differential involvement of somatosensory and interoceptive cortices during the observation of affective touch. J Cogn Neurosci 23:1808–1822. Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25:1325–1335. Graziano MS, Cooke DF (2006) Parieto-frontal interactions, personal space, and defensive behavior. Neuropsychologia 44:845–859. Guipponi O, Wardak C, Ibarrola D, Comte J-C, Sappey-Marinier D, Pinede S, Ben Hamed S (2013) Multimodal convergence within the intraparietal sulcus of the macaque monkey. J Neurosci 33 (9):4128–4139. Holmes NP, Spence C (2004) The body schema and the multisensory representation(s): of peripersonal space. Cogn Process 5:94–105. Holt DJ, Cassidy BS, Yue X, Rauch SL, Boeke EA, Nasr S, Tootell RBH, Coombs G (2014) Neural correlates of personal space intrusion. J Neurosci 34(12):4123–4134. Kennedy DP, Gla¨scher J, Tyszka JM, Adolphs R (2009) Personal space regulation by the human amygdala. Nat Neurosci 12:1226–1227.
5
LeDoux JE (2014) Coming to terms with fear. Proc Natl Acad Sci U S A 111:2871–2878. Lundqvist D, Flykt A, O¨hman A (1998) The Karolinska Directed Emotional Faces – KDEF. CD ROM Department of Clinical Neuroscience, Psychology Section, Karolinska Institute. Margraf J (1994) Mini-DIPS: Diagnostisches Kurz-Interview bei psychischen Sto¨rungen; mit 15 Tabellen. Berlin [u.a.]: Springer. Miller HC, Chabriac AS, Molet M (2013) The impact of facial emotional expressions and sex on interpersonal distancing as evaluated in a computerized stop-distance task. Can J Exp Psychol 67:188–194. Schaefer M, Heinze H-J, Rotte M (2012) Close to you: embodied simulation for peripersonal space in primary somatosensory cortex. PLoS One 7:e42308. http://dx.doi.org/10.1371/journal. pone.0042308. Schienle A, Wabnegger A, Scho¨ngassner F, Leutgeb V (2015) Effects of personal space intrusion in affective contexts: an fMRI investigation with women suffering from borderline personality disorder. Soc Cogn Affect Neurosci 10(10):1424–1428. Schienle A, Wabnegger A, Leitner M, Leutgeb V (2016) Neuronal correlates of personal space intrusion in violent offenders. Brain Imag Behav. http://dx.doi.org/10.1007/s11682-016-9526-5. Published online 02 March 2016. Uzzell D, Horne N (2006) The influence of biological sex, sexuality and gender role on interpersonal distance. Br J Soc Psychol 45:579–597.
(Accepted 11 May 2016) (Available online xxxx)
Please cite this article in press as: Wabnegger A et al. Differential amygdala activation during simulated personal space intrusion by men and women. Neuroscience (2016), http://dx.doi.org/10.1016/j.neuroscience.2016.05.023
359 360 361 362 363 364 365 366 367 368 369 370 371 372 373 374 375 376 377 378 379 380 381 382 383 384