The cycling brain: menstrual cycle related fluctuations in hippocampal and fronto-striatal activation and connectivity during cognitive tasks

Pletzer, Belinda; Harris, TiAnni; Scheuringer, Andrea; Hidalgo-Lopez, Esmeralda

doi:10.1038/s41386-019-0435-3

Cited by 83 publications

(106 citation statements)

References 54 publications

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“…A recent longitudinal study of 36 women extends earlier findings showing a relation between increased levels of estradiol and hippocampal function . Interestingly, however, this relation appeared stronger in a spatial navigation than verbal fluency task.…”

Section: Menstrual Cyclesupporting

confidence: 81%

Ovarian hormones: a long overlooked but critical contributor to cognitive brain structures and function

Beltz

Moser

2019

Annals of the New York Academy of Sciences

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Cognitive neuroscience research has traditionally overlooked half of the population. Arguing that variability in ovarian hormones confounds empirical findings, girls and women have been excluded from research for decades. But times are changing. This review summarizes historical trends that have led to a knowledge gap in the role of ovarian hormones in neuroscience, synthesizes recent findings on ovarian hormone contributions to cognitive brain structures and function, and highlights areas ripe for future work. This is accomplished by reviewing research that has leveraged natural experiments in humans across the life span that focus on puberty, the menstrual cycle, hormonal contraceptive use, menopause, and menopausal hormone therapy. Although findings must be considered in light of study designs (e.g., sample characteristics and group comparisons versus randomized crossover trials), across natural experiments there is consistent evidence for associations of estradiol with cortical thickness, especially in frontal regions, and hippocampal volumes, as well as with frontal regions during cognitive processing. There are also emerging investigations of resting state connectivity and progesterone along with exciting opportunities for future work, particularly concerning biopsychosocial moderators of and individual differences in effects in novel natural experiments. Thus, delineating complex ovarian hormone contributions to cognitive brain structures and function will advance neuroscience.

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Section: Menstrual Cyclesupporting

confidence: 81%

Ovarian hormones: a long overlooked but critical contributor to cognitive brain structures and function

Beltz

Moser

2019

Annals of the New York Academy of Sciences

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“…As expected, the basal ganglia showed a significantly higher ALFF during the luteal phase but only for the caudate. Similarly, in a task-based design, we have recently observed an increased caudate activation irrespective of the task performed (Pletzer et al 2019). Although the relationship between ALFF and structure is not yet clear, an increase in caudate GM has been related to impaired pain and emotion processing, which are also altered during the luteal phase (Catenaccio et al 2016).…”

Section: Discussionmentioning

confidence: 70%

“…These results are in line with findings from Arélin et al (2015), where the increased connectivity between hippocampus and sensorimotor cortex was related to increased progesterone levels. Alternatively, the increase in the hippocampus' hierarchical position within the global network connectivity could reflect a compensatory mechanism for the drop in activation observed during the luteal phase (Pletzer et al 2019).…”

Section: Discussionmentioning

confidence: 99%

“…Despite the complex relation between structural and functional connectivity (Pessoa 2014), given the acute trophic effects on dendritic spine density and consequent synapse formation, these effects would also be expected to reflect on brain function and connectivity (Kitamura et al 2018). Indeed, higher brain activity has been observed in hippocampus before ovulation and in basal ganglia during the luteal phase (Pletzer et al 2019). Furthermore, both at rest and during different tasks, increased functional cortico-subcortical connectivity has been reported during the higher hormone phases (Peper et al 2011;Arélin et al 2015).…”

Section: Electronic Supplementary Materialsmentioning

confidence: 99%

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Human menstrual cycle variation in subcortical functional brain connectivity: a multimodal analysis approach

et al. 2020

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Increasing evidence suggests that endogenous sex steroid changes affect human brain functional connectivity, which could be obtained by resting-state fMRI (RS-fMRI). Nevertheless, RS studies on the menstrual cycle (MC) are underrepresented and yield inconsistent results. We attribute these inconsistencies to the use of various methods in exploratory approaches and small sample sizes. Hormonal fluctuations along the MC likely elicit subtle changes that, however, may still have profound impact on network dynamics when affecting key brain nodes. To address these issues, we propose a ROI-based multimodal analysis approach focusing on areas of high functional relevance to adequately capture these changes. To that end, sixty naturally cycling women underwent RS-fMRI in three different cycle phases and we performed the following analyses: (1) group-independent component analyses to identify intrinsic connectivity networks, (2) eigenvector centrality (EC) as a measure of centrality in the global connectivity hierarchy, (3) amplitude of low-frequency fluctuations (ALFF) as a measure of oscillatory activity and (4) seed-based analyses to investigate functional connectivity from the ROIs. For (2)-(4), we applied a hypothesis-driven ROI approach in the hippocampus, caudate and putamen. In the luteal phase, we found (1) decreased intrinsic connectivity of the right angular gyrus with the default mode network, (2) heightened EC for the hippocampus, and (3) increased ALFF for the caudate. Furthermore, we observed (4) stronger putamen-thalamic connectivity during the luteal phase and stronger fronto-striatal connectivity during the pre-ovulatory phase. This hormonal modulation of connectivity dynamics may underlie behavioural, emotional and sensorimotor changes along the MC.

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“…Specifically, the right MFG increased its activation during the luteal phase irrespective of the task [28][29][30] (Hidalgo-Lopez et al, under review). Relatedly, during resting state, increased eigenvector centrality in bilateral dorsolateral PFC has been found in the presence of higher progesterone levels 31 .…”

Section: Introductionmentioning

confidence: 99%

Predicting ovulation from brain connectivity: Dynamic causal modelling of the menstrual cycle

Hidalgo-Lopez

Zeidman

Harris

et al. 2020

Preprint

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Longitudinal menstrual cycle research allows the assessment of sex hormones effects on brain organization in a natural framework. Here, we used spectral dynamic causal modelling (spDCM) in a triple network model consisting of the default mode, salience and executive central networks (DMN, SN, and ECN), in order to address the changes in effective connectivity across the menstrual cycle. Sixty healthy young women were scanned three times (menses, pre-ovulatory and luteal phase) and spDCM was estimated for a total of 174 scans. Group level analysis using Parametric empirical Bayes showed lateralized and anterior-posterior changes in connectivity patterns depending on the cycle phase and related to the endogenous hormonal milieu. Right before ovulation the left insula recruited the frontoparietal network, while the right middle frontal gyrus decreased its connectivity to the precuneus. In exchange, the precuneus engaged bilateral angular gyrus, decoupling the DMN into anterior/posterior parts. During the luteal phase, bilateral insula engaged to each other decreasing the connectivity to parietal ECN, which in turn engaged the posterior DMN. Remarkably, the specific cycle phase in which a woman was in could be predicted by the connections that showed the strongest changes. These findings further corroborate the plasticity of the female brain in response to acute hormone fluctuations and have important implications for understanding the neuroendocrine interactions underlying cognitive changes along the menstrual cycle.

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The cycling brain: menstrual cycle related fluctuations in hippocampal and fronto-striatal activation and connectivity during cognitive tasks

Cited by 83 publications

References 54 publications

Ovarian hormones: a long overlooked but critical contributor to cognitive brain structures and function

Ovarian hormones: a long overlooked but critical contributor to cognitive brain structures and function

Human menstrual cycle variation in subcortical functional brain connectivity: a multimodal analysis approach

Predicting ovulation from brain connectivity: Dynamic causal modelling of the menstrual cycle

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