Neuroimaging the menstrual cycle: A multimodal systematic review

Dubol, Manon; Epperson, C. Neill; Sacher, Julia; Pletzer, Belinda; Derntl, Birgit; Lanzenberger, Rupert; Sundström‐Poromaa, Inger; Comasco, Erika

doi:10.1016/j.yfrne.2020.100878

Cited by 103 publications

(106 citation statements)

References 126 publications

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“…Lastly, there are very recent systematic reviews on the brain sites responding to naturally fluctuating sex hormones during the female menstrual cycle ( Dubol et al, 2021 ) and under contraceptive use ( Brønnick et al, 2020 ). It is now time to relate the identified action sites to specific areas of emotional processing such as emotion recognition and emotional memory.…”

Section: Discussionmentioning

confidence: 99%

Facial Emotion Recognition and Emotional Memory From the Ovarian-Hormone Perspective: A Systematic Review

2021

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BackgroundWe review original papers on ovarian-hormone status in two areas of emotional processing: facial emotion recognition and emotional memory. Ovarian-hormone status is operationalized by the levels of the steroid sex hormones 17β-estradiol (E2) and progesterone (P4), fluctuating over the natural menstrual cycle and suppressed under oral contraceptive (OCs) use. We extend previous reviews addressing single areas of emotional processing. Moreover, we systematically examine the role of stimulus features such as emotion type or stimulus valence and aim at elucidating factors that reconcile the inconsistent results.MethodsWe followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines and included papers published until September 2020 indexed in PubMed and Web of Science databases. Search terms were MeSH terms (emotional OR emotion) AND (X) AND (estrogen OR progesterone OR menstrual cycle OR oral contraceptives) with (X) representing our separately searched areas, resulting in (processing OR recognition OR empathy), and (memory OR recall). To be included, articles had to (1) be written and published in English, (2) examine healthy, non-pregnant adult women in their reproductive age, and (3) measure or at least estimate levels of E2 and P4. In PubMed, the search was (4) limited to humans and (5) to the search term present in the title or abstract.ResultsFeatures of the provided stimulus material (emotion type and/or valence) constitute a relevant influence that interacts with E2- and P4-related ovarian-hormone status. For instance, recognition of basic emotions appears to be more related to P4- than E2-levels. Quite consistent, OC intake (vs. natural menstrual cycling) was accompanied by impaired recognition accuracy of basic and also complex emotions, although not in a recent large-sample study assessing complex emotions. Memory recall of negative content was mainly enhanced by P4, especially after having been stressed.Discussion and ConclusionWe document the methodological diversity in the field, presumably contributing to the heterogeneity of results. More studies explicitly contrasting the early follicular phase, mid-cycle phase, mid-luteal, and OC intake while standardizing tasks are needed. Research would take advantage of using within-subject designs and accounting for the recognition of complex emotions.

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Section: Discussionmentioning

confidence: 99%

Facial Emotion Recognition and Emotional Memory From the Ovarian-Hormone Perspective: A Systematic Review

2021

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“…Previous work in a developmental cohort has shown males exhibit stronger inter-network connectivity, while females exhibit stronger intra-network connectivity (Satterthwaite et al, 2015). Extant literature also suggests hormonal modulation of functional connectivity (Dubol et al, 2020; Fitzgerald, Pritschet, Santander, Grafton, & Jacobs, 2020; Hjelmervik, Hausmann, Osnes, Westerhausen, & Specht, 2014; Pritschet et al, 2020; Weis, Hodgetts, et al, 2019). In terms of functional connectivity features that discriminate sex, two studies identified that connections within and between frontoparietal and default mode networks strongly contribute to the predictions (Weis, Patil, et al, 2019; Zhang et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Shared functional connections within and between cortical networks predict cognitive abilities in adult males and females

Dhamala

Jamison

Jaywant

et al. 2021

Preprint

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A thorough understanding of sex-independent and sex-specific neurobiological features that underlie cognitive abilities in healthy individuals is essential for the study of neurological illnesses in which males and females differentially experience and exhibit cognitive impairment. Here, we evaluate sex-independent and sex-specific relationships between functional connectivity and individual cognitive abilities in 392 healthy young adults (196 males) from the Human Connectome Project. First, we establish that sex-independent models comparably predict crystallised abilities in males and females, but more accurately predict fluid abilities in males. Second, we demonstrate sex-specific models comparably predict crystallised abilities within and between sexes, and generally fail to predict fluid abilities in either sex. Third, we reveal that largely overlapping connections between visual, dorsal attention, ventral attention, and default mode networks are associated with better performance on crystallised and fluid cognitive tests in males and females, while connections within visual, somatomotor, and default mode networks are associated with poorer performance. Together, our findings suggest that shared neurobiological features of the functional connectome underlie crystallised and fluid abilities across the sexes.

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“…Indeed, recent studies have demonstrated that the sex hormones estrogen and progesterone differentially influence the density of steroid hormone receptors across the brain throughout the menstrual cycle [45]. Moreover, this view aligns with the nonlinear and nonstationary contribution of luteinizing hormone to hormone dynamics across the menstrual cycle; large surges in LH near ovulation disrupt the phasic coupling of sex steroid and gonadotropic hormones [41], suggesting that structural changes caused by acute changes in hormone concentration, such as receptor density, influence network connectivity in addition to the direct effects of hormones on cells. Sex hormones are intrinsically involved in micro-level structural changes as well, given that estrogen-and progesterone-mediated changes in subcortical receptor density induce the release of gonadotropin-releasing hormone to induce luteinizing hormone spike [46].…”

Section: Discussionmentioning

confidence: 83%

“…While this observation is in line with previous studies that have reported links between reproductive hormones and both brain activity [21,22] and functional connectivity [23,26,[34][35][36][37][38][39][40], our results extend this link to ultrafast network dynamics. Changes in network structure at this timescale have been relatively unexplored in previous studies due to their cross-sectional study design and low temporal resolution of sliding-window methods for estimating time-varying functional connectivity [41] (although, see [24]).…”

Section: Discussionmentioning

confidence: 99%

High-amplitude network co-fluctuations linked to variation in hormone concentrations over menstrual cycle

Greenwell

Faskowitz

Pritschet

et al. 2021

Preprint

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Many studies have shown that the human endocrine system modulates brain function, reporting associations between fluctuations in hormone concentrations and both brain activity and connectivity. However, how hormonal fluctuations impact fast changes in brain network structure over short timescales remains unknown. Here, we leverage ``edge time series'' analysis to investigate the relationship between high-amplitude network states and quotidian variation in sex steroid and gonadotropic hormones in a single individual sampled over the course of two endocrine states, across a natural menstrual cycle and under a hormonal regimen. We find that the frequency of high-amplitude network states are associated with follicle-stimulating and luteinizing hormone, but not the sex hormones estradiol and progesterone. Nevertheless, we show that scan-to-scan variation in the co-fluctuation patterns expressed during network states are robustly linked with the concentration of all four hormones, positing a network-level target of hormonal control. We conclude by speculating on the role of hormones in shaping ongoing brain dynamics.

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Neuroimaging the menstrual cycle: A multimodal systematic review

Cited by 103 publications

References 126 publications

Facial Emotion Recognition and Emotional Memory From the Ovarian-Hormone Perspective: A Systematic Review

Facial Emotion Recognition and Emotional Memory From the Ovarian-Hormone Perspective: A Systematic Review

Shared functional connections within and between cortical networks predict cognitive abilities in adult males and females

High-amplitude network co-fluctuations linked to variation in hormone concentrations over menstrual cycle

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