Abstract

The menstrual cycle (MC) is a sex hormone‐related phenomenon that repeats itself cyclically during the woman's reproductive life. In this explorative study, we hypothesized that coordinated variations of multiple sex hormones may affect the large‐scale organization of the brain functional network and that, in turn, such changes might have psychological correlates, even in the absence of overt clinical signs of anxiety and/or depression. To test our hypothesis, we investigated longitudinally, across the MC, the relationship between the sex hormones and both brain network and psychological changes. We enrolled 24 naturally cycling women and, at the early‐follicular, peri‐ovulatory, and mid‐luteal phases of the MC, we performed: (a) sex hormone dosage, (b) magnetoencephalography recording to study the brain network topology, and (c) psychological questionnaires to quantify anxiety, depression, self‐esteem, and well‐being. We showed that during the peri‐ovulatory phase, in the alpha band, the leaf fraction and the tree hierarchy of the brain network were reduced, while the betweenness centrality (BC) of the right posterior cingulate gyrus (rPCG) was increased. Furthermore, the increase in BC was predicted by estradiol levels. Moreover, during the luteal phase, the variation of estradiol correlated positively with the variations of both the topological change and environmental mastery dimension of the well‐being test, which, in turn, was related to the increase in the BC of rPCG. Our results highlight the effects of sex hormones on the large‐scale brain network organization as well as on their possible relationship with the psychological state across the MC. Moreover, the fact that physiological changes in the brain topology occur throughout the MC has widespread implications for neuroimaging studies.

Highlights

  • The brain, over the course of a lifetime, undergoes continuous and dynamic changes on multiple time scales (Sporns, 2018)

  • Unlike puberty or menopause, which are processes that occur in adolescence and adulthood, respectively, the menstrual cycle (MC) is a hormone-­related phenomenon that accompanies the women from puberty to menopause and repeats itself cyclically with periodical and coordinated variations of multiple hormones, such as estradiol, progesterone, follicular-­stimulating hormone (FSH), and luteinizing hormone (LH)

  • The correlation analysis evidenced that the betweenness centrality (BC) values increase in the right posterior cingulate gyrus (rPCG) was positively correlated with the changes in the blood levels of estradiol during the luteal phase

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Summary

Introduction

The brain, over the course of a lifetime, undergoes continuous and dynamic changes on multiple time scales (Sporns, 2018). During puberty, sex hormones contribute to morphological variations of the cortical and subcortical regions (Giedd et al, 1996; Sowell et al, 2007; van Duijvenvoorde et al, 2019) involved in sensorimotor processing, such as the thalamus and the caudate, as well as areas involved in emotion and memory processes, such as the amygdala and the hippocampus. Menopause is another example of the effects that sex hormones play on brain functions affecting both cognition (Maki & Henderson, 2016) and mood (Santoro et al, 2015). Such variations can induce a number of physical (acne, breast pain, cramps, headaches), neuro-­vegetative (sleep and eating disorders) (Guida et al, 2020; Yen et al, 2018), and psychopathological changes (anxiety, depression, moodiness) (Parry & Haynes, 2000)

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