Chapter 2 Hypothalamic Neural Systems Controlling the Female Reproductive Life Cycle

Jacqueline A. Maffucci; Andrea C. Gore

doi:10.1016/s1937-6448(08)02002-9

Cited by 94Hypothalamic control of reproductive hormonesReproductive Biology and FertilityNeuroendocrine regulation and behavior

Chapter 2 Hypothalamic Neural Systems Controlling the Female Reproductive Life Cycle

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Jacqueline A. Maffucci, Andrea C. Gore·2009·International Review of Cell and Molecular Biology

DOI 10.1016/s1937-6448(08)02002-9PMC PMC2821833

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Abstract

The hypothalamic-pituitary-gonadal (HPG) axis undergoes a number of changes throughout the reproductive life cycle that are responsible for the development, puberty, adulthood, and senescence of reproductive systems. This natural progression is dictated by the neural network controlling the hypothalamus including the cells that synthesize and release gonadotropin-releasing hormone (GnRH) and their regulatory neurotransmitters. Glutamate and GABA are the primary excitatory and inhibitory neurotransmitters in the central nervous system, and as such contribute a great deal to modulating this axis throughout the lifetime via their actions on receptors in the hypothalamus, both directly on GnRH neurons as well as indirectly through other hypothalamic neural networks. Interactions among GnRH neurons, glutamate, and GABA, including the regulation of GnRH gene and protein expression, hormone release, and modulation by estrogen, are critical to age-appropriate changes in reproductive function. Here, we present evidence for the modulation of GnRH neurosecretory cells by the balance of glutamate and GABA in the hypothalamus, and the functional consequences of these interactions on reproductive physiology across the life cycle.

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The occurrence of the LH surge is coincident with a decline of GABAergic transmission to both POA kisspeptin neurons and GnRH neurons.
“and that its occurrence is coincident with a decline of GABAergic transmission to both POA kisspeptin neurons and GnRH neurons [106,107].”
From Fibromyalgia pathogenesis explained by a neuroendocrine multistable model (2024) · cites this paper as [107]
Section V.C reports that GABA levels in the POA-AH decrease just before the LH surge and suggests this disinhibits GnRH neurons. It does not report a decline in GABAergic transmission to POA kisspeptin neurons; the Conclusion mentions kisspeptin only as a neuropeptide feeding into the circuitry. The evidence also places the observed GABA decline before, rather than precisely coincident with, the surge. Page numbers were not available in our copy. (LLM, conf=0.89)
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Gamma-Aminobutyric Acid Neurons in the Preoptic/Anterior Hypothalamic Area Synchronize the Phasic Activity of the Gonadotropin-Releasing Hormone Pulse Generator in Ovariectomized Rats
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Age-Related Changes in Pulsatile Luteinizing Hormone Release Precede the Transition to Estrous Acyclicity and Depend upon Estrous Cycle History*
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Neuroendocrine control of reproductive aging: roles of GnRH neurons
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A role for medial preoptic nucleus on afternoon of proestrus in female rats
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Sex differences in γ-aminobutyric acid and glutamate concentrations in discrete rat brain nuclei
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Neuroendocrine Changes in the Aging Reproductive Axis of Female Rhesus Macaques (Macaca mulatta)1
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Developmental sex differences in amino acid neurotransmitter levels in hypothalamic and limbic areas of rat brain
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γ-Aminobutyric Acid Neurons Integrate and Rapidly Transmit Permissive and Inhibitory Metabolic Cues to Gonadotropin-Releasing Hormone Neurons
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Several GABAA receptor subunits are expressed in LHRH neurons of juvenile female rats1This work was supported by grants from the National Institutes of Health, HD25123 (S.R.O.), P30 Population Center Grant HD18185 and RR00163 for the operation of the Oregon Regional Primate Research Center.1
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N-methyl-D-aspartate (NMDA) receptors mediate the release of gonadotropin-releasing hormone (GnRH) by NMDA in a hypothalamic GnRH neuronal cell line (GT1-1)
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Preoptic rather than Mediobasal Hypothalamic Amino Acid Neurotransmitter Release Regulates GnRH Secretion during the Estrogen-Induced LH Surge in the Ovariectomized Rat
Jarry, H., Leonhardt, S., Schwarze, T., & Wuttke, W. (2008) · Neuroendocrinology · doi:10.1159/000127037 · Cited by 84 · see citing works
LHRH neurons in the female C57BL/6J mouse brain during reproductive aging: No loss up to middle age
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Glutamate Inhibits GABA Excitatory Activity in Developing Neurons
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Excitatory Neurotransmission and Sexual Differentiation of the Brain
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The Morphometry of Astrocytes in the Rostral Preoptic Area Exhibits a Diurnal Rhythm on Proestrus: Relationship to the Luteinizing Hormone Surge and Effects of Age
Cashion, A. B., Smith, M. J., & Wise, P. M. (2002) · Endocrinology · doi:10.1210/en.2002-220711 · Cited by 80 · see citing works
Neurosteroids Alter γ-Aminobutyric Acid Postsynaptic Currents in Gonadotropin-Releasing Hormone Neurons: A Possible Mechanism for Direct Steroidal Control
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Menopausal Increases in Pulsatile Gonadotropin-Releasing Hormone Release in a Nonhuman Primate (Macaca mulatta)
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Biphasic Gabaergic Regulation of GnRH Secretion in GT 1 Cell Lines
de la Escalera, G. M., Choi, A. L. H., & Weiner, R. I. (2008) · Neuroendocrinology · doi:10.1159/000126687 · Cited by 78 · see citing works
Glutamatergic Signaling through theN-Methyl- d -Aspartate Receptor Directly Activates Medial Subpopulations of Luteinizing Hormone-Releasing Hormone (LHRH) Neurons, But Does Not Appear to Mediate the Effects of Estradiol on LHRH Gene Expression
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REGIONAL CHANGES IN AMINO ACID CONTENT IN DEVELOPING RAT BRAIN1
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Aging Results in Attenuated Gonadotropin Releasing Hormone‐Luteinizing Hormone Axis Responsiveness to Glutamate Receptor Agonist N‐Methyl‐D‐Aspartate*
Bonavera, J. J., Swerdloff, R. S., HIKIM, A. P. S., Lue, Y., & Wang, C. (1998) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1998.00177.x · Cited by 75 · see citing works
Firing Pattern and Rapid Modulation of Activity by Estrogen in Primate Luteinizing Hormone Releasing Hormone-1 Neurons
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GABA receptors precede glutamate receptors in hypothalamic development; differential regulation by astrocytes
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Sustained Intermittent Release of Gonadotropin-Releasing Hormone in the Prepubertal Male Rhesus Monkey Induced by N-Methyl-DL-Aspartic Acid
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GABA-Dependent Firing of Glutamate-Evoked Action Potentials at AMPA/Kainate Receptors in Developing Hypothalamic Neurons
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GABAergic neuronal activity and mRNA levels for both forms of glutamic acid decarboxylase (GAD65 and GAD67) are reduced in the diagonal band of Broca during the afternoon of proestrus
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Regulation of GABA transporter activity and mRNA expression by estrogen in rat preoptic area
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Activation of Central GABA A - but Not of GABA B – Receptors Rapidly Reduces Pituitary LH Release and GnRH Gene Expression in the Preoptic/Anterior Hypothalamic Area of Ovariectomized Rats
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Neuroendocrine Aging in the Female Rat: The Changing Relationship of Hypothalamic Gonadotropin-Releasing Hormone Neurons and N-Methyl-d-Aspartate Receptors**Preliminary versions of this work were presented at the 28th and 29th Annual Meetings of the Society for Neuroscience (Abstracts 110.11 and 777.10). This work was supported by the Brookdale Foundation (to A.C.G.), NIH Grant 1-PO1-AG16765–01 (to A.C.G. and J.H.M.).
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Steroid modulation of GABAA receptor-mediated transmission in the hypothalamus: Effects on reproductive function
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Neuroendocrine Mechanisms for Reproductive Senescence in the Female Rat: Gonadotropin-Releasing Hormone Neurons
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Qualitative Changes in Luteinizing Hormone and Prolactin Responses toN-Methyl-Aspartic Acid during Lactation in the Rat*
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Age-Related Changes in Estrogen Receptor β in Rat Hypothalamus: A Quantitative Analysis
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Release of Glutamate and Aspartate from the Preoptic Area during the Progesterone-Induced LH Surge: In vivo Microdialysis Studies
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Role of medial preoptic GABA neurones in regulating luteinising hormone secretion in the ovariectomised rat
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Activation of A‐Type γ‐Amino Butyric Acid Receptors Excites Gonadotrophin‐Releasing Hormone Neurones Isolated from Adult Rats
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A progesterone metabolite stimulates the release of gonadotropin-releasing hormone from GT1-1 hypothalamic neurons via the gamma-aminobutyric acid type A receptor.
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Immortalized hypothalamic GT1-7 neurons express functional gamma-aminobutyric acid type A receptors.
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Glutamate Modulates [Ca 2+ ] i and Gonadotropin-Releasing Hormone Secretion in Immortalized Hypothalamic GT1-7 Neurons
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The number and distribution of detectable luteinizing hormone (LH)-releasing hormone cell bodies changes in association with the preovulatory LH surge in the brains of young but not middle-aged female rats.
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Differential expression of gamma-aminobutyric acid receptors in immortalized luteinizing hormone-releasing hormone neurons
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Live View of Gonadotropin-Releasing Hormone Containing Neuron Migration
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[128]Jung H Shannon EM Fritschy JM Ojeda SR Several GABAA receptor subunits are expressed in LHRH neurons of juvenile female rats Brain Res 1998 780 218 229 9507141
[150]Maffucci JA Walker DM Ikegami A Woller MJ Gore AC The NMDA receptor subunit NR2b affects LH release and GnRH gene expression in female rats, with modulation by estradiol Neuroendocrinology 2008 87 129 141 18025808 PMC2671961
[231]van den Pol AN GABA immunoreactivity in hypothalamic neurons and growth cones in early development in vitro before synapse formation J Comp Neurol 1997 383 178 188 9182847

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Self-citation

Authors: Maffucci, J. A., & Gore, A. C.
Affiliations: The University of Texas at Austin (US)
ORCID: Andrea C. Gore
Venue: International Review of Cell and Molecular Biology
Publisher: Elsevier
Published: 2009
Volume: 274
Pages: 69-127
ISSN: 0074-7696 (ISSN-L)
1937-6448
DOI: 10.1016/s1937-6448(08)02002-9
PMC: PMC2821833
OpenAlex: W1496951129
Cited by: 93
References: 259
Citations by year: 2026: 3 · 2025: 8 · 2024: 3 · 2023: 5 · 2022: 3 · 2021: 4 · 2020: 9 · 2019: 9 · 2018: 3 · 2017: 6 · 2016: 3 · 2015: 5 · 2014: 7 · 2013: 5 · 2012: 3
FWCI: 23.91
Type: book chapter
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: International review of cytology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute on Aging (AG-16765, AG028051, R01AG028051, P01AG016765)
Topics: Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Keywords: hypothalamic-pituitary-gonadal axis, gonadotropin-releasing hormone, GnRH neurons, glutamate, GABA, neurotransmitter modulation, puberty, reproductive aging, estrogen modulation, GnRH gene expression
MeSH terms: Animals, Female, gamma-Aminobutyric Acid, Glutamates, Humans, Hypothalamo-Hypophyseal System, Gonadotropin-Releasing Hormone, Nervous System, Reproduction

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Chapter 2 Hypothalamic Neural Systems Controlling the Female Reproductive Life Cycle

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