Psychoneuroendocrinology
Volume 33, Issue 8 , Pages 1031-1040 , September 2008

Facial emotion recognition and amygdala activation are associated with menstrual cycle phase

  • Birgit Derntl

      Affiliations

    • MR Centre of Excellence, Medical University of Vienna, Vienna, Austria
    • Institute for Clinical, Biological and Differential Psychology, Faculty of Psychology, University of Vienna, Vienna, Austria
    • Department of Psychiatry and Psychotherapy, RWTH Aachen University, Pauwelsstrasse 30, 52074 Aachen, Germany
    • Corresponding Author InformationCorresponding author at: Department of Psychiatry and Psychotherapy, RWTH Aachen University, Pauwelsstrasse 30, 52074 Aachen, Germany. Tel.: +49 241 8080279; fax: +49 241 8082401.
    • ,
  • Christian Windischberger

      Affiliations

    • MR Centre of Excellence, Medical University of Vienna, Vienna, Austria
    • Centre for Biomedical Engineering and Physics, Medical University of Vienna, Vienna, Austria
    • ,
  • Simon Robinson

      Affiliations

    • MR Centre of Excellence, Medical University of Vienna, Vienna, Austria
    • Center of Mind/Brain Sciences, University of Trento, Mattarello, Italy
    • ,
  • Elisabeth Lamplmayr

      Affiliations

    • Institute for Clinical, Biological and Differential Psychology, Faculty of Psychology, University of Vienna, Vienna, Austria
    • ,
  • Ilse Kryspin-Exner

      Affiliations

    • Institute for Clinical, Biological and Differential Psychology, Faculty of Psychology, University of Vienna, Vienna, Austria
    • ,
  • Ruben C. Gur

      Affiliations

    • Department of Psychiatry, University of Pennsylvania Medical School, Philadelphia, USA
    • ,
  • Ewald Moser

      Affiliations

    • MR Centre of Excellence, Medical University of Vienna, Vienna, Austria
    • Centre for Biomedical Engineering and Physics, Medical University of Vienna, Vienna, Austria
    • Department of Psychiatry, University of Pennsylvania Medical School, Philadelphia, USA
    • ,
  • Ute Habel

      Affiliations

    • Department of Psychiatry and Psychotherapy, RWTH Aachen University, Pauwelsstrasse 30, 52074 Aachen, Germany

Received 8 February 2008 ,Revised 7 April 2008 ,Accepted 8 April 2008.

References 

  1. Adolphs R. Neural systems for recognizing emotion. Curr. Opin. Neurobiol. 2002;12:169–177
  2. Aikey JL, Nyby JG, Anmuth DM, James PJ. Testosterone rapidly reduces anxiety in male house mice (mus musculus). Horm. Behav. 2002;42:448–460
  3. Akwa Y, Purdy RH, Koob GF, Britton KT. The amygdala mediates the anxiolytic-like effect of the neurosteroid allopregnanolone in rat. Behav. Brain Res. 1999;106:119–125
  4. Amin Z, Epperson CN, Constable RT, Canli T. Effects of estrogen variation on neural correlates of emotional response inhibition. Neuroimage. 2006;32:457–464
  5. Andréen L, Sundström-Poromaa I, Bixo M, Nyberg S, Bäckström T. Allopregnanolone concentration and mood—a bimodal association in postmenopausal women treated with oral progesterone. Psychopharmacology (Berlin). 2006;187:209–221
  6. Bagby RM, Parker JDA, Taylor GJ. The twenty-item toronto alexithymia scale–I. Item selection and cross-validation of the factor structure. J. Psychosom. Res. 1994;38:33–40
  7. Becker JB, Arnold AP, Berkley KJ, Blaustein JD, Eckel LA, Hampson E, et al. Strategies and methods for research on sex differences in brain and behavior. Endocrinology. 2005;146:1650–1673
  8. Bethea CL, Pecins-Thompson M, Schutzer WE, Gundlah C, Lu ZN. Ovarian steroids and serotonin neural function. Mol. Neurobiol. 1998;18:87–123
  9. Boissy A, Bouissou MF. Effects of androgen treatment on behavioural and physiological responses of heifers to fear-eliciting situations. Horm. Behav. 1994;28:66–83
  10. Burris AS, Banks SM, Carter CS, Davidson JM, Sherins RJ. A long-term, prospective study of the physiologic and behavioral effects of hormone replacement in untreated hypogonadal men. J. Androl. 1992;13:297–304
  11. Conway CA, Jones BC, DeBruine LM, Welling LLM, Law Smith MJ, Perrett DI, et al. Salience of emotional displays of danger and contagion in faces is enhanced when progesterone levels are raised. Horm. Behav. 2007;51:202–206
  12. Derntl B, Kryspin-Exner I, Fernbach EM, Moser E, Habel U. Emotion recognition accuracy in healthy young females is associated with cycle phase. Horm. Behav. 2008;53:90–95
  13. Dreher JC, Schmidt PJ, Kohn P, Furman D, Rubinow D, Berman KF. Menstrual cycle phase modulates reward-related neural function in women. Proc. Natl. Acad. Sci. U.S.A. 2007;104:2465–2470
  14. Engin E, Treit D. The anxiolytic-like effects of allopregnanolone vary as a function of intracerebral microinfusion site: the amygdala, medial prefrontal cortex, or hippocampus. Behav. Pharmacol. 2007;18:461–470
  15. Epperson CN, Wisner KL, Yamamoto B. Gonadal steroids in the treatment of mood disorders. Psychosom. Med. 1999;61:676–697
  16. Fernandez G, Weis S, Stoffel-Wagner B, Tendolkar I, Reuber M, Beyenburg S, et al. Menstrual cycle-dependent neural plasticity in the adult human brain is hormone, task, and region specific. J. Neurosci. 2003;23:3790–3795
  17. Fish EW, Faccidomo S, DeBold JF, Miczek KA. Alcohol, allopregnanolone and aggression in mice. Psychopharmacology (Berlin). 2001;153:473–483
  18. Frye CA, Seliga AM. Testosterone increases analgesia, anxiolysis, and cognitive performance in male rats. Cogn. Affect Behav. Neurosci. 2001;1:371–381
  19. Gangestad SW, Garvar-Apgar CE, Simpson JA, Cousins AJ. Changes in women's mate preferences across the ovulatory cycle. J. Pers. Soc. Psychol. 2007;92:151–163
  20. Glover GH, Li TQ, Ress D. Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magn. Reson. Med. 2000;44:162–167
  21. Goldstein JM, Jerram M, Poldrack R, Ahern T, Kennedy DN, Seidman LJ, et al. Hormonal cycle modulates arousal circuitry in women using functional magnetic resonance imaging. J. Neurosci. 2005;25:9309–9316
  22. Gur RC, Ewin RJ, Gur RE. Neurobehavioral probes for physiologic neuroimaging studies. Arch. Gen. Psychiatry. 1992;49:409–414
  23. Gur RC, Sara R, Hagendoorn M, Marom O, Hughett P, Macy L, et al. A method for obtaining 3-dimensional facial expressions and its standardization for use in neurocognitive studies. J. Neurosci. Methods. 2002;115:137–143
  24. Gur RC, Schroeder L, Turner T, McGrath C, Chan RM, Turetsky BI, et al. Brain activation during facial emotion processing. Neuroimage. 2002;16:651–662
  25. Habel U, Windischberger C, Derntl B, Robinson S, Kryspin-Exner I, Gur RC, et al. Amygdala activation and facial expressions: explicit emotion discrimination versus implicit emotion processing. Neuropsychologia. 2007;45:2369–2377
  26. Hermans EJ, Putman P, Baas JM, Koppeschaar HP, van Honk J. A single administration of testosterone reduces fear-potentiated startle in humans. Biol. Psychiatry. 2006;59:872–874
  27. Hiroi R, Neumaier JF. Differential effects of ovarian steroids on anxiety versus fear as measured by open field test and fear-potentiated startle. Behav. Brain Res. 2006;166:93–100
  28. Hoheisel B, Kryspin-Exner I. Emotionserkennung in Gesichtern und emotionales Gesichtergedächtnis—Neuropsychologische Erkenntnisse und Darstellung von Einflussfaktoren. Zeitschrift Neuropsy. 2005;16:77–87(emotion recognition and memory for emotional faces—neuropsychological findings and influencing factors)
  29. Hu X, Le TH, Parrish T, Erhard P. Retrospective estimation and correction of physiological fluctuation in functional MRI. Magn. Reson. Med. 1995;34:201–212
  30. Johnson MR, Carter G, Grint C, Lightman SL. Relationship between ovarian steroids, gonadotrophins and relaxin during the menstrual cycle. Acta Endocrinol. 1993;129:121–125
  31. Kurshan N, Neill Epperson C. Oral contraceptives and mood in women with and without premenstrual dysphoria: a theoretical model. Arch. Women's Ment. Health. 2006;9:1–14
  32. Loy R. Sexual dimorphism in the septohippocampal system. In:  Isaacson RL,  Pribram KH editor. The Hippocampus. New York: Plenum; 1986;p. 301–321
  33. Macrae CN, Alnwick KA, Milne AB, Schloerscheidt AM. Person perception across the menstrual cycle: hormonal influences on social-cognitive functioning. Psychol. Sci. 2002;13:532–536
  34. McEwen BS, Alves SE, Bulloch K, Weiland NJ. Ovarian steroids and the brain: implications for cognition and aging. Neurology. 1997;48:S8–S15
  35. Moonen CTW, Bandettini PA, Aquirre GK. Functional MRI. New York: Springer; 1999;
  36. Moser E, Derntl B, Robinson S, Fink B, Gur RC, Grammer K. Amygdala activation at 3T in response to human and avatar facial expressions of emotions. J. Neurosci. Methods. 2007;161:126–133
  37. Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9:97–113
  38. Osterlund MK, Hurd YL. Estrogen receptors in the human forebrain and the relation to neuropsychiatric disorders. Prog. Neurobiol. 2001;64:251–267
  39. Pearson R, Lewis MB. Fear recognition across the menstrual cycle. Horm. Behav. 2005;47:267–271
  40. Protopopescu X, Pan H, Altemus M, Tuescher O, Polanecsky M, McEwen B, et al. Orbitofrontal cortex activity related to emotional processing changes across the menstrual cycle. Proc. Natl. Acad. Sci. U.S.A. 2005;102:16060–16062
  41. Robinson S, Hoheisel B, Windischberger C, Habel U, Lanzenberger R, Moser E. FMRI of the emotions: towards an improved understanding of amygdala function. Med. Imaging Rev. 2005;1:115–129
  42. Robinson S, Pripfl J, Bauer H, Moser E. Empirical evidence for the minimum voxel size required for reliable 3T fMRI of the amygdala. Neuroimage. 2005;26:S35
  43. Robinson S, Windischberger C, Rauscher A, Moser E. Optimized 3T EPI of the amygdalae. Neuroimage. 2004;22:203–210
  44. Talairach J, Tournoux P. Co-planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System—An Approach to Cerebral Imaging. New York: Thieme; 1988;
  45. Triantafyllou C, Hoge RD, Krüger G, Wiggins CJ, Potthast A, Wiggins GC, et al. Comparison of physiological noise at 1.5T, 3T and 7T and optimization of fMRI acquisition parameters. Neuroimage. 2005;26:243–250
  46. Van der Ven AHGS, Ellis JL. A Rasch analysis of Raven's standard progressive matrices. Pers. Indiv. Differ. 2000;29:45–64
  47. Van Honk J, Peper JS, Schutter DJLG. Testosterone reduces unconscious fear but not consciously experienced anxiety: implications for the disorders of fear and anxiety. Biol. Psychiatry. 2005;58:218–225
  48. Van Wingen GA, van Broekhoven F, Verkes RJ, Petersson KM, Bäckström T, Buitelaar JK, et al. Progesterone selectively increases amygdala reactivity in women. Mol. Psychiatry. 2007;13:325–333
  49. Van Wingen GA, van Broekhoven F, Verkes RJ, Petersson KM, Bäckström T, Buitelaar J, et al. How progesterone impairs memory for biologically salient stimuli in healthy young women. J. Neurosci. 2007;27:11416–11423
  50. Wang C, Alexander G, Berman N, Salehian B, Davidson T, McDonald V, et al. Testosterone replacement therapy improves mood in hypogonadal men–a clinical research center study. J. Clin. Endocrinol. Metab. 1996;81:3578–3583
  51. Williams CL. Estrogen effects on cognition across the lifespan. Horm. Behav. 1998;34:80–84
  52. Windischberger C, Friedreich S, Hoheisel B, Moser E. The impact of physiological artifact correction on individual and group results of fMRI of the amygdala. Neuroimage. 2006;31:S28
  53. Windischberger C, Langenberger H, Sycha T, Tschernko EM, Fuchsjäger-Mayerl G, Schmetterer L, et al. On the origin of respiratory artifacts in BOLD-EPI of the human brain. Magn. Reson. Imaging. 2002;20:575–582
  54. Wittchen HU, Zaudig M, Fydrich T. Strukturiertes Klinisches Interview für DSM-IV. Göttingen: Hogrefe; 1997;

PII: S0306-4530(08)00096-6

doi: 10.1016/j.psyneuen.2008.04.014

Psychoneuroendocrinology
Volume 33, Issue 8 , Pages 1031-1040 , September 2008

Article Tools

* Image Usage & Resolution