Brain reactivity during aggressive response in women with premenstrual dysphoric disorder treated with a selective progesterone receptor modulator.
Journal
Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology
ISSN: 1740-634X
Titre abrégé: Neuropsychopharmacology
Pays: England
ID NLM: 8904907
Informations de publication
Date de publication:
07 2021
07 2021
Historique:
received:
27
11
2020
accepted:
01
04
2021
revised:
17
02
2021
pubmed:
1
5
2021
medline:
29
6
2021
entrez:
30
4
2021
Statut:
ppublish
Résumé
Premenstrual dysphoric disorder (PMDD) is a psychiatric condition characterized by late luteal phase affective, cognitive, and physical impairment. The disorder causes significant suffering in about 5% of women in their reproductive age. Altered sensitivity of cognitive-affective brain circuits to progesterone and its downstream metabolite allopregnanolone is suggested to underlie PMDD symptomatology. Core mood symptoms include irritability and anger, with aggression being the behavioral outcome of these symptoms. The present study sought to investigate the neural correlates of reactive aggression during the premenstrual phase in women with PMDD, randomized to a selective progesterone receptor modulator (SPRM) or placebo. Self-reports on the Daily Record of Severity of Problems were used to assess PMDD symptoms and gonadal hormone levels were measured by liquid chromatography tandem mass spectrometry. Functional magnetic resonance imaging was performed in 30 women with PMDD, while performing the point subtraction aggression paradigm. Overall, a high SPRM treatment response rate was attained (93%), in comparison with placebo (53.3%). Women with PMDD randomized to SPRM treatment had enhanced brain reactivity in the dorsal anterior cingulate cortex and dorsomedial prefrontal cortex during the aggressive response condition. The fronto-cingulate reactivity during aggressive responses depended on treatment, with a negative relationship between brain reactivity and task-related aggressiveness found in the placebo but not the SPRM group. The findings contribute to define the role of progesterone in PMDD symptomatology, suggesting a beneficial effect of progesterone receptor antagonism, and consequent anovulation, on top-down emotion regulation, i.e., greater fronto-cingulate activity in response to provocation stimuli.
Identifiants
pubmed: 33927343
doi: 10.1038/s41386-021-01010-9
pii: 10.1038/s41386-021-01010-9
pmc: PMC8209206
doi:
Substances chimiques
Receptors, Progesterone
0
Progesterone
4G7DS2Q64Y
Pregnanolone
BXO86P3XXW
Types de publication
Journal Article
Randomized Controlled Trial
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1460-1467Références
Rapkin AJ, Winer SA. Premenstrual syndrome and premenstrual dysphoric disorder: quality of life and burden of illness. Expert Rev Pharmacoecon Outcomes Res. 2009;9:157–70.
pubmed: 19402804
doi: 10.1586/erp.09.14
Ko C-H, Long C-Y, Chen S-YCI-J, Huang T-H, Yen J-Y. Depression, Irritability, and Anxiety in Women with Premenstrual Dysphoric Disorder. Int J Psychiatry Med. 2013;46:39–55.
pubmed: 24547609
doi: 10.2190/PM.46.1.d
Dawson DN, Eisenlohr-Moul TA, Paulson JL, Peters JR, Rubinow DR, Girdler SS. Emotion-related impulsivity and rumination predict the perimenstrual severity and trajectory of symptoms in women with a menstrually related mood disorder. J Clin Psychol. 2018;74:579–93.
pubmed: 28898408
doi: 10.1002/jclp.22522
Gingnell M, Comasco E, Oreland L, Fredrikson M, Sundström-Poromaa I. Neuroticism-related personality traits are related to symptom severity in patients with premenstrual dysphoric disorder and to the serotonin transporter gene-linked polymorphism 5-HTTPLPR. Arch Women’s Ment Health. 2010;13:417–23.
doi: 10.1007/s00737-010-0164-4
Adewuya AO, Loto OM, Adewumi TA. Pattern and correlates of premenstrual symptomatology amongst Nigerian University students. J Psychosom Obstet Gynecol. 2009;30:127–32.
doi: 10.1080/01674820802545446
Anderson CA, Bushman BJ. Human aggression. Annu Rev Psychol. 2002;53:27–51.
McCloskey MS, New AS, Siever LJ, Goodman M, Koenigsberg HW, Flory JD, et al. Evaluation of behavioral impulsivity and aggression tasks as endophenotypes for borderline personality disorder. J Psychiatr Res. 2009;43:1036–48.
pubmed: 19232640
pmcid: 2853811
doi: 10.1016/j.jpsychires.2009.01.002
Coccaro EF. Intermittent Explosive Disorder as a Disorder of Impulsive Aggression for DSM-5. Am J Psychiatry. 2012;169:577–88.
pubmed: 22535310
doi: 10.1176/appi.ajp.2012.11081259
Yager J. Irritability Disorders in Adults: Diagnostic Categories Missing in Plain Sight? J Nerv Ment Dis. 2020;208:459–65.
pubmed: 32187127
doi: 10.1097/NMD.0000000000001158
Epperson CN, Steiner M, Hartlage SA, Eriksson E, Schmidt PJ, Jones I, et al. Premenstrual dysphoric disorder: evidence for a new category for DSM-5. Am J Psychiatry. 2012;169:465–75.
pubmed: 22764360
pmcid: 3462360
doi: 10.1176/appi.ajp.2012.11081302
Bäckström T, Andreen L, Birzniece V, Björn I, Johansson I-M, Nordenstam-Haghjo M, et al. The role of hormones and hormonal treatments in premenstrual syndrome. CNS Drugs. 2003;17:325–42.
pubmed: 12665391
doi: 10.2165/00023210-200317050-00003
Sundström-Poromaa I, Comasco E, Sumner R, Luders E. Progesterone - Friend or foe? Front Neuroendocrinol. 2020;59:100856.
pubmed: 32730861
doi: 10.1016/j.yfrne.2020.100856
Bäckström T, Bixo M, Johansson M, Nyberg S, Ossewaarde L, Ragagnin G, et al. Allopregnanolone and mood disorders. Prog Neurobiol. 2014;113:88–94.
pubmed: 23978486
doi: 10.1016/j.pneurobio.2013.07.005
Geniole SN, MacDonell ET, McCormick CM. The Point Subtraction Aggression Paradigm as a laboratory tool for investigating the neuroendocrinology of aggression and competition. Hormones Behav. 2017;92:103–16.
doi: 10.1016/j.yhbeh.2016.04.006
Peters JR, Owens SA, Schmalenberger KM, Eisenlohr-Moul TA. Differential effects of the menstrual cycle on reactive and proactive aggression in borderline personality disorder. Aggress Behav. 2020;46:151–61.
pubmed: 31957896
pmcid: 7458153
doi: 10.1002/ab.21877
Petersen N, London ED, Liang L, Ghahremani DG, Gerards R, Goldman L, et al. Emotion regulation in women with premenstrual dysphoric disorder. Arch Women’s Ment Health. 2016;19:891–98.
doi: 10.1007/s00737-016-0634-4
Epperson CN, Haga K, Mason GF, Sellers E, Gueorguieva R, Zhang W, et al. Cortical γ-aminobutyric acid levels across the menstrual cycle in healthy women and those with premenstrual dysphoric disorder: a proton magnetic resonance spectroscopy study. Arch Gen Psychiatry. 2002;59:851–58.
pubmed: 12215085
doi: 10.1001/archpsyc.59.9.851
Liu B, Wang G, Gao D, Gao F, Zhao B, Qiao M, et al. Alterations of GABA and glutamate–glutamine levels in premenstrual dysphoric disorder: a 3T proton magnetic resonance spectroscopy study. Psychiatry Res: Neuroimaging. 2015;231:64–70.
pubmed: 25465316
doi: 10.1016/j.pscychresns.2014.10.020
Bixo M, Ekberg K, Poromaa IS, Hirschberg AL, Jonasson AF, Andréen L, et al. Treatment of premenstrual dysphoric disorder with the GABAA receptor modulating steroid antagonist Sepranolone (UC1010)—A randomized controlled trial. Psychoneuroendocrinology. 2017;80:46–55.
pubmed: 28319848
doi: 10.1016/j.psyneuen.2017.02.031
Martinez PE, Rubinow DR, Nieman LK, Koziol DE, Morrow AL, Schiller CE, et al. 5α-Reductase Inhibition Prevents the Luteal Phase Increase in Plasma Allopregnanolone Levels and Mitigates Symptoms in Women with Premenstrual Dysphoric Disorder. Neuropsychopharmacology. 2016;41:1093–102.
pubmed: 26272051
doi: 10.1038/npp.2015.246
Smith SS, Gong QH, Li X, Moran MH, Bitran D, Frye CA, et al. Withdrawal from 3alpha-OH-5alpha-pregnan-20-One using a pseudopregnancy model alters the kinetics of hippocampal GABAA-gated current and increases the GABAA receptor alpha4 subunit in association with increased anxiety. J Neurosci. 1998;18:5275–84.
pubmed: 9651210
pmcid: 6793484
doi: 10.1523/JNEUROSCI.18-14-05275.1998
Smith SS, Gong QH, Hsu F-C, Markowitz RS, Li X. GABA A receptor α4 subunit suppression prevents withdrawal properties of an endogenous steroid. Nature. 1998;392:926–29.
pubmed: 9582073
doi: 10.1038/31948
Gulinello M, Gong QH, Li X, Smith SS. Short-term exposure to a neuroactive steroid increases α4 GABAA receptor subunit levels in association with increased anxiety in the female rat. Brain Res. 2001;910:55–66.
pubmed: 11489254
pmcid: 4170586
doi: 10.1016/S0006-8993(01)02565-3
Nallasamy S, Kim J, Sitruk-Ware R, Bagchi M, Bagchi I. Ulipristal Blocks Ovulation by Inhibiting Progesterone Receptor—Dependent Pathways Intrinsic to the Ovary. Reprod Sci. 2013;20:371–81.
pubmed: 23012316
pmcid: 3676258
doi: 10.1177/1933719112459239
Esber N, Le Billan F, Resche-Rigon M, Loosfelt H, Lombès M, Chabbert-Buffet N. Ulipristal Acetate Inhibits Progesterone Receptor Isoform A-Mediated Human Breast Cancer Proliferation and BCl2-L1 Expression. PLOS ONE. 2015;10:e0140795.
pubmed: 26474308
pmcid: 4608808
doi: 10.1371/journal.pone.0140795
Rosato E, Farris M, Bastianelli C. Mechanism of Action of Ulipristal Acetate for Emergency Contraception: a Systematic Review. Front Pharm. 2016;6:315–15.
doi: 10.3389/fphar.2015.00315
Comasco E, Kallner HK, Bixo, M, Hirschberg, AL, Nyback, S, de Grauw, H, et al. Ulipristal acetate for treatment of premenstrual dysphoric disorder – a proof-of-concept randomized controlled trial. Am J Psychiatry. 2021;178:256–65.
Whitaker LH, Williams AR, Critchley HO. Selective progesterone receptor modulators. Curr Opin Obstet Gynecol. 2014;26:237–42.
pubmed: 24950125
doi: 10.1097/GCO.0000000000000082
Brinton RD, Thompson RF, Foy MR, Baudry M, Wang J, Finch CE, et al. Progesterone receptors: form and function in brain. Front Neuroendocrinol. 2008;29:313–39.
pubmed: 18374402
pmcid: 2398769
doi: 10.1016/j.yfrne.2008.02.001
Barth C, Villringer A, Sacher J. Sex hormones affect neurotransmitters and shape the adult female brain during hormonal transition periods. Front Neurosci. 2015;9:37.
Witte AV, Savli M, Holik A, Kasper S, Lanzenberger R. Regional sex differences in grey matter volume are associated with sex hormones in the young adult human brain. NeuroImage. 2010;49:1205–12.
pubmed: 19796695
doi: 10.1016/j.neuroimage.2009.09.046
Berkowitz L. Aggression: Its causes, consequences, and control. Mcgraw-Hill Book Company; New York, NY, England; 1993.
Coccaro EF, McCloskey MS, Fitzgerald DA, Phan KL. Amygdala and orbitofrontal reactivity to social threat in individuals with impulsive aggression. Biol Psychiatry. 2007;62:168–78.
pubmed: 17210136
doi: 10.1016/j.biopsych.2006.08.024
Gan G, Preston-Campbell RN, Moeller SJ, Steinberg JL, Lane SD, Maloney T, et al. Reward vs. retaliation—The role of the mesocorticolimbic salience network in human reactive aggression. Front Behav Neurosci. 2016;10:179.
pubmed: 27729852
pmcid: 5037197
doi: 10.3389/fnbeh.2016.00179
Kose S, Steinberg JL, Moeller FG, Gowin JL, Zuniga E, Kamdar ZN, et al. Neural correlates of impulsive aggressive behavior in subjects with a history of alcohol dependence. Behav Neurosci. 2015;129:183.
pubmed: 25664566
pmcid: 4777896
doi: 10.1037/bne0000038
Siever LJ. Neurobiology of aggression and violence. Am J Psychiatry. 2008;165:429–42.
pubmed: 18346997
pmcid: 4176893
doi: 10.1176/appi.ajp.2008.07111774
Skibsted AP, Cunha‐Bang SD, Carré JM, Hansen AE, Beliveau V, Knudsen GM, et al. Aggression‐related brain function assessed with the Point Subtraction Aggression Paradigm in fMRI. Aggressive Behav. 2017;43:601–10.
doi: 10.1002/ab.21718
Dubol M, Epperson CN, Lanzenberger R, Sundström-Poromaa I, Comasco E. Neuroimaging premenstrual dysphoric disorder: a systematic and critical review. Front Neuroendocrinol. 2020;57:100838.
Gingnell M, Ahlstedt V, Bannbers E, Wikström J, Sundström-Poromaa I, Fredrikson M. Social stimulation and corticolimbic reactivity in premenstrual dysphoric disorder: a preliminary study. Biol Mood Anxiety Disord. 2014;4:3.
pubmed: 24572042
pmcid: 4015856
doi: 10.1186/2045-5380-4-3
Gingnell M, Bannbers E, Wikström J, Fredrikson M, Sundström-Poromaa I. Premenstrual dysphoric disorder and prefrontal reactivity during anticipation of emotional stimuli. Eur Neuropsychopharmacol. 2013;23:1474–83.
pubmed: 24001875
doi: 10.1016/j.euroneuro.2013.08.002
Denson TF, O’Dean SM, Blake KR, Beames JR. Aggression in women: behavior, brain and hormones. Front Behav Neurosci. 2018;12:81.
pubmed: 29770113
pmcid: 5942158
doi: 10.3389/fnbeh.2018.00081
Sheehan DV, Lecrubier Y, Sheehan KH, Amorim P, Janavs J, Weiller E, et al. The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry. 1998;59:22–33. Suppl 20quiz 34-57
pubmed: 9881538
Endicott J, Nee J, Harrison W. Daily Record of Severity of Problems (DRSP): reliability and validity. Arch Women’s Ment Health. 2006;9:41–49.
doi: 10.1007/s00737-005-0103-y
Gustavsson JP, Bergman H, Edman G, Ekselius L, Von Knorring L, Linder J. Swedish universities Scales of Personality (SSP): construction, internal consistency and normative data. Acta Psychiatr Scandinavica. 2000;102:217–25.
doi: 10.1034/j.1600-0447.2000.102003217.x
Prochazka H, Agren H. Aggression in the general Swedish population, measured with a new self-rating inventory: the Aggression Questionnaire-revised Swedish version (AQ-RSV). Nord J Psychiatry. 2001;55:17–23.
pubmed: 11827602
doi: 10.1080/080394801750093661
Eklund A, Nichols TE, Knutsson H. Cluster failure: why fMRI inferences for spatial extent have inflated false-positive rates. Proc Natl Acad Sci. 2016;113:7900.
pubmed: 27357684
doi: 10.1073/pnas.1602413113
Friston K, Buechel C, Fink G, Morris J, Rolls E, Dolan RJ. Psychophysiological and modulatory interactions in neuroimaging. Neuroimage. 1997;6:218–29.
pubmed: 9344826
doi: 10.1006/nimg.1997.0291
Gitelman DR, Penny WD, Ashburner J, Friston KJ. Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution. NeuroImage. 2003;19:200–07.
pubmed: 12781739
doi: 10.1016/S1053-8119(03)00058-2
Leibenluft E. Pediatric Irritability: a Systems Neuroscience Approach. Trends Cogn Sci. 2017;21:277–89.
pubmed: 28274677
pmcid: 5366079
doi: 10.1016/j.tics.2017.02.002
Caprara GV, Cinanni V, D’imperio G, Passerini S, Renzi P, Travaglia G. Indicators of impulsive aggression: present status of research on irritability and emotional susceptibility scales. Personal Individ Differ. 1985;6:665–74.
doi: 10.1016/0191-8869(85)90077-7
Toffoletto S, Lanzenberger R, Gingnell M, Sundström-Poromaa I, Comasco E. Emotional and cognitive functional imaging of estrogen and progesterone effects in the female human brain: a systematic review. Psychoneuroendocrinology. 2014;50:28–52.
pubmed: 25222701
doi: 10.1016/j.psyneuen.2014.07.025
Schiller CE, Johnson SL, Abate AC, Schmidt PJ, Rubinow DR. Reproductive steroid regulation of mood and behavior. Compr Physiol. 2011;6:1135–60.
Comasco E, Hahn A, Ganger S, Gingnell M, Bannbers E, Oreland L, et al. Emotional fronto-cingulate cortex activation and brain derived neurotrophic factor polymorphism in premenstrual dysphoric disorder. Hum Brain Mapp. 2014;35:4450–58.
pubmed: 24615932
pmcid: 4107029
doi: 10.1002/hbm.22486
Etkin A, Egner T, Kalisch R. Emotional processing in anterior cingulate and medial prefrontal cortex. Trends Cogn Sci. 2011;15:85–93.
pubmed: 21167765
doi: 10.1016/j.tics.2010.11.004
Krämer UM, Jansma H, Tempelmann C, Münte TF. Tit-for-tat: the neural basis of reactive aggression. Neuroimage. 2007;38:203–11.
pubmed: 17765572
doi: 10.1016/j.neuroimage.2007.07.029
Botvinick MM, Cohen JD, Carter CS. Conflict monitoring and anterior cingulate cortex: an update. Trends Cogn Sci. 2004;8:539–46.
pubmed: 15556023
doi: 10.1016/j.tics.2004.10.003
Etkin A, Egner T, Peraza DM, Kandel ER, Hirsch J. Resolving emotional conflict: a role for the rostral anterior cingulate cortex in modulating activity in the amygdala. Neuron. 2006;51:871–82.
pubmed: 16982430
doi: 10.1016/j.neuron.2006.07.029
Amin Z, Epperson CN, Constable RT, Canli T. Effects of estrogen variation on neural correlates of emotional response inhibition. NeuroImage. 2006;32:457–64.
pubmed: 16644236
doi: 10.1016/j.neuroimage.2006.03.013
Prochazka H, Agren H. Self-rated aggression and cerebral monoaminergic turnover. Sex differences in patients with persistent depressive disorder. Eur Arch Psychiatry Clin Neurosci. 2003;253:185–92.
pubmed: 12910349
doi: 10.1007/s00406-003-0423-8
Etkin A, Büchel C, Gross JJ. The neural bases of emotion regulation. Nat Rev Neurosci. 2015;16:693–700.
pubmed: 26481098
doi: 10.1038/nrn4044
Pan J, Zhan L, Hu C, Yang J, Wang C, Gu L, et al. Emotion Regulation and Complex Brain Networks: association Between Expressive Suppression and Efficiency in the Fronto-Parietal Network and Default-Mode Network. Front Hum Neurosci. 2018;12:70–70.
pubmed: 29662443
pmcid: 5890121
doi: 10.3389/fnhum.2018.00070
Repple J, Pawliczek CM, Voss B, Siegel S, Schneider F, Kohn N, et al. From provocation to aggression: the neural network. BMC Neurosci. 2017;18:73.
pubmed: 29041906
pmcid: 5646154
doi: 10.1186/s12868-017-0390-z
da Cunha-Bang S, Fisher PM, Hjordt LV, Perfalk E, Persson Skibsted A, Bock C, et al. Violent offenders respond to provocations with high amygdala and striatal reactivity. Social Cognitive and Affective Neuroscience. 2017;12:802-10.
Schmidt PJ, Nieman LK, Danaceau MA, Adams LF, Rubinow DR. Differential behavioral effects of gonadal steroids in women with and in those without premenstrual syndrome. N Engl J Med. 1998;338:209–16.
pubmed: 9435325
doi: 10.1056/NEJM199801223380401
Schmidt PJ, Martinez PE, Nieman LK, Koziol DE, Thompson KD, Schenkel L, et al. Premenstrual dysphoric disorder symptoms following ovarian suppression: triggered by change in ovarian steroid levels but not continuous stable levels. Am J Psychiatry. 2017;174:980–89.
pubmed: 28427285
pmcid: 5624833
doi: 10.1176/appi.ajp.2017.16101113
Middelkoop M-A, Huirne JAF, van der Weide MCJ, Bosmans JE, Hehenkamp WJK. A multi-centre, randomized, non-inferiority trial to compare ulipristal with standard surgical treatment in women with symptomatic uterine fibroids: protocol of the MYOMEX-2 trial. Eur J Obstet Gynecol Reprod Biol. 2021;256:63–69.
pubmed: 33171419
doi: 10.1016/j.ejogrb.2020.10.058
Rabe T, Saenger N, Ebert AD, Roemer T, Tinneberg H-R, De Wilde RL, et al. Selective Progesterone Receptor Modulators for the Medical Treatment of Uterine Fibroids with a Focus on Ulipristal Acetate. BioMed Res Int. 2018;2018:1374821–21.
pubmed: 30539001
pmcid: 6261240
Möller C, Bone W, Cleve A, Klar U, Rotgeri A, Rottmann A, et al. Discovery of vilaprisan (BAY 1002670): a highly potent and selective progesterone receptor modulator optimized for gynecologic therapies. ChemMedChem. 2018;13:2271–80.
pubmed: 30407750
pmcid: 6282584
doi: 10.1002/cmdc.201800487