Identification of a narrow post-ovulatory window of vulnerability to distressing involuntary memories in healthy women
Open accessAbstract
Psychological disorders characterised by intrusive memories are more prevalent in women than men. The biological, social and cognitive processes underlying this gender-difference have yet to be fully elucidated. Some evidence suggests that (fluctuations in) ovarian hormone levels are responsible for altered sensitivity to emotional stimuli during certain phases in the menstrual-cycle and this may form the basis of a specific vulnerability to psychological disorders in women. The post-ovulatory (luteal) phase has been identified as a period of particular vulnerability to the development of post-traumatic stress disorder (PTSD). Using an experimental model of PTSD, we examine whether differences are detectable between discrete phases in the menstrual-cycle in the experience of intrusive memories. Women (18-35 years-old) in one of three tightly-defined periods within the menstrual cycle--mid-follicular (n=15), early-luteal (n=15) and late-luteal (n=11)--provided saliva samples for ovarian-hormone assay and watched a distressing film. Subsequent intrusive memories, assessed using a daily online-diary, occurred significantly more frequently in the early-luteal group compared to mid-follicular and late-luteal groups. Intrusion frequency was negatively correlated with the estradiol-to-progesterone ratio, but not estradiol or progesterone alone, suggesting that the interactive effect of low estradiol and high progesterone at encoding contributes to the observed effect. Our results support the need for further research in a clinical context with naturally-cycling women who experience a traumatic event, since assessment of days-since-last-menses and ovarian hormone levels may help to identify those at greatest risk of developing re-experiencing symptoms akin to those seen in psychological disorder such as depression and PTSD.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
(1970) · Cited by 24,983 · see citing works
Anxiety, sensitivity, anxiety frequency, and the prediction of fearfulness
Reiss, S., Peterson, R. A., Gursky, D. M., & McNally, R. J. (1986) · Behaviour Research and Therapy · doi:10.1016/0005-7967(86)90143-9 · Cited by 3,169 · see citing works
Longitudinal Effects of Aging on Serum Total and Free Testosterone Levels in Healthy Men
Harman, S. M., Metter, E. J., Tobin, J. D., Pearson, J., & Blackman, M. R. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.2.7219 · Cited by 2,760 · see citing works
Constructive and unconstructive repetitive thought
Watkins, E. R. (2008) · Psychological Bulletin · doi:10.1037/0033-2909.134.2.163 · Cited by 2,421 · see citing works
Kirschbaum, C., Kudielka, B. M., Gaab, J., Schommer, N. C., & Hellhammer, D. H. (1999) · Psychosomatic Medicine · doi:10.1097/00006842-199903000-00006 · Cited by 1,890 · see citing works
Sex differences in HPA axis responses to stress: a review
Kudielka, B. M., & Kirschbaum, C. (2005) · Biological Psychology · doi:10.1016/j.biopsycho.2004.11.009 · Cited by 1,624 · see citing works
Brewin, C. R., Gregory, J. D., Lipton, M., & Burgess, N. (2010) · Psychological Review · doi:10.1037/a0018113 · Cited by 1,226 · see citing works
Brave men and timid women? A review of the gender differences in fear and anxiety
McLean, C. P., & Anderson, E. R. (2009) · Clinical Psychology Review · doi:10.1016/j.cpr.2009.05.003 · Cited by 1,149 · see citing works
Progesterone receptors: form and function in brain
Brinton, R. D., Thompson, R. F., Foy, M. R., Baudry, M., Wang, J., Finch, C. E., Morgan, T. E., Pike, C. J., Mack, W. J., Stanczyk, F. Z., et al. (2008) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2008.02.001 · Cited by 675 · see citing works
Psychiatric Sequelae of Posttraumatic Stress Disorder in Women
Breslau, N. (1997) · Archives of General Psychiatry · doi:10.1001/archpsyc.1997.01830130087016 · Cited by 563 · see citing works
Prevalence, incidence and stability of premenstrual dysphoric disorder in the community
WITTCHEN, H.-U., BECKER, E., LIEB, R., & KRAUSE, P. (2002) · Psychological Medicine · doi:10.1017/s0033291701004925 · Cited by 554 · see citing works
Kendler, K. S., Thornton, L. M., & Prescott, C. A. (2001) · American Journal of Psychiatry · doi:10.1176/appi.ajp.158.4.587 · Cited by 520 · see citing works
Dalgleish, T. (2004) · Psychological Bulletin · doi:10.1037/0033-2909.130.2.228 · Cited by 498 · see citing works
Trauma films, information processing, and intrusive memory development
Holmes, E. A., Brewin, C. R., & Hennessy, R. G. (2004) · Journal of Experimental Psychology: General · doi:10.1037/0096-3445.133.1.3 · Cited by 457 · see citing works
Inducing and modulating intrusive emotional memories: A review of the trauma film paradigm
Holmes, E. A., & Bourne, C. (2008) · Acta Psychologica · doi:10.1016/j.actpsy.2007.11.002 · Cited by 410 · see citing works
Current Status of Salivary Hormone Analysis
Gröschl, M. (2008) · Clinical Chemistry · doi:10.1373/clinchem.2008.108910 · Cited by 370 · see citing works
Implicit memory varies across the menstrual cycle: estrogen effects in young women
Maki, P. M., Rich, J. B., & Rosenbaum, R. S. (2002) · Neuropsychologia · doi:10.1016/s0028-3932(01)00126-9 · Cited by 342 · see citing works
Lebrón‐Milad, K., & Milad, M. R. (2012) · Biology of Mood & Anxiety Disorders · doi:10.1186/2045-5380-2-3 · Cited by 298 · see citing works
Blockade of Estrogen by Hormonal Contraceptives Impairs Fear Extinction in Female Rats and Women
Graham, B. M., & Milad, M. R. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.09.018 · Cited by 281 · see citing works
Progesterone selectively increases amygdala reactivity in women
van Wingen, G. A., van Broekhoven, F., Verkes, R. J., Petersson, K. M., Bäckström, T., Buitelaar, J. K., & Fernández, G. (2008) · Molecular Psychiatry · doi:10.1038/sj.mp.4002030 · Cited by 273 · see citing works
Holmes, E. A., James, E. L., Kilford, E. J., & Deeprose, C. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013706 · Cited by 273 · see citing works
Estrogen receptors in the human forebrain and the relation to neuropsychiatric disorders
Österlund, M. K., & Hurd, Y. L. (2001) · Progress in Neurobiology · doi:10.1016/s0301-0082(00)00059-9 · Cited by 263 · see citing works
Estrogen Levels Are Associated with Extinction Deficits in Women with Posttraumatic Stress Disorder
Glover, E. M., Jovanović, T., Mercer, K. B., Kerley, K. A., Bradley, B., Ressler, K. J., & Norrholm, S. D. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.02.031 · Cited by 259 · see citing works
Ditlevsen, D. N., & Elklit, A. (2010) · Annals of General Psychiatry · doi:10.1186/1744-859x-9-32 · Cited by 204 · see citing works
Reynolds, M., & Brewin, C. R. (1998) · Behaviour Research and Therapy · doi:10.1016/s0005-7967(98)00013-8 · Cited by 177 · see citing works
Bäckström, T., Haage, D., Löfgren, M., Johansson, I. M., Strömberg, J., Nyberg, S., Andréen, L., Ossewaarde, L., van Wingen, G. A., Turkmen, S., et al. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.03.061 · Cited by 169 · see citing works
Menstrual cycle modulation of the relationship between cortisol and long-term memory
Andreano, J. M., Arjomandi, H., & Cahill, L. F. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.03.009 · Cited by 156 · see citing works
Beyond the HPA Axis: Progesterone-Derived Neuroactive Steroids in Human Stress and Emotion
Wirth, M. M. (2011) · Frontiers in Endocrinology · doi:10.3389/fendo.2011.00019 · Cited by 121 · see citing works
Patterns of Salivary Estradiol and Progesterone across the Menstrual Cycle
Gandara, B., LeResche, L., & Mancl, L. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1384.022 · Cited by 114 · see citing works
Ferree, N. K., Kamat, R., & Cahill, L. (2011) · Consciousness and Cognition · doi:10.1016/j.concog.2011.02.003 · Cited by 114 · see citing works
The association between menstrual cycle and traumatic memories
Bryant, R. A., Felmingham, K. L., Silove, D., Creamer, M., O'Donnell, M., & McFarlane, A. C. (2011) · Journal of Affective Disorders · doi:10.1016/j.jad.2010.10.049 · Cited by 105 · see citing works
Rab Proteins and the Secretory Pathway: The Case of Rab18 in Neuroendocrine Cells
Vázquez‐Martínez, R., & Malagón, M. M. (2011) · Frontiers in Endocrinology · doi:10.3389/fendo.2011.00001 · Cited by 98 · see citing works
Hormonal contraception usage is associated with altered memory for an emotional story
Nielsen, S. E., Ertman, N., Lakhani, Y. S., & Cahill, L. F. (2011) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2011.06.013 · Cited by 95 · see citing works
Ferree, N. K., & Cahill, L. (2009) · Consciousness and Cognition · doi:10.1016/j.concog.2008.11.008 · Cited by 94 · see citing works
Kornstein, S. G., Harvey, A. T., Rush, A. J., Wisniewski, S. R., Trivedi, M. H., Svikis, D. S., McKenzie, N., Bryan, C. J., & Harley, R. M. (2005) · Psychological Medicine · doi:10.1017/s0033291704004106 · Cited by 93 · see citing works
Nillni, Y., Toufexis, D., & Rohan, K. (2011) · Clinical Psychology Review · doi:10.1016/j.cpr.2011.07.006 · Cited by 87 · see citing works
Symptoms Related to the Menstrual Cycle: Diagnosis, Prevalence, and Treatment
Clayton, A. H. (2008) · Journal of Psychiatric Practice · doi:10.1097/01.pra.0000308491.54885.f8 · Cited by 81 · see citing works
Intrusive images and intrusive thoughts as different phenomena: Two experimental studies
Hagenaars, M. A., Brewin, C. R., van Minnen, A., Holmes, E. A., & Hoogduin, K. A. L. (2010) · Memory · doi:10.1080/09658210903476522 · Cited by 77 · see citing works
Bisby, J. A., King, J. A., Brewin, C. R., Burgess, N., & Curran, H. V. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.01.010 · Cited by 65 · see citing works
The Effects of Female Reproductive Hormones in Generalized Social Anxiety Disorder
van Veen, J. F., Jonker, B., van Vliet, I. V., & Zitman, F. G. (2009) · International Journal of Psychiatry in Medicine · doi:10.2190/pm.39.3.e · Cited by 57 · see citing works
Oestrogen, Cognition and the Maturing Female Brain
Craig, M., & Murphy, D. (2006) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2006.01500.x · Cited by 52 · see citing works
The premenstrual tension syndrome rating scales: An updated version
Steiner, M. S., Peer, M., Macdougall, M., & Haskett, R. F. (2011) · Journal of Affective Disorders · doi:10.1016/j.jad.2011.06.058 · Cited by 40 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Liu, N., Zhang, F., Wei, C., Jia, Y., Shang, Z., Sun, L., Wu, L., Sun, Z., Zhou, Y., Wang, Y., et al. (2020) · Psychiatry Research · doi:10.1016/j.psychres.2020.112921 · Cited by 1,548 · see citing works
Sex differences in anxiety and depression clinical perspectives
Altemus, M., Sarvaiya, N., & Neill Epperson, C. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.05.004 · Cited by 1,413 · see citing works
Li, S. H., & Graham, B. M. (2017) · The Lancet Psychiatry · doi:10.1016/s2215-0366(16)30358-3 · Cited by 579 · see citing works
Sundström Poromaa, I., & Gingnell, M. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00380 · Cited by 291 · see citing works
Iyadurai, L., Visser, R. M., Lau-Zhu, A., Porcheret, K., Horsch, A., Holmes, E. A., & James, E. L. (2019) · Clinical Psychology Review · doi:10.1016/j.cpr.2018.08.005 · Cited by 255 · see citing works
Psychiatric Symptoms Across the Menstrual Cycle in Adult Women: A Comprehensive Review
Handy, A. B., Greenfield, S. F., Yonkers, K. A., & Payne, L. A. (2022) · Harvard Review of Psychiatry · doi:10.1097/hrp.0000000000000329 · Cited by 153 · see citing works
Wegerer, M., Kerschbaum, H., Blechert, J., & Wilhelm, F. H. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.10.001 · Cited by 122 · see citing works
Menstrual cycle effects on psychological symptoms in women with PTSD
Nillni, Y. I., Pineles, S. L., Patton, S. C., Rouse, M. H., Sawyer, A. T., & Rasmusson, A. M. (2015) · Journal of Traumatic Stress · doi:10.1002/jts.21984 · Cited by 100 · see citing works
Das, R. K., Tamman, A., Nikolova, V., Freeman, T. P., Bisby, J. A., Lazzarino, A. I., & Kamboj, S. K. (2016) · Psychological Medicine · doi:10.1017/s003329171600026x · Cited by 49 · see citing works
Self-citation
- Authors
- Soni, M., Curran, V. H., & Kamboj, S. K.
- Affiliations
- University College London (GB)
- Corresponding author
- Kamboj, Sunjeev K.
- Venue
- Neurobiology of Learning and Memory
- Publisher
- Elsevier BV
- Published
- 2013-09
- Volume
- 104
- Pages
- 32-38
- ISSN
- 1074-7427 (ISSN-L)
- OpenAlex
- W2078412093
- Cited by
- 102
- References
- 42
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 10 · 2023: 6 · 2022: 18 · 2021: 19 · 2020: 14 · 2019: 7 · 2018: 8 · 2017: 1 · 2016: 4 · 2015: 3 · 2014: 6 · 2013: 1
- FWCI
- 5.19
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Neurobiology of Learning and Memory (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Research Bank (Australian Catholic University) (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Topics
- Social Sciences › Psychology › Clinical Psychology › Posttraumatic Stress Disorder Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Social Sciences › Psychology › Developmental and Educational Psychology › Identity, Memory, and Therapy
- Keywords
- menstrual cycle, luteal phase, ovarian hormones, estradiol, progesterone, estradiol/progesterone ratio, intrusive memories, post-traumatic stress disorder, gender differences, women's mental health, re-experiencing symptoms, depression
- MeSH terms
- Adolescent, Adult, Affect, Anxiety, Estradiol, Female, Humans, Memory, Menstrual Cycle, Progesterone, Time Factors, Young Adult
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
