Beking, T.; University of Groningen, Department Clinical & Developmental Neuropsychology, Grote Kruisstraat 2/1, Groningen, TS 9712, Netherlands
Burke, S. M.; Leiden University, Brain & Development Research Centre, Department of Developmental and Educational Psychology, Wassenaarseweg 52, Leiden, AK 2333, Netherlands
Geuze, R. H.; University of Groningen, Department Clinical & Developmental Neuropsychology, Grote Kruisstraat 2/1, Groningen, TS 9712, Netherlands
Staphorsius, A. S.; Amsterdam University Medical Centers, Location VU, Department of Internal Medicine, Center of Expertise on Gender Dysphoria, PO Box 7057, Amsterdam, MB 1007, Netherlands
Bakker, Julie ; Université de Liège - ULiège > Neurosciences-Neuroendocrinology
Groothuis, A. G. G.; University of Groningen, Groningen Institute for Evolutionary Life Sciences, Nijenborgh 7, Groningen, AG 9747, Netherlands
Kreukels, B. P. C.; Amsterdam University Medical Centers, Location VU, Department of Medical Psychology, Center of Expertise on Gender Dysphoria, PO Box 7057, Amsterdam, MB 1007, Netherlands
Language :
English
Title :
Testosterone effects on functional amygdala lateralization: A study in adolescent transgender boys and cisgender boys and girls
Publication date :
2020
Journal title :
Psychoneuroendocrinology
ISSN :
0306-4530
eISSN :
1873-3360
Publisher :
Elsevier Ltd
Volume :
111
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
NWO - Nederlandse Organisatie voor Wetenschappelijk Onderzoek
Ackermann, S., Spalek, K., Rasch, B., Gschwind, L., Coynel, D., Fastenrath, M., Papassotiropoulos, A., Quervain, D., 2012. Testosterone levels in healthy men are related to amygdala reactivity and memory performance. Psychoneuroendocrinology 37, 1417–1424. https://doi.org/10.1016/J.PSYNEUEN.2012.01.008
American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders (DSM-5), 5th ed.Arlington, VA: American Psychiatric Publishing; 2013.
Antyukhov, A.D., 2016. Morphometric Characteristics of the Structure of the Central Nucleus of the Amygdaloid Complex in Men and Women. Neurosci. Behav. Physiol. 46, 743–747. https://doi.org/10.1007/s11055-016-0304-z
Arnold, A.P., McCarthy, M.M., 2016. Sexual Differentiation of the Brain and Behavior: A Primer, in: Neuroscience in the 21st Century. Springer New York, New York, NY, pp. 2139–2168. https://doi.org/10.1007/978-1-4939-3474-4_141
Beking, T., Geuze, R.H., Groothuis, T.G.G., 2017. Investigating Effects of Steroid Hormones on Lateralization of Brain and Behavior, in: Rogers, L., Vallortigara, G. (Eds.), Lateralized Brain Functions - Methods in Human and Non-Human Species. Springer, pp. 633–666. https://doi.org/10.1007/978-1-4939-6725-4_20
Beking, T., Geuze, R.H., van Faassen, M., Kema, I.P., Kreukels, B.P.C., Groothuis, T.G.G., 2018. Prenatal and pubertal testosterone affect brain lateralization. Psychoneuroendocrinology 88, 78–91. https://doi.org/10.1016/j.psyneuen.2017.10.027
Bos, P.A., Panksepp, J., Bluthé, R.-M., van Honk, J., 2012. Acute effects of steroid hormones and neuropeptides on human social–emotional behavior: A review of single administration studies. Front. Neuroendocrinol. 33, 17–35. https://doi.org/10.1016/J.YFRNE.2011.01.002
Bos, P.A., van Honk, J., Ramsey, N.F., Stein, D.J., Hermans, E.J., 2013. Testosterone administration in women increases amygdala responses to fearful and happy faces. Psychoneuroendocrinology 38, 808–817. https://doi.org/10.1016/J.PSYNEUEN.2012.09.005
Bramen, J.E., Hranilovich, J.A., Dahl, R.E., Forbes, E.E., Chen, J., Toga, A.W., Dinov, I.D., Worthman, C.M., Sowell, E.R., 2011. Puberty Influences Medial Temporal Lobe and Cortical Gray Matter Maturation Differently in Boys Than Girls Matched for Sexual Maturity. Cereb. Cortex 21, 636–646. https://doi.org/10.1093/cercor/bhq137
Bryden, M.P., Mcmanus, I.C., Bulmanfleming, M.B., 1994. Evaluating the Empirical Support for the Geschwind-Behan-Galaburda Model of Cerebral Lateralization. Brain Cogn. 26, 103–167. https://doi.org/10.1006/BRCG.1994.1045
Bui, H.N., Schagen, S.E.E., Klink, D.T., Delemarre-van de Waal, H.A., Blankenstein, M.A., Heijboer, A.C., 2013. Salivary testosterone in female-to-male transgender adolescents during treatment with intra-muscular injectable testosterone esters. Steroids 78, 91–95. https://doi.org/10.1016/j.steroids.2012.10.006
Burke, S.M., Kreukels, B.P.C., Cohen-Kettenis, P.T., Veltman, D.J., Klink, D.T., Bakker, J., 2016. Male-typical visuospatial functioning in gynephilic girls with gender dysphoria - organizational and activational effects of testosterone. J. Psychiatry Neurosci. 41, 150147.
Cahill, L., Uncapher, M., Kilpatrick, L., Alkire, M.T., Turner, J., 2004. Sex-related hemispheric lateralization of amygdala function in emotionally influenced memory: An fMRI investigation. Learning & Memory 11, 261-266. doi: 10.1101/lm.70504
Canli, T., Desmond, J.E., Zhao, Z., Gabrieli, J.D.E., 2002. Sex differences in the neural basis of emotional memories. Proceedings of the National Academy of Sciences 99, 10789-10794. www.pnas.orgcgidoi10.1073pnas.162356599
Cohen-Kettenis, P.T., Goozen, S.H.M. van, Cees D. Doorn, C.D., Gooren, L.J.G. 1998. Cognitive ability and cerebral lateralization in transsexuals. Psychoneuroendocrinology 23, 631–641.
Derntl, B., Windischberger, C., Robinson, S., Kryspin-Exner, I., Gur, R.C., Moser, E., Habel, U., 2009. Amygdala activity to fear and anger in healthy young males is associated with testosterone. Psychoneuroendocrinology 34, 687–693. https://doi.org/10.1016/j.psyneuen.2008.11.007
Derntl, B., Windischberger, C., Robinson, S., Lamplmayr, E., Kryspin-Exner, I., Gur, R.C., Moser, E., Habel, U., 2008. Facial emotion recognition and amygdala activation are associated with menstrual cycle phase. Psychoneuroendocrinology 33, 1031–40. https://doi.org/10.1016/j.psyneuen.2008.04.014
Ernst, M., Maheu, F.S., Schroth, E., Hardin, J., Golan, L.G., Cameron, J., Allen, R., Holzer, S., Nelson, E., Pine, D.S., Merke, D.P., 2007. Amygdala function in adolescents with congenital adrenal hyperplasia: a model for the study of early steroid abnormalities. Neuropsychologia 45, 2104–13. https://doi.org/10.1016/j.neuropsychologia.2007.01.019
Fusar-Poli, P., Placentino, A., Carletti, F., Landi, P., Allen, P., Surguladze, S., Benedetti, F., Abbamonte, M., Gasparotti, R., Barale, F., Perez, J., McGuire, P., Politi, P., 2009. Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. J. Psychiatry Neurosci. 34, 418–32.
Geschwind, N., Galaburda, A.M., 1985. Cerebral lateralization: biological mechanisms, associations, and pathology. I. A hypothesis and program for research. Arch Neurol. 42, 428.
Goddings, A.-L., Mills, K.L., Clasen, L.S., Giedd, J.N., Viner, R.M., Blakemore, S.-J., 2014. The influence of puberty on subcortical brain development. Neuroimage 88, 242–251. https://doi.org/10.1016/j.neuroimage.2013.09.073
Guadalupe, T., Mathias, S.R., vanErp, T.G.M., Whelan, C.D., Zwiers, M.P., Abe, Y., Abramovic, L., Agartz, I., Andreassen, O.A., Arias-Vásquez, A., Aribisala, B.S., Armstrong, N.J., Arolt, V., Artiges, E., Ayesa-Arriola, R., Baboyan, V.G., Banaschewski, T., Barker, G., Bastin, M.E., Baune, B.T., Blangero, J., Bokde, A.L.W., Boedhoe, P.S.W., Bose, A., Brem, S., Brodaty, H., Bromberg, U., Brooks, S., Büchel, C., Buitelaar, J., Calhoun, V.D., Cannon, D.M., Cattrell, A., Cheng, Y., Conrod, P.J., Conzelmann, A., Corvin, A., Crespo-Facorro, B., Crivello, F., Dannlowski, U., de Zubicaray, G.I., de Zwarte, S.M.C., Deary, I.J., Desrivières, S., Doan, N.T., Donohoe, G., Dørum, E.S., Ehrlich, S., Espeseth, T., Fernández, G., Flor, H., Fouche, J.-P., Frouin, V., Fukunaga, M., Gallinat, J., Garavan, H., Gill, M., Suarez, A.G., Gowland, P., Grabe, H.J., Grotegerd, D., Gruber, O., Hagenaars, S., Hashimoto, R., Hauser, T.U., Heinz, A., Hibar, D.P., Hoekstra, P.J., Hoogman, M., Howells, F.M., Hu, H., Hulshoff Pol, H.E., Huyser, C., Ittermann, B., Jahanshad, N., Jönsson, E.G., Jurk, S., Kahn, R.S., Kelly, S., Kraemer, B., Kugel, H., Kwon, J.S., Lemaitre, H., Lesch, K.-P., Lochner, C., Luciano, M., Marquand, A.F., Martin, N.G., Martínez-Zalacaín, I., Martinot, J.-L., Mataix-Cols, D., Mather, K., McDonald, C., McMahon, K.L., Medland, S.E., Menchón, J.M., Morris, D.W., Mothersill, O., Maniega, S.M., Mwangi, B., Nakamae, T., Nakao, T., Narayanaswaamy, J.C., Nees, F., Nordvik, J.E., Onnink, A.M.H., Opel, N., Ophoff, R., Paillère Martinot, M.-L., Papadopoulos Orfanos, D., Pauli, P., Paus, T., Poustka, L., Reddy, J.Y., Renteria, M.E., Roiz-Santiáñez, R., Roos, A., Royle, N.A., Sachdev, P., Sánchez-Juan, P., Schmaal, L., Schumann, G., Shumskaya, E., Smolka, M.N., Soares, J.C., Soriano-Mas, C., Stein, D.J., Strike, L.T., Toro, R., Turner, J.A., Tzourio-Mazoyer, N., Uhlmann, A., Hernández, M.V., van den Heuvel, O.A., van der Meer, D., van Haren, N.E…, Veltman, D.J., Venkatasubramanian, G., Vetter, N.C., Vuletic, D., Walitza, S., Walter, H., Walton, E., Wang, Z., Wardlaw, J., Wen, W., Westlye, L.T., Whelan, R., Wittfeld, K., Wolfers, T., Wright, M.J., Xu, J., Xu, X., Yun, J.-Y., Zhao, J., Franke, B., Thompson, P.M., Glahn, D.C., Mazoyer, B., Fisher, S.E., Francks, C., 2016. Human subcortical brain asymmetries in 15,847 people worldwide reveal effects of age and sex. Brain Imaging Behav. 1–18. https://doi.org/10.1007/s11682-016-9629-z
Hariri, A.R., Bookheimer, S.Y., Mazziotta, J.C., 2000. Modulating emotional responses: effects of a neocortical network on the limbic system. Neuroreport 11, 43–48.
Hembree, W.C., Cohen-Kettenis, P., Delemarre-van de Waal, H.A., Gooren, L.J., Meyer III, W.J., Spack, N.P., Tangpricha, V., Montor, V.M., 2009. Endocrine treatment of transsexual persons: an endocrine society clinical practice guideline. Clin Endocrinol Metab. 94, 3132–3154.
Herman, A., Grabowska, A., Dulko, S., 1993. Transsexualism and sex-related differences in hemispheric asymmetry. Acta Neurobiol. Exp. (Wars). 53, 269–274.
Hermans, E.J., Ramsey, N.F., van Honk, J., 2008. Exogenous Testosterone Enhances Responsiveness to Social Threat in the Neural Circuitry of Social Aggression in Humans. Biol. Psychiatry 63, 263–270. https://doi.org/10.1016/j.biopsych.2007.05.013
Herting, M.M., Gautam, P., Spielberg, J.M., Kan, E., Dahl, R.E., Sowell, E.R., 2014. The role of testosterone and estradiol in brain volume changes across adolescence: A longitudinal structural MRI study. Hum. Brain Mapp. 35. https://doi.org/10.1002/hbm.22575
Hines, M. & Shipley, C., 1984. Prenatal exposure to Diethylstilbesterol (Des) and the development of sexually dimorphic cognitive abilities and cerebral lateralization. Developmental Psychology 20, 81-94.
Hirnstein, M., Hugdahl, K., Hausmann, M., 2018. Cognitive sex differences and hemispheric asymmetry: A critical review of 40 years of research. Laterality Asymmetries Body, Brain Cogn. 1–49. https://doi.org/10.1080/1357650X.2018.1497044
Killgore, W.D.S., Yurgelun-Todd, D.A., 2004. Sex-related developmental differences in the lateralized activation of the prefrontal cortex and amygdala during perception of facial affect. Percept. Mot. Skills 99, 371–91.
Lemieux L., Salek-Haddadi A, Lund TE, Laufs H, Carmichael D 2007. Modelling large motion events in fMRI studies of patients with epilepsy, Magnetic Resonance Imaging, 25, 894–901. 10.1016/j.mri.2007.03.009
Manuck, S.B., Marsland, A.L., Flory, J.D., Gorka, A., Ferrell, R.E., Hariri, A.R., 2010. Salivary testosterone and a trinucleotide (CAG) length polymorphism in the androgen receptor gene predict amygdala reactivity in men. Psychoneuroendocrinology 35, 94–104. https://doi.org/10.1016/j.psyneuen.2009.04.013
Marusak, H.A., Carré, J.M., Thomason, M.E., 2013. The stimuli drive the response: An fMRI study of youth processing adult or child emotional face stimuli. Neuroimage 83, 679–689.
McCarthy, M.M., 2016. Multifaceted origins of sex differences in the brain. Philos. Trans. R. Soc. B Biol. Sci. 371. https://doi.org/10.1098/rstb.2015.0106
Morris, J.A., Jordan, C.L., Breedlove, S.M., 2008. Sexual dimorphism in neuronal number of the posterodorsal medial amygdala is independent of circulating androgens and regional volume in adult rats. J. Comp. Neurol. 506, 851–859. https://doi.org/10.1002/cne.21536
Neufang, S., Specht, K., Hausmann, M., Güntürkün, O., Herpertz-Dahlmann, B., Fink, G.R., Konrad, K., 2009. Sex differences and the impact of steroid hormones on the developing human brain. Cereb. Cortex 19, 464–73. https://doi.org/10.1093/cercor/bhn100
Pareto, D., Alvarado, M., Hanrahan, S.M., Biegon, a, 2004. In vivo occupancy of female rat brain estrogen receptors by 17beta-estradiol and tamoxifen. Neuroimage 23, 1161–7. https://doi.org/10.1016/j.neuroimage.2004.07.036
Peper, J.S., Hulshoff Pol, H.E., Crone, E.A., van Honk, J., 2011. Sex steroids and brain structure in pubertal boys and girls: a mini-review of neuroimaging studies. Neuroscience 191, 28–37. https://doi.org/10.1016/j.neuroscience.2011.02.014
Petersen, S.E., van Mier, H., Fiez, J.A., Raichle, M.E., 1998. The effects of practice on the functional anatomy of task performance. Proc. Natl. Acad. Sci. U. S. A. 95, 853–60.
Pfannkuche, K.A., Bouma, A., Groothuis, T.G.G., 2009. Does testosterone affect lateralization of brain and behaviour? A meta-analysis in humans and other animal species. Philos. Trans. R. Soc. B Biol. Sci. 364, 929–942. https://doi.org/10.1098/rstb.2008.0282
Reiman, E.M., Lane, R.D., Ahern, G.L., Schwartz, G.E., Davidson, R.J., Friston, K.J., Yun, L.S., Chen, K., 1997. Neuroanatomical correlates of externally and internally generated human emotion. Am. J. Psychiatry 154, 918–25. https://doi.org/10.1176/ajp.154.7.918
Sano, K., Nakata, M., Musatov, S., Morishita, M., Sakamoto, T., Tsukahara, S., Ogawa, S., 2016. Pubertal activation of estrogen receptor α in the medial amygdala is essential for the full expression of male social behavior in mice. Proc. Natl. Acad. Sci. U. S. A. 113, 7632–7. https://doi.org/10.1073/pnas.1524907113
Savic, I., Lindström, P., 2008. PET and MRI show differences in cerebral asymmetry and functional connectivity between homo- and heterosexual subjects. Proc. Natl. Acad. Sci. U. S. A. 105, 9403–8. https://doi.org/10.1073/pnas.0801566105
Scherf, K.S., Smyth, J.M., Delgado, M.R., 2013. The amygdala: an agent of change in adolescent
Schneider, S., Peters, J., Bromberg, U., Brassen, S., Menz, M.M., Miedl, S.F., Loth, E., Banaschewski, T., Barbot, A., Barker, G., Conrod, P.J., Dalley, J.W., Flor, H., Gallinat, J., Garavan, H., Heinz, A., Itterman, B., Mallik, C., Mann, K., Artiges, E., Paus, T., Poline, J.-B., Rietschel, M., Reed, L., Smolka, M.N., Spanagel, R., Speiser, C., Ströhle, A., Struve, M., Schumann, G., Büchel, C., 2011. Boys do it the right way: sex-dependent amygdala lateralization during face processing in adolescents. Neuroimage 56, 1847–53. https://doi.org/10.1016/j.neuroimage.2011.02.019
Sergerie, K., Chochol, C., Armony, J.L., 2008. The role of the amygdala in emotional processing: A quantitative meta-analysis of functional neuroimaging studies. Neurosci. Biobehav. Rev. 32, 811–830. https://doi.org/10.1016/j.neubiorev.2007.12.002
Sisk, C.L., Zehr, J.L., 2005. Pubertal hormones organize the adolescent brain and behavior. Front. Neuroendocrinol. 26, 163–174. https://doi.org/10.1016/j.yfrne.2005.10.003
Soleman, R.S., Schagen, S.E.E., Veltman, D.J., Kreukels, B.P.C., Cohen-Kettenis, P.T., Lambalk, C.B., Wouters, F., Delemarre-van de Waal, H.A., 2013. Sex differences in verbal fluency during adolescence: a functional magnetic resonance imaging study in gender dysphoric and control boys and girls. J. Sex. Med. 10, 1969–77. https://doi.org/10.1111/jsm.12083
Soleman, R.S., Staphorsius, A.S., Cohen-Kettenis, P.T., Lambalk, C.B., Veltman, D.J., Van Trotsenburg, M.A.A., Hompes, P.G.A., Drent, M.L., De Ronde, W.P., Kreukels, B.P.C., 2016. Oestrogens are Not Related to Emotional Processing: A Study of Regional Brain Activity in Female-to-Male Transsexuals under Gonadal Suppression. Cereb. Cortex 26. https://doi.org/10.1093/cercor/bhu201
Sommer I.E., Cohen-Kettenis P.T., van Raalten T., vd Veer A.J., Ramsey L.E., Gooren L.J.G., Kahn R.S., Ramsey N.F. 2008. Effects of cross-sex hormones on cerebral activation during language and mental rotation: An fMRI study in transsexuals, Eur. Neuropsychopharmacol., 18, 215–221, 10.1016/j.euroneuro.2007.10.002
Stanton, S.J., Wirth, M.M., Waugh, C.E., Schultheiss, O.C., 2009. Endogenous testosterone levels are associated with amygdala and ventromedial prefrontal cortex responses to anger faces in men but not women. Biol. Psychol. 81, 118–122. https://doi.org/10.1016/j.biopsycho.2009.03.004
Staphorsius, A.S., Kreukels, B.P.C., Cohen-Kettenis, P.T., Veltman, D.J., Burke, S.M., Schagen, S.E.E., Wouters, F.M., Delemarre-van de Waal, H.A., Bakker, J., 2015. Puberty suppression and executive functioning: An fMRI-study in adolescents with gender dysphoria. Psychoneuroendocrinology 56, 190–9. https://doi.org/10.1016/j.psyneuen.2015.03.007
Tarr, M.J., Gauthier, I., 2000. FFA: a flexible fusiform area for subordinate-level visual processing automatized by expertise. Nat. Neurosci. 3, 764–9. https://doi.org/10.1038/77666
Tottenham, N., Tanaka, J.W., Leon, A.C., McCarry, T., Nurse, M., Hare, T.A., Marcus, D.J., Westerlund, A., Casey, B., Nelson, C., 2009. The NimStim set of facial expressions: Judgments from untrained research participants. Psychiatry Res. 168, 242–249. https://doi.org/10.1016/j.psychres.2008.05.006
Turner, B.M., Paradiso, S., Marvel, C.L., Pierson, R., Boles Ponto, L.L., Hichwa, R.D., Robinson, R.G., 2007. The cerebellum and emotional experience. Neuropsychologia 45, 1331–41. https://doi.org/10.1016/j.neuropsychologia.2006.09.023
Uematsu, A., Matsui, M., Tanaka, C., Takahashi, T., Noguchi, K., Suzuki, M., Nishijo, H., 2012. Developmental Trajectories of Amygdala and Hippocampus from Infancy to Early Adulthood in Healthy Individuals. PLoS One 7, e46970. https://doi.org/10.1371/journal.pone.0046970
van Strien, J.W., 2002. Vragenlijst voor Handvoorkeur. Ned. Tijdschr. Psychol. 47, 88–92.
van Wingen, G.A., Zylicz, S.A., Pieters, S., Mattern, C., Verkes, R.J., Buitelaar, J.K., Fernández, G., 2009. Testosterone Increases Amygdala Reactivity in Middle-Aged Women to a Young Adulthood Level. Neuropsychopharmacology 34, 539–547. https://doi.org/10.1038/npp.2008.2
Wager, T.D., Phan, K.L., Liberzon, I., Taylor, S.F., 2003. Valence, gender, and lateralization of functional brain anatomy in emotion: a meta-analysis of findings from neuroimaging. Neuroimage 19, 513–531. https://doi.org/10.1016/S1053-8119(03)00078-8
Wallen, K., 2005. Hormonal influences on sexually differentiated behavior in nonhuman primates. Front. Neuroendocrinol. 26, 7–26. https://doi.org/10.1016/j.yfrne.2005.02.001
Wilke, M., Lidzba, K., 2007. LI-tool: a new toolbox to assess lateralization in functional MR-data. J. Neurosci. Methods 163, 128–36. https://doi.org/10.1016/j.jneumeth.2007.01.026
Witelson, S.F., Nowakovski, R.S., 1991. Left out axons make men right: a hypothesis for the origin of handedness and functional asymmetry. Neuropsychologia 29, 327-333.
