Abstract
The steroid hormone testosterone (T) has been suggested to influence reactive aggression upon its action on the basolateral amygdala (BLA), a key brain region for threat detection. However, it is unclear whether T modulates resting-state functional connectivity (rsFC) of the BLA, and whether this predicts subsequent aggressive behavior. Aggressive interactions themselves, which often induce changes in T concentrations, could further alter BLA rsFC, but this too remains untested. Here we investigated the effect of endogenous T on rsFC of the BLA at baseline as well as after an aggressive encounter, and whether this was related to behavioral aggression in healthy young women (n = 39). Pre-scan T was negatively correlated with basal rsFC between BLA and left superior temporal gyrus (STG; p < .001, p < .05 Family-Wise Error [FWE] cluster-level corrected), which in turn was associated with increased aggression (r = .37, p = .020). BLA-STG coupling at rest might thus underlie hostile readiness in low-T women. In addition, connectivity between the BLA and the right superior parietal lobule (SPL), a brain region involved in higher-order perceptual processes, was reduced in aggressive participants (p < .001, p < .05 FWE cluster-level corrected). On the other hand, post-task increases in rsFC between BLA and medial orbitofrontal cortex (mOFC) were linked to reduced aggression (r = −.36, p = .023), consistent with the established notion that the mOFC regulates amygdala activity in order to curb aggressive impulses. Finally, competition-induced changes in T were associated with increased coupling between the BLA and the right lateral OFC (p < .001, p < .05 FWE cluster-level corrected), but this effect was unrelated to aggression. We thus identified connectivity patterns that prospectively predict aggression in women, and showed how aggressive interactions in turn impact these neural systems.
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Aghajani, M., Colins, O. F., Klapwijk, E. T., Veer, I. M., Andershed, H., Popma, A., van der Wee, N. J., & Vermeiren, R. R. J. M. (2016). Dissociable relations between amygdala subregional networks and psychopathy trait dimensions in conduct-disordered juvenile offenders. Human Brain Mapping, 37(11), 4017–4033. https://doi.org/10.1002/hbm.23292.
Aghajani, M., Veer, I. M., van Tol, M.-J., Aleman, A., van Buchem, M. A., Veltman, D. J., Rombouts, S. A. R. B., & van der Wee, N. J. (2014). Neuroticism and extraversion are associated with amygdala resting-state functional connectivity. Cognitive, Affective, & Behavioral Neuroscience, 14(2), 836–848. https://doi.org/10.3758/s13415-013-0224-0.
Anderson, C. A., & Bushman, B. J. (1997). External validity of "trivial" experiments: The case of laboratory aggression. Review of General Psychology, 1(1), 19–41.
Archer, J., Graham-Kevan, N., & Davies, M. (2005). Testosterone and aggression: A reanalysis of book, Starzyk, and Quinsey's (2001) study. Aggression and Violent Behavior, 10(2), 241–261. https://doi.org/10.1016/j.avb.2004.01.001.
Aubé, W., Angulo-Perkins, A., Peretz, I., Concha, L., & Armony, J. L. (2015). Fear across the senses: Brain responses to music, vocalizations and facial expressions. Social Cognitive and Affective Neuroscience, 10(3), 399–407. https://doi.org/10.1093/scan/nsu067.
Baczkowski, B. M., van Zutphen, L., Siep, N., Jacob, G. A., Domes, G., Maier, S., Sprenger, A., Senft, A., Willenborg, B., Tüscher, O., Arntz, A., & van de Ven, V. (2016). Deficient amygdala–prefrontal intrinsic connectivity after effortful emotion regulation in borderline personality disorder. European Archives of Psychiatry and Clinical Neuroscience, 267, 1–15. https://doi.org/10.1007/s00406-016-0760-z.
Banks, S. J., Eddy, K. T., Angstadt, M., Nathan, P. J., & Phan, K. L. (2007). Amygdala–frontal connectivity during emotion regulation. Social Cognitive and Affective Neuroscience, 2(4), 303–312. https://doi.org/10.1093/scan/nsm029.
Beyer, F., Münte, T. F., Göttlich, M., & Krämer, U. M. (2015). Orbitofrontal cortex reactivity to angry facial expression in a social interaction correlates with aggressive behavior. Cerebral Cortex, 25(9), 3057–3063. https://doi.org/10.1093/cercor/bhu101.
Bos, P. A., Hofman, D., Hermans, E. J., Montoya, E. R., Baron-Cohen, S., & van Honk, J. (2016). Testosterone reduces functional connectivity during the ‘reading the mind in the eyes’ test. Psychoneuroendocrinology, 68, 194–201. https://doi.org/10.1016/j.psyneuen.2016.03.006.
Bos, P. A., Panksepp, J., Bluthé, R.-M., & Honk, J. v. (2012). Acute effects of steroid hormones and neuropeptides on human social–emotional behavior: A review of single administration studies. Frontiers in Neuroendocrinology, 33(1), 17–35. https://doi.org/10.1016/j.yfrne.2011.01.002.
Buades-Rotger, M., Engelke, C., Beyer, F., Keevil, B. G., Brabant, G., & Krämer, U. M. (2016). Endogenous testosterone is associated with lower amygdala reactivity to angry faces and reduced aggressive behavior in healthy young women. Scientific Reports, 6, 38538. https://doi.org/10.1038/srep38538.
Buckner, R. L., Krienen, F. M., & Yeo, B. T. T. (2013). Opportunities and limitations of intrinsic functional connectivity MRI. Nature Neuroscience, 16(7), 832–837. https://doi.org/10.1038/nn.3423.
Bui, H. N., Sluss, P. M., Blincko, S., Knol, D. L., Blankenstein, M. A., & Heijboer, A. C. (2013). Dynamics of serum testosterone during the menstrual cycle evaluated by daily measurements with an ID-LC–MS/MS method and a 2nd generation automated immunoassay. Steroids, 78(1), 96–101. https://doi.org/10.1016/j.steroids.2012.10.010.
Burke, S. M., Manzouri, A. H., Dhejne, C., Bergstrom, K., Arver, S., Feusner, J. D., et al. (2017). Testosterone effects on the brain in transgender men. Cerebral Cortex, 28, 1–15. https://doi.org/10.1093/cercor/bhx054.
Carré, J. M., & Olmstead, N. A. (2015). Social neuroendocrinology of human aggression: Examining the role of competition-induced testosterone dynamics. Neuroscience, 286, 171–186. https://doi.org/10.1016/j.neuroscience.2014.11.029.
Castellanos, F. X., & Aoki, Y. (2016). Intrinsic functional connectivity in attention-deficit/hyperactivity disorder: A science in development. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 1(3), 253–261. https://doi.org/10.1016/j.bpsc.2016.03.004.
Casto, K. V., Rivell, A., & Edwards, D. A. (2017). Competition-related testosterone, cortisol, and perceived personal success in recreational women athletes. Hormones and Behavior, 92, 29–36. https://doi.org/10.1016/j.yhbeh.2017.05.006.
Chen, H. J., Wang, Y. F., Qi, R., Schoepf, U. J., Varga-Szemes, A., Ball, B. D., Zhang, Z., Kong, X., Wen, J., Li, X., Lu, G. M., & Zhang, L. J. (2017). Altered amygdala resting-state functional connectivity in maintenance hemodialysis end-stage renal disease patients with depressive mood. Molecular Neurobiology, 54(3), 2223–2233. https://doi.org/10.1007/s12035-016-9811-8.
Clemens, B., Wagels, L., Bauchmüller, M., Bergs, R., Habel, U., & Kohn, N. (2017). Alerted default mode: Functional connectivity changes in the aftermath of social stress. Scientific Reports, 7, 40180. https://doi.org/10.1038/srep40180.
Coccaro, E. F., McCloskey, M. S., Fitzgerald, D. A., & Phan, K. L. (2007). Amygdala and orbitofrontal reactivity to social threat in individuals with impulsive aggression. Biological Psychiatry, 62(2), 168–178. https://doi.org/10.1016/j.biopsych.2006.08.024.
Coccaro, E. F., Sripada, C. S., Yanowitch, R. N., & Phan, K. L. (2011). Corticolimbic function in impulsive aggressive behavior. Biological Psychiatry, 69(12), 1153–1159. https://doi.org/10.1016/j.biopsych.2011.02.032.
Cole, M. W., Bassett, D. S., Power, J. D., Braver, T. S., & Petersen, S. E. (2014). Intrinsic and task-evoked network architectures of the human brain. Neuron, 83(1), 238–251. https://doi.org/10.1016/j.neuron.2014.05.014.
Cole, M. W., Ito, T., Bassett, D. S., & Schultz, D. H. (2016). Activity flow over resting-state networks shapes cognitive task activations. Nature Neuroscience, 19(12), 1718–1726. https://doi.org/10.1038/nn.4406.
Davidson, R. J., Putnam, K. M., & Larson, C. L. (2000). Dysfunction in the neural circuitry of emotion regulation--a possible prelude to violence. Science, 289(5479), 591–594. https://doi.org/10.1126/science.289.5479.591.
de Gelder, B., Terburg, D., Morgan, B., Hortensius, R., Stein, D. J., & van Honk, J. (2014). The role of human basolateral amygdala in ambiguous social threat perception. Cortex, 52, 28–34, https://doi.org/10.1016/j.cortex.2013.12.010.
Denson, T. F., Ronay, R., von Hippel, W., & Schira, M. M. (2013). Endogenous testosterone and cortisol modulate neural responses during induced anger control. Social Neuroscience, 8(2), 165–177. https://doi.org/10.1080/17470919.2012.655425.
Deris, N., Montag, C., Reuter, M., Weber, B., & Markett, S. (2017). Functional connectivity in the resting brain as biological correlate of the affective neuroscience personality scales. NeuroImage, 147, 423–431. https://doi.org/10.1016/j.neuroimage.2016.11.063.
Eickhoff, S. B., Paus, T., Caspers, S., Grosbras, M.-H., Evans, A. C., Zilles, K., et al. (2007). Assignment of functional activations to probabilistic cytoarchitectonic areas revisited. NeuroImage, 36(3), 511–521, https://doi.org/10.1016/j.neuroimage.2007.03.060.
Eisenegger, C., Haushofer, J., & Fehr, E. (2011). The role of testosterone in social interaction. Trends in Cognitive Sciences, 15(6), 263–271, https://doi.org/10.1016/j.tics.2011.04.008.
Elson, M., Mohseni, M. R., Breuer, J., Scharkow, M., & Quandt, T. (2014). Press CRTT to measure aggressive behavior: The unstandardized use of the competitive reaction time task in aggression research. Psychological Assessment, 26(2), 419–432. https://doi.org/10.1037/a0035569.
Enter, D., Terburg, D., Harrewijn, A., Spinhoven, P., & Roelofs, K. (2016). Single dose testosterone administration alleviates gaze avoidance in women with Social Anxiety Disorder. Psychoneuroendocrinology, 63, 26–33, https://doi.org/10.1016/j.psyneuen.2015.09.008.
Fabiansson, E. C., Denson, T. F., Moulds, M. L., Grisham, J. R., & Schira, M. M. (2012). Don't look back in anger: Neural correlates of reappraisal, analytical rumination, and angry rumination during recall of an anger-inducing autobiographical memory. NeuroImage, 59(3), 2974–2981. https://doi.org/10.1016/j.neuroimage.2011.09.078.
Fanning, J. R., Keedy, S., Berman, M. E., Lee, R., & Coccaro, E. F. (2017). Neural correlates of aggressive behavior in real time: A review of fMRI studies of laboratory reactive aggression. Current Behavioral Neuroscience Reports, 4(2), 138–150. https://doi.org/10.1007/s40473-017-0115-8.
Fox, M. D., Snyder, A. Z., Vincent, J. L., & Raichle, M. E. (2007). Intrinsic Fluctuations within Cortical Systems Account for Intertrial Variability in Human Behavior. Neuron, 56(1), 171–184, https://doi.org/10.1016/j.neuron.2007.08.023.
Frühholz, S., Klaas, H. S., Patel, S., & Grandjean, D. (2015). Talking in fury: The Cortico-subcortical network underlying angry vocalizations. Cerebral Cortex, 25(9), 2752–2762. https://doi.org/10.1093/cercor/bhu074.
Fulwiler, C. E., King, J. A., & Zhang, N. (2012). Amygdala-orbitofrontal resting state functional connectivity is associated with trait anger. Neuroreport, 23(10), 606–610. https://doi.org/10.1097/WNR.0b013e3283551cfc.
Geissmann, L., Gschwind, L., Schicktanz, N., Deuring, G., Rosburg, T., Schwegler, K., Gerhards, C., Milnik, A., Pflueger, M. O., Mager, R., de Quervain, D. J. F., & Coynel, D. (2018). Resting-state functional connectivity remains unaffected by preceding exposure to aversive visual stimuli. NeuroImage, 167, 354–365. https://doi.org/10.1016/j.neuroimage.2017.11.046.
Giancola, P. R., & Parrott, D. J. (2008). Further evidence for the validity of the Taylor aggression paradigm. Aggressive Behavior, 34(2), 214–229. https://doi.org/10.1002/ab.20235.
Gilam, G., Maron-Katz, A., Kliper, E., Lin, T., Fruchter, E., Shamir, R., & Hendler, T. (2017). Tracing the neural carryover effects of interpersonal anger on resting-state fMRI in men and their relation to traumatic stress symptoms in a subsample of soldiers. Frontiers in Behavioral Neuroscience, 11(252). https://doi.org/10.3389/fnbeh.2017.00252.
Gospic, K., Mohlin, E., Fransson, P., Petrovic, P., Johannesson, M., & Ingvar, M. (2011). Limbic justice—Amygdala involvement in immediate rejection in the ultimatum game. PLoS Biology, 9(5), e1001054. https://doi.org/10.1371/journal.pbio.1001054.
Granger, D. A., Kivlighan, K. T., Fortunato, C., Harmon, A. G., Hibel, L. C., Schwartz, E. B., et al. (2007). Integration of salivary biomarkers into developmental and behaviorally-oriented research: Problems and solutions for collecting specimens. Physiology & Behavior, 92(4), 583-590, https://doi.org/10.1016/j.physbeh.2007.05.004.
Grèzes, J., Adenis, M.-S., Pouga, L., & Armony, J. L. (2013). Self-relevance modulates brain responses to angry body expressions. Cortex, 49(8), 2210–2220, https://doi.org/10.1016/j.cortex.2012.08.025.
Hahn, A., Kranz, G. S., Sladky, R., Kaufmann, U., Ganger, S., Hummer, A., Seiger, R., Spies, M., Vanicek, T., Winkler, D., Kasper, S., Windischberger, C., Swaab, D. F., & Lanzenberger, R. (2016b). Testosterone affects language areas of the adult human brain. Human Brain Mapping, 37(5), 1738–1748. https://doi.org/10.1002/hbm.23133.
Hahn, A. C., Fisher, C. I., Cobey, K. D., DeBruine, L. M., & Jones, B. C. (2016a). A longitudinal analysis of women’s salivary testosterone and intrasexual competitiveness. Psychoneuroendocrinology, 64, 117–122. https://doi.org/10.1016/j.psyneuen.2015.11.014.
Herpertz, S. C., Nagy, K., Ueltzhöffer, K., Schmitt, R., Mancke, F., Schmahl, C., & Bertsch, K. (2017). Brain mechanisms underlying reactive aggression in borderline personality disorder—Sex matters. Biological Psychiatry, 82, 257–266. https://doi.org/10.1016/j.biopsych.2017.02.1175.
Ho, N.-F., Chong, J. S. X., Koh, H. L., Koukouna, E., Lee, T.-S., Fung, D., Lim, C. G., & Zhou, J. (2015). Intrinsic affective network is impaired in children with attention-deficit/hyperactivity disorder. PLoS One, 10(9), e0139018. https://doi.org/10.1371/journal.pone.0139018.
Hoptman, M. J., D'Angelo, D., Catalano, D., Mauro, C. J., Shehzad, Z. E., Kelly, A. M. C., Castellanos, F. X., Javitt, D. C., & Milham, M. P. (2010). Amygdalofrontal functional Disconnectivity and aggression in schizophrenia. Schizophrenia Bulletin, 36(5), 1020–1028. https://doi.org/10.1093/schbul/sbp012.
Hull, J. V., Jacokes, Z. J., Torgerson, C. M., Irimia, A., & Van Horn, J. D. (2017). Resting-state functional connectivity in autism Spectrum disorders: A review. Frontiers in Psychiatry, 7, 205. https://doi.org/10.3389/fpsyt.2016.00205.
Kaufman, M. J., Janes, A. C., Hudson, J. I., Brennan, B. P., Kanayama, G., Kerrigan, A. R., Jensen, J. E., & Pope Jr., H. G. (2015). Brain and cognition abnormalities in long-term anabolic-androgenic steroid users. Drug and Alcohol Dependence, 152, 47–56. https://doi.org/10.1016/j.drugalcdep.2015.04.023.
Keevil, B., MacDonald, P., Macdowall, W., Lee, D., & Wu, F. (2013). Salivary testosterone measurement by liquid chromatography tandem mass spectrometry in adult males and females. Annals of Clinical Biochemistry: An international journal of biochemistry and laboratory medicine, 51(3), 368–378. https://doi.org/10.1177/0004563213506412.
Low, K. L., Ma, C., & Soma, K. K. (2017). Tyramide signal amplification permits Immunohistochemical analyses of androgen receptors in the rat prefrontal cortex. Journal of Histochemistry & Cytochemistry, 65(5), 295–308. https://doi.org/10.1369/0022155417694870.
Madsen, M. K., Mc Mahon, B., Andersen, S. B., Siebner, H. R., Knudsen, G. M., & Fisher, P. M. (2016). Threat-related amygdala functional connectivity is associated with 5-HTTLPR genotype and neuroticism. Social Cognitive and Affective Neuroscience, 11(1), 140–149. https://doi.org/10.1093/scan/nsv098.
Maron-Katz, A., Vaisvaser, S., Lin, T., Hendler, T., & Shamir, R. (2016). A large-scale perspective on stress-induced alterations in resting-state networks. Scientific Reports, 6, 21503. https://doi.org/10.1038/srep21503.
McCloskey, M. S., Phan, K. L., Angstadt, M., Fettich, K. C., Keedy, S., & Coccaro, E. F. (2016). Amygdala hyperactivation to angry faces in intermittent explosive disorder. Journal of Psychiatric Research, 79, 34–41, https://doi.org/10.1016/j.jpsychires.2016.04.006.
Mehta, P. H., & Beer, J. (2009). Neural mechanisms of the testosterone–aggression relation: The role of orbitofrontal cortex. Journal of Cognitive Neuroscience, 22(10), 2357–2368. https://doi.org/10.1162/jocn.2009.21389.
Mennes, M., Kelly, C., Colcombe, S., Castellanos, F. X., & Milham, M. P. (2013). The extrinsic and intrinsic functional architectures of the human brain are not equivalent. Cerebral Cortex, 23(1), 223–229. https://doi.org/10.1093/cercor/bhs010.
Mothes-Lasch, M., Miltner, W. H. R., & Straube, T. (2012). Processing of angry voices is modulated by visual load. NeuroImage, 63(1), 485–490, https://doi.org/10.1016/j.neuroimage.2012.07.005.
Motzkin, J. C., Newman, J. P., Kiehl, K. A., & Koenigs, M. (2011). Reduced prefrontal connectivity in psychopathy. The Journal of Neuroscience, 31(48), 17348–17357. https://doi.org/10.1523/jneurosci.4215-11.2011.
New, A. S., Hazlett, E. A., Buchsbaum, M. S., Goodman, M., Mitelman, S. A., Newmark, R., Trisdorfer, R., Haznedar, M. M., Koenigsberg, H. W., Flory, J., & Siever, L. J. (2007). Amygdala-prefrontal disconnection in borderline personality disorder. Neuropsychopharmacology, 32(7), 1629–1640.
Peters, S., Jolles, D. J., Duijvenvoorde, A. C. K. V., Crone, E. A., & Peper, J. S. (2015). The link between testosterone and amygdala–orbitofrontal cortex connectivity in adolescent alcohol use. Psychoneuroendocrinology, 53, 117–126, https://doi.org/10.1016/j.psyneuen.2015.01.004.
Peters, S., Peper, J. S., Van Duijvenvoorde, A. C. K., Braams, B. R., & Crone, E. A. (2016). Amygdala–orbitofrontal connectivity predicts alcohol use two years later: A longitudinal neuroimaging study on alcohol use in adolescence. Developmental Science, 20(4), 1–11, https://doi.org/10.1111/desc.12448.
Pope, J. H. G., Wood, R. I., Rogol, A., Nyberg, F., Bowers, L., & Bhasin, S. (2014). Adverse health consequences of performance-enhancing drugs: An Endocrine Society scientific statement. Endocrine Reviews, 35(3), 341–375. https://doi.org/10.1210/er.2013-1058.
Power, J. D., Barnes, K. A., Snyder, A. Z., Schlaggar, B. L., & Petersen, S. E. (2012). Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage, 59(3), 2142–2154. https://doi.org/10.1016/j.neuroimage.2011.10.018.
Prada, P., Hasler, R., Baud, P., Bednarz, G., Ardu, S., Krejci, I., et al. (2014). Distinguishing borderline personality disorder from adult attention deficit/hyperactivity disorder: A clinical and dimensional perspective. Psychiatry Research, 217(1), 107–114, https://doi.org/10.1016/j.psychres.2014.03.006.
Qin, S., Young, C. B., Duan, X., Chen, T., Supekar, K., & Menon, V. (2014). Amygdala Subregional Structure and Intrinsic Functional Connectivity Predicts Individual Differences in Anxiety During Early Childhood. Biological Psychiatry, 75(11), 892–900, https://doi.org/10.1016/j.biopsych.2013.10.006.
Rausch, J., Gäbel, A., Nagy, K., Kleindienst, N., Herpertz, S. C., & Bertsch, K. (2015). Increased testosterone levels and cortisol awakening responses in patients with borderline personality disorder: Gender and trait aggressiveness matter. Psychoneuroendocrinology, 55, 116–127, https://doi.org/10.1016/j.psyneuen.2015.02.002.
Ritter, D., & Eslea, M. (2005). Hot sauce, toy guns, and graffiti: A critical account of current laboratory aggression paradigms. Aggressive Behavior, 31(5), 407–419. https://doi.org/10.1002/ab.20066.
Roy, A. K., Shehzad, Z., Margulies, D. S., Kelly, A. M. C., Uddin, L. Q., Gotimer, K., et al. (2009). Functional connectivity of the human amygdala using resting state fMRI. NeuroImage, 45(2), 614–626, https://doi.org/10.1016/j.neuroimage.2008.11.030.
Sadaghiani, S., Poline, J.-B., Kleinschmidt, A., & D’Esposito, M. (2015). Ongoing dynamics in large-scale functional connectivity predict perception. Proceedings of the National Academy of Sciences of the United States of America, 112(27), 8463–8468. https://doi.org/10.1073/pnas.1420687112.
Savic, I., Frisen, L., Manzouri, A., Nordenstrom, A., & Hirschberg, A. L. (2017). Role of testosterone and Y chromosome genes for the masculinization of the human brain. Human Brain Mapping, 38, 1801–1814. https://doi.org/10.1002/hbm.23483.
Scheperjans, F., Eickhoff, S. B., Hömke, L., Mohlberg, H., Hermann, K., Amunts, K., et al. (2008). Probabilistic maps, morphometry, and variability of Cytoarchitectonic areas in the human superior parietal cortex. Cerebral Cortex, 18(9), 2141–2157. https://doi.org/10.1093/cercor/bhm241.
Sohn, W. S., Yoo, K., Lee, Y.-B., Seo, S. W., Na, D. L., & Jeong, Y. (2015). Influence of ROI selection on resting state functional connectivity: An individualized approach for resting state fMRI analysis. Frontiers in Neuroscience, 9, 280. https://doi.org/10.3389/fnins.2015.00280.
Spielberg, J. M., Forbes, E. E., Ladouceur, C. D., Worthman, C. M., Olino, T. M., Ryan, N. D., & Dahl, R. E. (2015). Pubertal testosterone influences threat-related amygdala–orbitofrontal cortex coupling. Social Cognitive and Affective Neuroscience, 10(3), 408–415. https://doi.org/10.1093/scan/nsu062.
Stanton, S. J., & Edelstein, R. S. (2009). The physiology of women’s power motive: Implicit power motivation is positively associated with estradiol levels in women. Journal of Research in Personality, 43(6), 1109–1113. https://doi.org/10.1016/j.jrp.2009.08.002.
Stanton, S. J., & Schultheiss, O. C. (2007). Basal and dynamic relationships between implicit power motivation and estradiol in women. Hormones and Behavior, 52(5), 571–580. https://doi.org/10.1016/j.yhbeh.2007.07.002.
Sussman, T. J., Weinberg, A., Szekely, A., Hajcak, G., & Mohanty, A. (2017). Here comes trouble: Prestimulus brain activity predicts enhanced perception of threat. Cerebral Cortex, 27(4), 2695–2707. https://doi.org/10.1093/cercor/bhw104.
Terburg, D., Syal, S., Rosenberger, L. A., Heany, S. J., Stein, D. J., & Honk, J. v. (2016). Testosterone abolishes implicit subordination in social anxiety. Psychoneuroendocrinology, 72, 205-211, https://doi.org/10.1016/j.psyneuen.2016.07.203.
Terburg, D., & van Honk, J. (2013). Approach–avoidance versus dominance–submissiveness: A multilevel neural framework on how testosterone promotes social status. Emotion Review, 5(3), 296–302. https://doi.org/10.1177/1754073913477510.
Toschi, N., Duggento, A., & Passamonti, L. (2017). Functional connectivity in Amygdalar-sensory/(pre)motor networks at rest: New evidence from the human connectome project. European Journal of Neuroscience, 45, 1224–1229. https://doi.org/10.1111/ejn.13544.
Tremblay, P. F., Graham, K., & Wells, S. (2008). Severity of physical aggression reported by university students: A test of the interaction between trait aggression and alcohol consumption. Personality and Individual Differences, 45(1), 3–9, https://doi.org/10.1016/j.paid.2008.02.008.
Van den Stock, J., Hortensius, R., Sinke, C., Goebel, R., & de Gelder, B. (2015). Personality traits predict brain activation and connectivity when witnessing a violent conflict. Scientific Reports, 5, 13779. https://doi.org/10.1038/srep13779.
van Wingen, G., Mattern, C., Verkes, R. J., Buitelaar, J., & Fernández, G. (2010). Testosterone reduces amygdala–orbitofrontal cortex coupling. Psychoneuroendocrinology, 35(1), 105–113. https://doi.org/10.1016/j.psyneuen.2009.09.007.
Vigil-Colet, A., Ruiz-Pamies, M., Anguiano-Carrasco, C., & Lorenzo-Seva, U. (2012). The impact of social desirability on psychometric measures of aggression. Psicothema, 24(2), 310–315.
Wahlund, K., & Kristiansson, M. (2009). Aggression, psychopathy and brain imaging — Review and future recommendations. International Journal of Law and Psychiatry, 32(4), 266–271, https://doi.org/10.1016/j.ijlp.2009.04.007.
Wang, J., Yang, Y., Fan, L., Xu, J., Li, C., Liu, Y., et al. (2015). Convergent functional architecture of the superior parietal lobule unraveled with multimodal neuroimaging approaches. Human Brain Mapping, 36(1), 238–257, https://doi.org/10.1002/hbm.22626.
Welker, K. M., Norman, R. E., Goetz, S., Moreau, B. J. P., Kitayama, S., & Carré, J. M. (2017). Preliminary evidence that testosterone's association with aggression depends on self-construal. Hormones and Behavior, 92, 117–127, https://doi.org/10.1016/j.yhbeh.2016.10.014.
Westlye, L. T., Kaufmann, T., Alnæs, D., Hullstein, I. R., & Bjørnebekk, A. (2017). Brain connectivity aberrations in anabolic-androgenic steroid users. NeuroImage: Clinical, 13, 62–69, https://doi.org/10.1016/j.nicl.2016.11.014.
White, S. F., VanTieghem, M., Brislin, S. J., Sypher, I., Sinclair, S., Pine, D. S., Hwang, S., & Blair, R. J. R. (2015). Neural correlates of the propensity for retaliatory behavior in youths with disruptive behavior disorders. American Journal of Psychiatry, 173(3), 282–290. https://doi.org/10.1176/appi.ajp.2015.15020250.
Whitfield-Gabrieli, S., & Nieto-Castanon, A. (2012). Conn: A functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connectivity, 2, 125–141. https://doi.org/10.1089/brain.2012.0073.
Yoder, K. J., Porges, E. C., & Decety, J. (2015). Amygdala subnuclei connectivity in response to violence reveals unique influences of individual differences in psychopathic traits in a nonforensic sample. Human Brain Mapping, 36(4), 1417–1428. https://doi.org/10.1002/hbm.22712.
Zhou, M., Hu, X., Lu, L., Zhang, L., Chen, L., Gong, Q., et al. (2017). Intrinsic cerebral activity at resting state in adults with major depressive disorder: A meta-analysis. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 75, 157-164, https://doi.org/10.1016/j.pnpbp.2017.02.001.
Zuo, X.-N., Di Martino, A., Kelly, C., Shehzad, Z. E., Gee, D. G., Klein, D. F., et al. (2010). The oscillating brain: Complex and reliable. NeuroImage, 49(2), 1432–1445. https://doi.org/10.1016/j.neuroimage.2009.09.037.
Acknowledgements
We are grateful to Matthias Liebrand, Alice Nöh, Christian Erdmann, and Susanne Schellbach for their help with the data acquisition. The authors report no conflicts of interest.
Funding
This study was funded by the German Science Foundation (grant number KR3691/5–1).
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All procedures performed in this study were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. The study had been approved by the ethics committee of the University of Lübeck.
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Buades-Rotger, M., Engelke, C. & Krämer, U.M. Trait and state patterns of basolateral amygdala connectivity at rest are related to endogenous testosterone and aggression in healthy young women. Brain Imaging and Behavior 13, 564–576 (2019). https://doi.org/10.1007/s11682-018-9884-2
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DOI: https://doi.org/10.1007/s11682-018-9884-2