Amygdala structure and aggressiveness in borderline personality disorder

  • Falk Mancke
  • Sabine C. Herpertz
  • Dusan Hirjak
  • Rebekka Knies
  • Katja Bertsch
Original Paper

Abstract

Aggressiveness is considered an important clinical feature of borderline personality disorder (BPD) and has been associated with alterations of the amygdala. However, studies that analyzed the exact location of amygdala alterations associated with aggressiveness in BPD or that systematically compared female and male BPD patients are missing. In the current study, we therefore investigated a sex-mixed sample of BPD patients and healthy volunteers and applied an automated segmentation method that allows the study of both, alterations of amygdala volume and localized amygdala shape. Volumetric results revealed no difference in amygdala volume between BPD patients and healthy volunteers, but a trend for a positive association between volume of the right amygdala and aggressiveness in male BPD patients. Analyses of amygdala shape showed a trend for a group by sex interaction effect in the left laterobasal amygdala, without a difference in subgroup analyses. Finally, regions of the left superficial and laterobasal amygdala of male BPD patients were positively associated with aggressiveness. In sum, our results emphasize the need to consider sex-specific effects and demonstrate a link between male BPD patients’ aggressiveness and amygdala regions that are particularly related to social information processing and associative emotional learning.

Keywords

Volume Shape Surface Superficial amygdala Cortical amygdala Laterobasal amygdala 

Notes

Acknowledgements

The study was supported by Grants from the German Research Foundation (DFG) awarded to S. C. Herpertz within the KFO 256 (He 2660/12-1; He 2660/7-2).

Compliance with ethical standards

Conflict of interest

None.

Supplementary material

406_2016_747_MOESM1_ESM.pptx (73 kb)
Partial regression plots depicting the association between whole right amygdala volume and aggressiveness in BPD patients and healthy volunteers (HV). Values of both axes are residual scores after regressing each variable of interest onto the control variables and were z-transformed before analysis. (PPTX 72 kb)
406_2016_747_MOESM2_ESM.pptx (191 kb)
Region of the left laterobasal amygdala from an anterior view that showed a trend for a group by sex interaction. Blue depicts the amygdala mask. Orange depicts voxels that were significant at the < .10 level, fwe. (PPTX 191 kb)
406_2016_747_MOESM3_ESM.pptx (64 kb)
Partial regression plots depicting the associations between regions (see Table S2 for exact localization) of the left amygdala and aggressiveness in female BPD patients and healthy volunteers. Values of the x-axes derive from the vertex analysis of the voxel with the lowest p -value. These values represent the signed, perpendicular distance from the average amygdala shape of the group under study. Values of all axes are residual scores after regressing each variable of interest onto the control variables and were z-transformed before analysis. (PPTX 63 kb)
406_2016_747_MOESM4_ESM.docx (21 kb)
Differences in amygdala shape between BPD patients and healthy volunteers (HV). All p -values are family-wise error - corrected. -values < .05 are in bold. Location of cluster refers to the amygdala subregion with the highest probability according to Juelich Histological Atlas. (DOCX 21 kb)
406_2016_747_MOESM5_ESM.docx (92 kb)
Differences in amygdala shape between BPD patients and healthy volunteers (HV). All -values are family-wise error - corrected. -values < .05 are in bold. Location of cluster refers to the amygdala subregion with the highest probability according to Juelich Histological Atlas. (DOCX 92 kb)

References

  1. 1.
    Anderson CA, Bushman BJ (2002) Human aggression. Annu Rev Psychol 53:27–51. doi: 10.1146/annurev.psych.53.100901.135231 CrossRefPubMedGoogle Scholar
  2. 2.
    Buss A (1961) The psychology of aggression. Wiley, HobokenCrossRefGoogle Scholar
  3. 3.
    Newhill CE, Eack SM, Mulvey EP (2009) Violent behavior in borderline personality. J Pers Disord 23:541–554. doi: 10.1521/pedi.2009.23.6.541 CrossRefPubMedGoogle Scholar
  4. 4.
    Soloff PH, Meltzer C, Becker C (2003) Impulsivity and prefrontal hypometabolism in borderline personality disorder. Psychiatry Res Neuroimaging 123:153–163. doi: 10.1016/S0925-4927 CrossRefGoogle Scholar
  5. 5.
    Whisman M, Schonbrun Y (2009) Social consequences of borderline personality disorder symptoms in a population-based survey: marital distress, marital violence, and marital disruption. J Pers Disord 23:410–415CrossRefPubMedGoogle Scholar
  6. 6.
    McCloskey MS, New AS, Siever LJ et al (2009) Evaluation of behavioral impulsivity and aggression tasks as endophenotypes for borderline personality disorder. J Psychiatr Res 43:1036–1048. doi: 10.1016/j.jpsychires.2009.01.002 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Mancke F, Herpertz SC, Bertsch K (2015) Aggression in borderline personality disorder - a multidimensional model. Personal Disord Theory, Res Treat 6:278–291. doi: 10.1037/per0000098 CrossRefGoogle Scholar
  8. 8.
    Berkowitz L (1993) Aggression: its causes, consequences, and control. McGraw-Hill, New YorkGoogle Scholar
  9. 9.
    Barratt ES, Felthous AR (2003) Impulsive versus premeditated aggression: implications for mens rea decisions. Behav Sci Law 21:619–630. doi: 10.1002/bsl.555 CrossRefPubMedGoogle Scholar
  10. 10.
    Poulin F, Boivin M (2000) Reactive and proactive aggression: evidence of a two-factor model. Psychol Assess 12:115–122CrossRefPubMedGoogle Scholar
  11. 11.
    Dougherty D, Bjork JM, Huckabee HC et al (1999) Laboratory measures of aggression and impulsivity in women with borderline personality disorder. Psychiatry Res 85:315–326CrossRefPubMedGoogle Scholar
  12. 12.
    New AS, Hazlett EA, Newmark RE et al (2009) Laboratory induced aggression: a positron emission tomography study of aggressive individuals with borderline personality disorder. Biol Psychiatry 66:1107–1114. doi: 10.1016/j.biopsych.2009.07.015 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Rosell DR, Siever LJ (2015) The neurobiology of aggression and violence. CNS Spectr 20:254–279. doi: 10.1017/S109285291500019X CrossRefPubMedGoogle Scholar
  14. 14.
    Ruocco AC, Amirthavasagam S, Zakzanis KK (2012) Amygdala and hippocampal volume reductions as candidate endophenotypes for borderline personality disorder: a meta-analysis of magnetic resonance imaging studies. Psychiatry Res 201:245–252. doi: 10.1016/j.pscychresns.2012.02.012 CrossRefPubMedGoogle Scholar
  15. 15.
    Schulze L, Schmahl C, Niedtfeld I (2016) Neural correlates of disturbed emotion processing in borderline personality disorder: a multimodal meta-analysis. Biol Psychiatry 79:97–106. doi: 10.1016/j.biopsych.2015.03.027 CrossRefPubMedGoogle Scholar
  16. 16.
    Matthies S, Rüsch N, Weber M et al (2012) Small amygdala-high aggression? The role of the amygdala in modulating aggression in healthy subjects. World J Biol Psychiatry 13:75–81. doi: 10.3109/15622975.2010.541282 CrossRefPubMedGoogle Scholar
  17. 17.
    Bobes MA, Ostrosky F, Diaz K et al (2013) Linkage of functional and structural anomalies in the left amygdala of reactive-aggressive men. Soc Cogn Affect Neurosci 8:928–936. doi: 10.1093/scan/nss101 CrossRefPubMedGoogle Scholar
  18. 18.
    Pardini D, Erickson K, Loeber R, Raine A (2013) Lower amygdala volume in men is associated with childhood aggression, early psychopathic traits, and future violence. Biol Psychiatry 75:73–80CrossRefPubMedGoogle Scholar
  19. 19.
    Zetzsche T, Preuss UW, Frodl T et al (2007) Hippocampal volume reduction and history of aggressive behaviour in patients with borderline personality disorder. Psychiatry Res 154:157–170. doi: 10.1016/j.pscychresns.2006.05.010 CrossRefPubMedGoogle Scholar
  20. 20.
    Gopal A, Clark E, Allgair A et al (2013) Dorsal/ventral parcellation of the amygdala: relevance to impulsivity and aggression. Psychiatry Res - Neuroimaging 211:24–30. doi: 10.1016/j.pscychresns.2012.10.010 CrossRefGoogle Scholar
  21. 21.
    Sah P, Faber ESL, Armentia MLDE, Power J (2009) The amygdaloid complex: anatomy and physiology. 83:803–834. doi: 10.1152/physrev.00002.2003 Google Scholar
  22. 22.
    Schmahl C, Herpertz S, Bertsch K et al (2014) Mechanisms of disturbed emotion processing and social interaction in borderline personality disorder: state of knowledge and research agenda of the German Clinical Research Unit. Borderline Personal Disord Emot Dysregulation 1:1–17CrossRefGoogle Scholar
  23. 23.
    Loranger AW, Sartorius N, Andreoli A et al (1994) The International Personality Disorder Examination. The World Health Organization/Alcohol, Drug Abuse, and Mental Health Administration international pilot study of personality disorders. Arch Gen Psychiatry 51:215–224CrossRefPubMedGoogle Scholar
  24. 24.
    Wittchen H, Zaudig M, Fydrich T (1997) SKID: Strukturiertes klinisches Interview für DSM-IV. Achse I und II, HogrefeGoogle Scholar
  25. 25.
    Buss A, Perry M (1992) The Aggression Questionnaire. J Pers Soc Psychol 63:452–459CrossRefPubMedGoogle Scholar
  26. 26.
    Beck AT, Steer RA, Brown GK (1996) Manual for the Beck Depression Inventory-II. Psychological Corporation, San AntonioGoogle Scholar
  27. 27.
    Bernstein D, Fink L (1998) Childhood Trauma Questionnaire. A retrospective self-report manual. The Psychological Corporation, San AntonioGoogle Scholar
  28. 28.
    Rösler M, Retz W, Retz-Junginger P et al (2004) Instrumente zur Diagnostik der Aufmerksamkeitsdefizit-/Hyperaktivitätsstörung (ADHS) im Erwachsenenalter. Selbstbeurteilungsskala (ADHS-SB) und Diagnosecheckliste (ADHS-DC). Nervenarzt 75:888–895. doi: 10.1007/s00115-003-1622-2 CrossRefPubMedGoogle Scholar
  29. 29.
    Raven J (2009) Standard Progressive Matrices (SPM). Deutsche Bearbeitung und Normierung nach J. C. Raven, 2th ed. earson Assessment., FrankfurtGoogle Scholar
  30. 30.
    Jenkinson M, Beckmann CF, Behrens TEJ et al (2012) Fsl. Neuroimage 62:782–790. doi: 10.1016/j.neuroimage.2011.09.015 CrossRefPubMedGoogle Scholar
  31. 31.
    Smith S, De Stefano N, Jenkinson M, Matthews PM (2001) Normalized accurate measurement of longitudinal brain change. J Comput Assist Tomogr 25:466–475. doi: 10.1097/00004728-200105000-00022 CrossRefPubMedGoogle Scholar
  32. 32.
    Smith S, Zhang Y, Jenkinson M et al (2002) Accurate, robust, and automated longitudinal and cross-sectional brain change analysis. Neuroimage 17:479–489. doi: 10.1006/nimg.2002.1040 CrossRefPubMedGoogle Scholar
  33. 33.
    Eickhoff SB, Paus T, Caspers S et al (2007) Assignment of functional activations to probabilistic cytoarchitectonic areas revisited. Neuroimage 36:511–521. doi: 10.1016/j.neuroimage.2007.03.060 CrossRefPubMedGoogle Scholar
  34. 34.
    Amunts K, Kedo O, Kindler M et al (2005) Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: intersubject variability and probability maps. Anat Embryol (Berl) 210:343–352. doi: 10.1007/s00429-005-0025-5 CrossRefGoogle Scholar
  35. 35.
    de-Almeida CP, Wenzel A, de-Carvalho CS, et al (2012) Amygdalar volume in borderline personality disorder with and without comorbid post-traumatic stress disorder: a meta-analysis. CNS Spectr 17:70–5. doi:  10.1017/S1092852912000466
  36. 36.
    Niedtfeld I, Schulze L, Krause-Utz A et al (2013) Voxel-based morphometry in women with borderline personality disorder with and without comorbid posttraumatic stress disorder. PLoS ONE 8:e65824. doi: 10.1371/journal.pone.0065824 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Zetzsche T, Frodl T, Preuss UW et al (2006) Amygdala volume and depressive symptoms in patients with borderline personality disorder. Biol Psychiatry 60:302–310. doi: 10.1016/j.biopsych.2005.11.020 CrossRefPubMedGoogle Scholar
  38. 38.
    Winkler AM, Ridgway GR, Webster M et al (2014) Permutation inference for the general linear model. Neuroimage 92:381–397. doi: 10.1016/j.neuroimage.2014.01.060 CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Smith S, Nichols TE (2009) Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 44:83–98. doi: 10.1016/j.neuroimage.2008.03.061 CrossRefPubMedGoogle Scholar
  40. 40.
  41. 41.
  42. 42.
    Kim HJ, Kim N, Kim S et al (2012) Sex differences in amygdala subregions: evidence from subregional shape analysis. Neuroimage 60:2054–2061. doi: 10.1016/j.neuroimage.2012.02.025 CrossRefPubMedGoogle Scholar
  43. 43.
    Eid M, Gollwitz M, Schmitt M (2013) Statistik und Forschungsmethoden: Lehrbuch. BeltzGoogle Scholar
  44. 44.
    Campbell A (2006) Sex differences in direct aggression: what are the psychological mediators? Aggress Violent Behav 11:237–264. doi: 10.1016/j.avb.2005.09.002 CrossRefGoogle Scholar
  45. 45.
    Mancke F, Bertsch K, Herpertz S (2015) Gender differences in aggression of borderline personality disorder. Borderline Personal Disord Emot Dysregulation 2:1–12CrossRefGoogle Scholar
  46. 46.
    Silberschmidt A, Lee S, Zanarini M, Schulz SC (2015) Gender differences in borderline personality disorder: results from a multinational, clinical trial sample. J Pers Disord. doi: 10.1521/pedi_2014_28_175 PubMedGoogle Scholar
  47. 47.
    Brambilla P, Soloff PH, Sala M et al (2004) Anatomical MRI study of borderline personality disorder patients. Psychiatry Res 131:125–133. doi: 10.1016/j.pscychresns.2004.04.003 CrossRefPubMedGoogle Scholar
  48. 48.
    New AS, Hazlett EA, Buchsbaum MS et al (2007) Amygdala-prefrontal disconnection in borderline personality disorder. Neuropsychopharmacology 32:1629–1640. doi: 10.1038/sj.npp.1301283 CrossRefPubMedGoogle Scholar
  49. 49.
    Chanen AM, Velakoulis D, Carison K et al (2008) Orbitofrontal, amygdala and hippocampal volumes in teenagers with first-presentation borderline personality disorder. Psychiatry Res 163:116–125. doi: 10.1016/j.pscychresns.2007.08.007 CrossRefPubMedGoogle Scholar
  50. 50.
    Schmahl C, Berne K, Krause A et al (2009) Hippocampus and amygdala volumes in patients with borderline personality disorder with or without posttraumatic stress disorder. J Psychiatry Neurosci 34:289–295. doi: 10.1521/pedi.2009.23.4.333 PubMedPubMedCentralGoogle Scholar
  51. 51.
    Minzenberg MJ, Fan J, New AS et al (2008) Frontolimbic structural changes in borderline personality disorder. J Psychiatr Res 42:727–733. doi: 10.1016/j.jpsychires.2007.07.015 CrossRefPubMedGoogle Scholar
  52. 52.
    Wrase J, Ph D, Makris N et al (2008) Amygdala volume associated with alcohol abuse relapse and craving. Am J Psychiatry 165:1179–1184CrossRefPubMedGoogle Scholar
  53. 53.
    Navari S, Dazzan P (2009) Do antipsychotic drugs affect brain structure? A systematic and critical review of MRI findings. Psychol Med 39:1763–1777. doi: 10.1017/S0033291709005315 CrossRefPubMedGoogle Scholar
  54. 54.
    Giedd JN, Raznahan A, Mills KL, Lenroot RK (2012) Review: magnetic resonance imaging of male/female differences in human adolescent brain anatomy. Biol Sex Differ 3:1–9. doi: 10.1186/2042-6410-3-19 CrossRefGoogle Scholar
  55. 55.
    Schmahl C, Vermetten E, Elzinga BM, Bremner JD (2003) Magnetic resonance imaging of hippocampal and amygdala volume in women with childhood abuse and borderline personality disorder. Psychiatry Res - Neuroimaging 122:193–198. doi: 10.1016/S0925-4927(03)00023-4 CrossRefGoogle Scholar
  56. 56.
    Weniger G, Lange C, Sachsse U, Irle E (2009) Reduced amygdala and hippocampus size in trauma-exposed women with borderline personality disorder and without posttraumatic stress disorder. J Psychiatry Neurosci 34:383–388PubMedPubMedCentralGoogle Scholar
  57. 57.
    Driessen M, Herrmann J, Stahl K et al (2000) Magnetic resonance imaging volumes of the hippocampus and the amygdala in women with borderline personality disorder and early traumatization. Arch Gen Psychiatry 57:1115–1122CrossRefPubMedGoogle Scholar
  58. 58.
    Tebartz van Elst L, Ludaescher P, Thiel T et al (2007) Evidence of disturbed amygdalar energy metabolism in patients with borderline personality disorder. Neurosci Lett 417:36–41. doi: 10.1016/j.neulet.2007.02.071 CrossRefPubMedGoogle Scholar
  59. 59.
    Tebartz Van Elst L, Hesslinger B, Thiel T (2003) Frontolimbic brain abnormalities in patients with borderline personality disorder: a volumetric magnetic resonance imaging study. Biol Psychiarry 54:163–171. doi: 10.1016/S0006-3223(03)01743-2 CrossRefGoogle Scholar
  60. 60.
    Fischbach F, Müller M, Bruhn H (2008) Magnetic resonance imaging of the cranial nerves in the posterior fossa: a comparative study of t2-weighted spin-echo sequences at 1.5 and 3.0 tesla. Acta Radiol 49:358–363. doi: 10.1080/02841850701824127 CrossRefPubMedGoogle Scholar
  61. 61.
    Huang BY, Castillo M (2009) Neurovascular imaging at 1.5 tesla versus 3.0 tesla. Magn Reson Imaging Clin N Am 17:29–46. doi: 10.1016/j.mric.2008.12.005 CrossRefPubMedGoogle Scholar
  62. 62.
    American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders, 5th edn. American Psychiatric Publishing, ArlingtonCrossRefGoogle Scholar
  63. 63.
    Wilke M, Krägeloh-Mann I, Holland SK (2007) Global and local development of gray and white matter volume in normal children and adolescents. Exp Brain Res 178:296–307. doi: 10.1007/s00221-006-0732-z CrossRefPubMedGoogle Scholar
  64. 64.
    Suzuki M, Hagino H, Nohara S et al (2005) Male-specific volume expansion of the human hippocampus during adolescence. Cereb Cortex 15:187–193. doi: 10.1093/cercor/bhh121 CrossRefPubMedGoogle Scholar
  65. 65.
    Schienle A, Leutgeb V, Wabnegger A (2015) Symptom severity and disgust-related traits in borderline personality disorder: the role of amygdala subdivisions. Psychiatry Res Neuroimaging 232:203–207. doi: 10.1016/j.pscychresns.2015.04.002 CrossRefGoogle Scholar
  66. 66.
    Olsson A, Phelps E (2007) Social learning of fear. Nat Neurosci 10:1095–1102. doi: 10.1038/nn1968 CrossRefPubMedGoogle Scholar
  67. 67.
    Ebner-Priemer UW, Mauchnik J, Kleindienst N et al (2009) Emotional learning during dissociative states in borderline personality disorder. J Psychiatry Neurosci 34:214–222PubMedPubMedCentralGoogle Scholar
  68. 68.
    Krause-Utz A, Keibel-Mauchnik J, Ebner-Priemer U et al (2015) Classical conditioning in borderline personality disorder: an fMRI study. Eur Arch Psychiatry Clin Neurosci. doi: 10.1007/s00406-015-0593-1 PubMedGoogle Scholar
  69. 69.
    Blair R (2013) The neurobiology of psychopathic traits in youths. Nat Rev Neurosci 14:786–799. doi: 10.1038/nrn3577 CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Bzdok D, Laird AR, Zilles K et al (2013) An investigation of the structural, connectional, and functional subspecialization in the human amygdala. Hum Brain Mapp 34:3247–3266. doi: 10.1002/hbm.22138 CrossRefPubMedGoogle Scholar
  71. 71.
    Goossens L, Kukolja J, Onur O et al (2009) Selective processing of social stimuli in the superficial amygdala. Hum Brain Mapp 30:3332–3338. doi: 10.1002/hbm.20755 CrossRefPubMedGoogle Scholar
  72. 72.
    Koelsch S, Skouras S, Fritz T et al (2013) The roles of superficial amygdala and auditory cortex in music-evoked fear and joy. Neuroimage 81:49–60. doi: 10.1016/j.neuroimage.2013.05.008 CrossRefPubMedGoogle Scholar
  73. 73.
    Dodge K, Malone PS, Lansford JE et al (2015) Hostile attributional bias and aggressive behavior in global context. Proc Natl Acad Sci 112:201418572. doi: 10.1073/pnas.1418572112 Google Scholar
  74. 74.
    Daros AR, Zakzanis KK, Ruocco AC (2012) Facial emotion recognition in borderline personality disorder. Psychol Med 43:1953–1963. doi: 10.1017/S0033291712002607 CrossRefPubMedGoogle Scholar
  75. 75.
    Izurieta N, Nagy K, Mancke F et al (2015) Time course of facial emotion processing in borderline personality disorder – an ERP study. J Psychiatry Neurosci 41:16–26. doi: 10.1503/jpn.140215 CrossRefGoogle Scholar
  76. 76.
    LeDoux J (2003) The emotional brain, fear, and the amygdala. Cell Mol Neurobiol 23:727–738. doi: 10.1023/A:1025048802629 CrossRefPubMedGoogle Scholar
  77. 77.
    Vuilleumier P (2005) How brains beware: neural mechanisms of emotional attention. Trends Cogn Sci 9:585–594. doi: 10.1016/j.tics.2005.10.011 CrossRefPubMedGoogle Scholar
  78. 78.
    Bohland JW, Bokil H, Allen CB, Mitra PP (2009) The brain atlas concordance problem: quantitative comparison of anatomical parcellations. PLoS ONE 4:e7200. doi: 10.1371/journal.pone.0007200 CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Domes G, Schulze L, Böttger M et al (2010) The neural correlates of sex differences in emotional reactivity and emotion regulation. Hum Brain Mapp 31:758–769. doi: 10.1002/hbm.20903 CrossRefPubMedGoogle Scholar
  80. 80.
    Hofer A, Siedentopf CM, Ischebeck A et al (2006) Gender differences in regional cerebral activity during the perception of emotion: a functional MRI study. Neuroimage 32:854–862. doi: 10.1016/j.neuroimage.2006.03.053 CrossRefPubMedGoogle Scholar
  81. 81.
    Sergerie K, Chochol C, Armony JL (2008) The role of the amygdala in emotional processing: a quantitative meta-analysis of functional neuroimaging studies. Neurosci Biobehav Rev 32:811–830. doi: 10.1016/j.neubiorev.2007.12.002 CrossRefPubMedGoogle Scholar
  82. 82.
    Kim N, Kim HJ, Hwang J et al (2011) Amygdalar shape analysis method using surface contour aligning, spherical mapping, and probabilistic subregional segmentation. Neurosci Lett 488:65–69. doi: 10.1016/j.neulet.2010.11.005 CrossRefPubMedGoogle Scholar
  83. 83.
    Österlund MK, Gustafsson J-A, Keller E, Hurd YL (2000) Estrogen receptor beta (ERbeta) messenger ribonucleic acid (mRNA) expression within the human forebrain: distinct distribution pattern to ERalpha RNA. J Clin Endocrinol Metab 85:3840–3846. doi: 10.1210/jc.85.10.3840 PubMedGoogle Scholar
  84. 84.
    Cao J, Patisaul HB (2011) Sexually dimorphic expression of hypothalamic estrogen receptors α and β and Kiss1 in neonatal male and female rats. J Comp Neurol 519:2954–2977. doi: 10.1002/cne.22648 CrossRefPubMedGoogle Scholar
  85. 85.
    Kozak MJ, Cuthbert BN (2016) The NIMH Research Domain Criteria Initiative: background, issues, and pragmatics. Psychophysiology 53:286–297. doi: 10.1111/psyp.12518 CrossRefPubMedGoogle Scholar
  86. 86.
    Sassenrath EN, Rowell TE, Hendrickx AG (1973) Perimenstrual aggression in groups of female rhesus monkeys. J Reprod Fertil 34:509–511. doi: 10.1530/jrf.0.0340509 CrossRefPubMedGoogle Scholar
  87. 87.
    Dougherty D, Bjork JM, Moeller FG, Swann AC (1997) The influence of menstrual-cycle phase on the relationship between testosterone and aggression. Physiol Behav 62:431–435CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of General Psychiatry, Center for Psychosocial MedicineUniversity of HeidelbergHeidelbergGermany
  2. 2.Department of Psychiatry and Psychotherapy, Central Institute of Mental HealthMedical Faculty Mannheim/Heidelberg UniversityMannheimGermany
  3. 3.Department of Psychosomatic Medicine and Psychotherapy, Central Institute of Mental HealthMedical Faculty Mannheim/Heidelberg UniversityMannheimGermany

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