Cyclic changes and actions of progesterone and allopregnanolone on cognition and hippocampal basal (stratum oriens) dendritic spines of female rats

Barreto-Cordero, Lorna Marcela; Ríos-Carrillo, Jorge; Roldán-Roldán, Gabriel; Rasia‐Filho, Alberto A.; Flores, Gonzalo; Bringas, María Elena; Briones-Aranda, Alfredo; Picazo, Ofir Picazo

doi:10.1016/j.bbr.2019.112355

Cited by 13 publications

(8 citation statements)

References 55 publications

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“…We have shown images from males. Nevertheless, pyramidal neurons in the rat CA1 hippocampal region are subject to various modulatory factors that can affect spine number and shape depending on sex steroids, such as fluctuations in estrogen and progesterone circulating levels and the expression of aromatase (Woolley et al, 1990;Brusco et al, 2008;Yague et al, 2010;Hansberg-Pastor et al, 2015;Sheppard et al, 2019;Barreto-Cordero et al, 2020). Indeed, morphological differences related to sex were reported for human insular pyramidal neurons (Anderson et al, 2009) and for the hippocampal estrogen receptor-α localization in neurofibrillary tangles along with AD (Wang et al, 2016).…”

Section: Integrating Pyramidal Morphology On Complex Network In the Human Brainmentioning

confidence: 99%

The Subcortical-Allocortical- Neocortical continuum for the Emergence and Morphological Heterogeneity of Pyramidal Neurons in the Human Brain

Rasia‐Filho

Guerra

Vásquez

et al. 2021

Front. Synaptic Neurosci.

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Human cortical and subcortical areas integrate emotion, memory, and cognition when interpreting various environmental stimuli for the elaboration of complex, evolved social behaviors. Pyramidal neurons occur in developed phylogenetic areas advancing along with the allocortex to represent 70–85% of the neocortical gray matter. Here, we illustrate and discuss morphological features of heterogeneous spiny pyramidal neurons emerging from specific amygdaloid nuclei, in CA3 and CA1 hippocampal regions, and in neocortical layers II/III and V of the anterolateral temporal lobe in humans. Three-dimensional images of Golgi-impregnated neurons were obtained using an algorithm for the visualization of the cell body, dendritic length, branching pattern, and pleomorphic dendritic spines, which are specialized plastic postsynaptic units for most excitatory inputs. We demonstrate the emergence and development of human pyramidal neurons in the cortical and basomedial (but not the medial, MeA) nuclei of the amygdala with cells showing a triangular cell body shape, basal branched dendrites, and a short apical shaft with proximal ramifications as “pyramidal-like” neurons. Basomedial neurons also have a long and distally ramified apical dendrite not oriented to the pial surface. These neurons are at the beginning of the allocortex and the limbic lobe. “Pyramidal-like” to “classic” pyramidal neurons with laminar organization advance from the CA3 to the CA1 hippocampal regions. These cells have basal and apical dendrites with specific receptive synaptic domains and several spines. Neocortical pyramidal neurons in layers II/III and V display heterogeneous dendritic branching patterns adapted to the space available and the afferent inputs of each brain area. Dendritic spines vary in their distribution, density, shapes, and sizes (classified as stubby/wide, thin, mushroom-like, ramified, transitional forms, “atypical” or complex forms, such as thorny excrescences in the MeA and CA3 hippocampal region). Spines were found isolated or intermingled, with evident particularities (e.g., an extraordinary density in long, deep CA1 pyramidal neurons), and some showing a spinule. We describe spiny pyramidal neurons considerably improving the connectional and processing complexity of the brain circuits. On the other hand, these cells have some vulnerabilities, as found in neurodegenerative Alzheimer’s disease and in temporal lobe epilepsy.

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Section: Integrating Pyramidal Morphology On Complex Network In the Human Brainmentioning

confidence: 99%

The Subcortical-Allocortical- Neocortical continuum for the Emergence and Morphological Heterogeneity of Pyramidal Neurons in the Human Brain

Rasia‐Filho

Guerra

Vásquez

et al. 2021

Front. Synaptic Neurosci.

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“…Animal research has broadly evidenced the rapid changes exerted by sex hormones on the neuronal excitatory/inhibitory balance 2 , synaptogenesis 3 , myelination and remyelination 4 . More importantly, these effects result in synaptic connectivity changes and therefore neural function 5,6 , and in rodents a direct link to improved cognition has already been established for both hormones 7,8 . However, in humans, menstrual cycle-related changes remain underinvestigated.…”

Section: Introductionmentioning

confidence: 97%

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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“…Animal research has broadly evidenced the rapid changes exerted by estradiol and progesterone on the neuronal excitatory/inhibitory balance 2 , synaptogenesis 3 , myelination and re-myelination 4 . These effects result in synaptic connectivity changes and therefore neural function 5,6 , and in rodents high levels of both hormones have been shown to improve cognition 7,8 . In ovariectomized rats, both estradiol and progesterone treatment enhances novel object recognition, mechanistically linked to increased long-term potentiation and Nmethyl-D-aspartic acid receptors at hippocampal synapses for estradiol 7 , and to an increased density of the basal dendrites of hippocampal neurons for progesterone 8 .…”

mentioning

confidence: 99%

“…These effects result in synaptic connectivity changes and therefore neural function 5,6 , and in rodents high levels of both hormones have been shown to improve cognition 7,8 . In ovariectomized rats, both estradiol and progesterone treatment enhances novel object recognition, mechanistically linked to increased long-term potentiation and Nmethyl-D-aspartic acid receptors at hippocampal synapses for estradiol 7 , and to an increased density of the basal dendrites of hippocampal neurons for progesterone 8 . More importantly, as evidenced in hormonal replacement studies in rodents 9 and nonhuman primates [10][11][12] at least some of the reported neuroactive effects are dependent on a cyclic variation of hormone levels, as opposed to a continuous schedule of treatment.…”

mentioning

confidence: 99%

Spectral dynamic causal modelling in healthy women reveals brain connectivity changes along the menstrual cycle

et al. 2021

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Longitudinal menstrual cycle studies allow to investigate the effects of ovarian hormones on brain organization. Here, we use spectral dynamic causal modelling (spDCM) in a triple network model to assess effective connectivity changes along the menstrual cycle within and between the default mode, salience and executive control networks (DMN, SN, and ECN). Sixty healthy young women were scanned three times along their menstrual cycle, during early follicular, pre-ovulatory and mid-luteal phase. Related to estradiol, right before ovulation the left insula recruits the ECN, while the right middle frontal gyrus decreases its connectivity to the precuneus and the DMN decouples into anterior/posterior parts. Related to progesterone during the mid-luteal phase, the insulae (SN) engage to each other, while decreasing their connectivity to parietal ECN, which in turn engages the posterior DMN. When including the most confident connections in a leave-one out cross-validation, we find an above-chance prediction of the left-out subjects’ cycle phase. These findings corroborate the plasticity of the female brain in response to acute hormone fluctuations and may help to further understand the neuroendocrine interactions underlying cognitive changes along the menstrual cycle.

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Cyclic changes and actions of progesterone and allopregnanolone on cognition and hippocampal basal (stratum oriens) dendritic spines of female rats

Cited by 13 publications

References 55 publications

The Subcortical-Allocortical- Neocortical continuum for the Emergence and Morphological Heterogeneity of Pyramidal Neurons in the Human Brain

The Subcortical-Allocortical- Neocortical continuum for the Emergence and Morphological Heterogeneity of Pyramidal Neurons in the Human Brain

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

Spectral dynamic causal modelling in healthy women reveals brain connectivity changes along the menstrual cycle

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