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Brain activation during emotion regulation in women with premenstrual dysphoric disorder

Published online by Cambridge University Press:  17 November 2017

Nicole Petersen ,
Dara G. Ghahremani ,
Andrea J. Rapkin ,
Steven M. Berman ,
Letty Liang  and
Edythe D. London
Nicole Petersen
Affiliation:
Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, Los Angeles, CA, 90024, USA
Dara G. Ghahremani
Affiliation:
Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, Los Angeles, CA, 90024, USA
Andrea J. Rapkin*
Affiliation:
Department of Obstetrics and Gynecology, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, 90024, USA
Steven M. Berman
Affiliation:
Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, Los Angeles, CA, 90024, USA
Letty Liang
Affiliation:
Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, Los Angeles, CA, 90024, USA
Edythe D. London
Affiliation:
Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, Los Angeles, CA, 90024, USA Department of Molecular and Medical Pharmacology, University of California Los Angeles, Los Angeles, CA, 90024, USA Brain Research Institute, David Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, 90024, USA
*
Address for correspondence: Andrea J. Rapkin, E-mail: arapkin@mednet.ucla.edu
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Abstract

Background

Difficulties in regulating emotions are linked to the core symptoms of premenstrual dysphoric disorder (PMDD). We therefore investigated the neural substrates of emotion-regulation problems in women with PMDD.

Methods

On the basis of self-evaluations over 2 months on the Daily Record of Severity of Problems, eligible participants were assigned to two groups: PMDD and control (18 per group). Functional magnetic resonance imaging (fMRI) and a well-validated task were used to assess brain function during emotion regulation. Participants were tested twice, once during the follicular (asymptomatic) and once in the late luteal (symptomatic) phase of the menstrual cycle.

Results

Women with PMDD gave higher ratings of negative affect in the luteal phase than in the follicular phase, and compared with healthy control participants during the luteal phase. A region-of-interest fMRI analysis indicated that during the late luteal phase, women with PMDD had hypoactivation in right dorsolateral prefrontal cortex (dlPFC) during all conditions of the emotion-regulation task, not only in the contrast that isolated emotion regulation. An exploratory whole-brain, voxel-wise analysis showed that women with PMDD had less activation in the precentral gyrus during the luteal phase than the follicular phase, and less activation in the postcentral gyrus compared with control participants.

Conclusions

During the luteal phase of the menstrual cycle, women with PMDD experience difficulty regulating emotions. Hypoactivation in the right dlPFC may contribute to this problem, but may be related more generally to other affective symptoms of PMDD. Hypofunction in the right pre- and postcentral gyri warrants additional study.

Keywords

Premenstrual dysphoric disorder; PMDDfMRIemotion regulationmenstrual cycleneuroendocrinology
Type
Original Articles
Information
Psychological Medicine , Volume 48 , Issue 11 , August 2018 , pp. 1795 - 1802
Copyright
Copyright © Cambridge University Press 2017 

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Footnotes

*

Both authors contributed equally to this work

References

Andersson, J, Jenkinson, M and Smith, S (2007) Non-linear registration, aka Spatial normalisation. FMRIB Technical Report.Google Scholar
American Psychiatric Association (2013). Diagnostic and Statistical Manual of Mental Disorders (5th ed.). Washington, DC: Author.Google Scholar
Baller, EB, Wei, SM, Kohn, PD, Rubinow, DR, Alarcon, G, Schmidt, PJ and Berman, KF (2013) Abnormalities of dorsolateral prefrontal function in women with premenstrual dysphoric disorder: a multimodal neuroimaging study. American Journal of Psychiatry 170, 305–314.Google Scholar
Banks, SJ, Eddy, KT, Angstadt, M, Nathan, PJ and Phan, KL (2007) Amygdala-frontal connectivity during emotion regulation. Social Cognitive Affective Neuroscience 2, 303–312.Google Scholar
Bannbers, E, Gingnell, M, Engman, J, Morell, A, Comasco, E, Kask, K, Garavan, H, Wikstrom, J and Sundstrom Poromaa, I (2012) The effect of premenstrual dysphoric disorder and menstrual cycle phase on brain activity during response inhibition. Journal of Affective Disorders 142, 347–350.Google Scholar
Berman, KF, Schmidt, PJ, Rubinow, DR, Danaceau, MA, Van Horn, JD, Esposito, G, Ostrem, JL and Weinberger, DR (1997) Modulation of cognition-specific cortical activity by gonadal steroids: a positron-emission tomography study in women. Proceedings of the National Academy of Sciences USA 94, 8836–8841.Google Scholar
Birtch, RL, Olatunbosun, OA and Pierson, RA (2006) Ovarian follicular dynamics during conventional vs. continuous oral contraceptive use. Contraception 73, 235–243.Google Scholar
Bloch, M, Schmidt, PJ and Rubinow, DR (1997) Premenstrual syndrome: evidence for symptom stability across cycles. American Journal of Psychiatry 154, 1741–1746.Google Scholar
Buhle, JT, Silvers, JA, Wager, TD, Lopez, R, Onyemekwu, C, Kober, H, Weber, J and Ochsner, KN (2014) Cognitive reappraisal of emotion: a meta-analysis of human neuroimaging studies. Cerebral Cortex 24, 2981–2990.Google Scholar
Cunningham-Bussel, AC, Root, JC, Butler, T, Tuescher, O, Pan, H, Epstein, J, Weisholtz, DS, Pavony, M, Silverman, ME, Goldstein, MS, Altemus, M, Cloitre, M, Ledoux, J, Mcewen, B, Stern, E and Silbersweig, D (2009) Diurnal cortisol amplitude and fronto-limbic activity in response to stressful stimuli. Psychoneuroendocrinology 34, 694–704.Google Scholar
Davis, AR, Kroll, R, Soltes, B, Zhang, N, Grubb, GS and Constantine, GD (2008) Occurrence of menses or pregnancy after cessation of a continuous oral contraceptive. Fertility and Sterility 89, 1059–1063.Google Scholar
Dickerson, LM, Mazyck, PJ and Hunter, MH (2003) Premenstrual syndrome. American Family Physician 67, 1743–1752.Google Scholar
Domes, G, Schulze, L, Bottger, M, Grossmann, A, Hauenstein, K, Wirtz, PH, Heinrichs, M and Herpertz, SC (2010) The neural correlates of sex differences in emotional reactivity and emotion regulation. Human Brain Mapping 31, 758–769.Google Scholar
Duijkers, I, Engels, L and Klipping, C (2005) Length of the menstrual cycle after discontinuation of oral contraceptives. Gynecological Endocrinology 20, 74–79.Google Scholar
Endicott, J, Nee, J and Harrison, W (2006) Daily record of severity of problems (DRSP): reliability and validity. Archives of Womens Mental Health 9, 41–49.Google Scholar
Epperson, CN, Steiner, M, Hartlage, SA, Eriksson, E, Schmidt, PJ, Jones, I and Yonkers, KA (2012) Premenstrual dysphoric disorder: evidence for a new category for DSM-5. American Journal of Psychiatry 169, 465–475.Google Scholar
Erk, S, Mikschl, A, Stier, S, Ciaramidaro, A, Gapp, V, Weber, B and Walter, H (2010) Acute and sustained effects of cognitive emotion regulation in major depression. Journal of Neuroscience 30, 15726–15734.Google Scholar
First, MB, Spitzer, RL, Gibbon, M and Williams, JBW (2002) Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Patient Edition. New York State: Psychiatric Institute.Google Scholar
Gingnell, M, Bannbers, E, Wikstrom, J, Fredrikson, M and Sundstrom-Poromaa, I (2013) Premenstrual dysphoric disorder and prefrontal reactivity during anticipation of emotional stimuli. European Journal of Neuropsychopharmacology 23, 1474–1483.Google Scholar
Gingnell, M, Morell, A, Bannbers, E, Wikstrom, J and Sundstrom Poromaa, I (2012) Menstrual cycle effects on amygdala reactivity to emotional stimulation in premenstrual dysphoric disorder. Hormones and Behavior 62, 400–406.Google Scholar
Goldin, PR, Mcrae, K, Ramel, W and Gross, JJ (2008) The neural bases of emotion regulation: reappraisal and suppression of negative emotion. Biological Psychiatry 63, 577–586.Google Scholar
Greicius, MD, Krasnow, B, Reiss, AL and Menon, V (2003) Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proceedings of the National Academy of Sciences USA 100, 253–258.Google Scholar
Halbreich, U, Borenstein, J, Pearlstein, T and Kahn, LS (2003) The prevalence, impairment, impact, and burden of premenstrual dysphoric disorder (PMS/PMDD). Psychoneuroendocrinology 28( suppl. 3), 1–23.Google Scholar
Hantsoo, L and Epperson, CN (2015) Premenstrual dysphoric disorder: epidemiology and treatment. Current Psychiatry Reports 17, 87.Google Scholar
Hong, JP, Park, S, Wang, HR, Chang, SM, Sohn, JH, Jeon, HJ, Lee, HW, Cho, SJ, Kim, BS, Bae, JN and Cho, MJ (2012) Prevalence, correlates, comorbidities, and suicidal tendencies of premenstrual dysphoric disorder in a nationwide sample of Korean women. Social Psychiatry and Psychiatric Epidemiology 47, 1937–1945.Google Scholar
Jenkinson, M and Smith, S (2001) A global optimisation method for robust affine registration of brain images. Medical Image Analysis 5, 143–156.Google Scholar
Johnstone, T, Van Reekum, CM, Urry, HL, Kalin, NH and Davidson, RJ (2007) Failure to regulate: counterproductive recruitment of top-down prefrontal-subcortical circuitry in major depression. Journal of Neuroscience 27, 8877–8884.Google Scholar
Koenigsberg, HW, Fan, J, Ochsner, KN, Liu, X, Guise, K, Pizzarello, S, Dorantes, C, Tecuta, L, Guerreri, S, Goodman, M, New, A, Flory, J and Siever, LJ (2010) Neural correlates of using distancing to regulate emotional responses to social situations. Neuropsychologia 48, 1813–1822.Google Scholar
Koenigsberg, HW, Fan, J, Ochsner, KN, Liu, X, Guise, KG, Pizzarello, S, Dorantes, C, Guerreri, S, Tecuta, L, Goodman, M, New, A and Siever, LJ (2009) Neural correlates of the use of psychological distancing to regulate responses to negative social cues: a study of patients with borderline personality disorder. Biological Psychiatry 66, 854–863.Google Scholar
Kohn, N, Eickhoff, SB, Scheller, M, Laird, AR, Fox, PT and Habel, U (2014) Neural network of cognitive emotion regulation – an ALE meta-analysis and MACM analysis. NeuroImage 87, 345–355.Google Scholar
Lang, PJ, Bradley, MM and Cuthbert, BN (2008) International affective picture system (IAPS): affective ratings of pictures and instruction manual. Technical Report.Google Scholar
Lopez, LM, Kaptein, AA and Helmerhorst, FM (2012) Oral contraceptives containing drospirenone for premenstrual syndrome. The Cochrane Database of Systematic Reviews 2, CD006586.Google Scholar
Mcrae, K, Misra, S, Prasad, AK, Pereira, SC and Gross, JJ (2012) Bottom-up and top-down emotion generation: implications for emotion regulation. Social Cognitive and Affective Neuroscience 7, 253–262.Google Scholar
Ochsner, KN and Gross, JJ (2005) The cognitive control of emotion. Trends in Cognitive Sciences 9, 242–249.Google Scholar
Ochsner, KN, Ray, RD, Cooper, JC, Robertson, ER, Chopra, S, Gabrieli, JD and Gross, JJ (2004) For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion. NeuroImage 23, 483–499.Google Scholar
Ochsner, KN, Silvers, JA and Buhle, JT (2012) Functional imaging studies of emotion regulation: a synthetic review and evolving model of the cognitive control of emotion. Annals of the New York Academy of Sciences 1251, E1–24.Google Scholar
Oldfield, RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97–113.Google Scholar
Petersen, N and Cahill, L (2015) Amygdala reactivity to negative stimuli is influenced by oral contraceptive use. Social Cognitive and Affective Neuroscience 10, 1266–1272.Google Scholar
Petersen, N, London, ED, Liang, L, Ghahremani, DG, Gerards, R, Goldman, L and Rapkin, AJ (2016) Emotion regulation in women with premenstrual dysphoric disorder. Archives of Women's Mental Health 19, 891–898.Google Scholar
Pilver, CE, Libby, DJ and Hoff, RA (2013) Premenstrual dysphoric disorder as a correlate of suicidal ideation, plans, and attempts among a nationally representative sample. Social Psychiatry and Psychiatric Epidemiology 48, 437–446.Google Scholar
Rapkin, AJ, Berman, SM, Mandelkern, MA, Silverman, DH, Morgan, M and London, ED (2011) Neuroimaging evidence of cerebellar involvement in premenstrual dysphoric disorder. Biological Psychiatry 69, 374–380.Google Scholar
Rapkin, AJ and Winer, SA (2009) Premenstrual syndrome and premenstrual dysphoric disorder: quality of life and burden of illness. Expert Rev Pharmacoeconomics & Outcomes Research 9, 157–170.Google Scholar
Reuveni, I, Dan, R, Segman, R, Evron, R, Laufer, S, Goelman, G, Bonne, O and Canetti, L (2016) Emotional regulation difficulties and premenstrual symptoms among Israeli students. Archives of Women's Mental Health 19, 1063–1070.Google Scholar
Ritchey, M, Dolcos, F, Eddington, KM, Strauman, TJ and Cabeza, R (2011) Neural correlates of emotional processing in depression: changes with cognitive behavioral therapy and predictors of treatment response. Journal of Psychiatric Research 45, 577–587.Google Scholar
Silvers, JA, Insel, C, Powers, A, Franz, P, Helion, C, Martin, RE, Weber, J, Mischel, W, Casey, BJ and Ochsner, KN (2016) vlPFC-vmPFC-amygdala interactions underlie age-related differences in cognitive regulation of emotion. Cerebral Cortex 27, 3502–3514.Google Scholar
Silvers, JA, Shu, J, Hubbard, AD, Weber, J and Ochsner, KN (2015) Concurrent and lasting effects of emotion regulation on amygdala response in adolescence and young adulthood. Developmental Science 18, 771–784.Google Scholar
Wager, TD, Davidson, ML, Hughes, BL, Lindquist, MA and Ochsner, KN (2008) Prefrontal-subcortical pathways mediating successful emotion regulation. Neuron 59, 1037–1050.Google Scholar
Wittchen, HU, Becker, E, Lieb, R and Krause, P (2002) Prevalence, incidence and stability of premenstrual dysphoric disorder in the community. Psychological Medicine 32, 119–132.Google Scholar
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