Estrogen positive feedback to gonadotropin-releasing hormone (GnRH) neurons in the rodent: The case for the rostral periventricular area of the third ventricle (RP3V)

Herbison, Allan E.

doi:10.1016/j.brainresrev.2007.05.006

Cited by 351Hypothalamic control of reproductive hormonesNeuroendocrine regulation and behaviorReproductive Biology and Fertility

Estrogen positive feedback to gonadotropin-releasing hormone (GnRH) neurons in the rodent: The case for the rostral periventricular area of the third ventricle (RP3V)

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Herbison, Allan E.·2008·Brain Research Reviews

DOI 10.1016/j.brainresrev.2007.05.006PMC PMC6116895

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Abstract

Increasing levels of circulating estradiol during the follicular phase of the ovarian cycle act on the brain to trigger a sudden and massive release of gonadotropin-releasing hormone (GnRH) that evokes the pituitary luteinizing hormone surge responsible for ovulation in mammals. The mechanisms through which estrogen is able to exert this potent "positive feedback" influence upon the GnRH neurons are beginning to be unravelled. Recent studies utilizing mouse models with global and cell-specific deletions of the different estrogen receptors (ERs) have shown that estrogen positive feedback is likely to use an indirect pathway involving the modulation of ERalpha-expressing neurons that project to GnRH neurons. Conventional tract tracing studies in rats, and experiments involving conditional pseudorabies virus tract tracing from GnRH neurons in the transgenic mouse, indicate that the dominant populations of ERalpha-expressing neuronal afferents to GnRH neurons reside in the anteroventral periventricular, median preoptic and periventricular preoptic nuclei. Together these estrogen-sensitive afferents to GnRH neurons form a periventricular continuum that can be referred to as rostral periventricular area of the third ventricle (RP3V) neurons. The neurochemical identity of some RP3V neurons has been determined and there is mounting evidence for important roles of glutamate, GABA, kisspeptin and neurotensin-expressing RP3V neurons in estrogen positive feedback. The definition of the key cluster of estrogen-sensitive neurons responsible for activating the GnRH neurons to evoke the GnRH surge (and ovulation) should be of substantial value to on-going efforts to understand the molecular and cellular basis of the estrogen positive feedback mechanism.

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Evidence supports the AVPV/PeN kisspeptin role in the LH surge: Kiss1 expression is higher in females, these neurons have ERα and activate during the surge, and Kiss1 or Kiss1R knockout mice lack the surge even with E2.
“Supporting this hypothesis, AVPV/PeN Kiss1 gene expression is greater in females than males (males do not show an LH surge), Kiss1 neurons in the AVPV/PeN express ERα and show increased neuronal activation exclusively during the LH surge, and Kiss1 knockout (KO) mice and Kiss1R KO mice do not exhibit an LH surge even with exogenous E2 treatment3,5.”
From Emerging insights into hypothalamic‐pituitary‐gonadal axis regulation and interaction with stress signalling (2018) · cites this paper as [3]
The “Neurochemical phenotypes of RP3V neurons” section describes a female-dominant distribution of AVPV/PVpo kisspeptin neurons, ERα expression, and c-Fos activation at the time of estrogen positive feedback. It also reports evidence that kisspeptin is required for the GnRH surge, but does not report that Kiss1 or Kiss1R knockout mice lack an LH surge despite exogenous E2 treatment. (LLM, conf=0.88)
Experimental — accuracy not yet measured
GnRH cells lack ERα and AR, so other steroid-sensitive circuits upstream relay feedback to them.
“Importantly, GnRH neurons do not express estrogen receptor α (ERα) or the androgen receptor (AR), the receptors that mediate sex steroid feedback, indicating that other sex steroid-sensitive circuits “upstream” of GnRH neurons receive and relay sex steroid feedback signals to GnRH cells3.”
From Emerging insights into hypothalamic‐pituitary‐gonadal axis regulation and interaction with stress signalling (2018) · cites this paper as [3]
The ‘Mechanism of estrogen positive feedback to GnRH neurons’ section states that GnRH neurons lack ERα and that ERα-expressing neurons mediate indirect estrogen feedback. It does not address whether GnRH neurons lack androgen receptors or whether upstream circuits relay androgen feedback. (LLM, conf=0.88)
Experimental — accuracy not yet measured
E2-induced AVPV/PeN kisspeptin expression accompanies increased neuronal activation and peptide release onto GnRH neurons to drive the preovulatory GnRH/LH surge.
“This E2-induced expression of AVPV/PeN kisspeptin occurs with an increase in kisspeptin neuronal activation and peptide release onto GnRH neurons to drive the pre-ovulatory surge of GnRH and LH3,5.”
From Emerging insights into hypothalamic‐pituitary‐gonadal axis regulation and interaction with stress signalling (2018) · cites this paper as [3]
In “Neurochemical phenotypes of RP3V neurons” (page not provided), the review reports estrogen-associated kisspeptin expression, activation of kisspeptin neurons during positive feedback, and evidence for their role in the GnRH surge. It does not establish increased kisspeptin release onto GnRH neurons; the same section says the relationship between rising neuropeptide mRNA and an abrupt increase in secretion is unknown. (LLM, conf=0.88)
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Detection of Estrogen Receptor- Messenger Ribonucleic Acid and 125I-Estrogen Binding Sites in Luteinizing Hormone-Releasing Hormone Neurons of the Rat Brain
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ENDOGENOUS EXCITATORY AMINO ACID NEUROTRANSMISSION REGULATES THE ESTRADIOL-INDUCED LH SURGE IN OVARIECTOMIZED RATS
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Further evidence that preoptic anterior hypothalamic GABAergic neurons are part of the GnRH pulse and surge generator
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Periventricular Preoptic Area Neurons Coactivated with Luteinizing Hormone (LH)-Releasing Hormone (LHRH) Neurons at the Time of the LH Surge Are LHRH Afferents
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Changes in the Release of Gamma‐Aminobutyric Acid and Catecholamines in the Preoptic/Septal Area Prior to and During the Preovulatory Surge of Luteinizing Hormone in the Ewe
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Variable patterns of gonadotropin-releasing hormone secretion during the estrogen-induced luteinizing hormone surge in ovariectomized ewes.
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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
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Estrogen-concentrating cells within cell groups of the medial preoptic area: sex differences and co-localization with galanin-immunoreactive cells
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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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Does estradiol induce the preovulatory gonadotropin-releasing hormone (GnRH) surge in the ewe by inducing a progressive change in the mode of operation of the GnRH neurosecretory system
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Evidence that Neurotensin Participates in the Central Regulation of the Preovulatory Surge of Luteinizing Hormone in the Rat*
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Possible Role of Non-NMDA Receptor-Mediated Neurotransmission in Steroid-Induced and Preovulatory Gonadotropin Surges in the Rat
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Variable patterns of gonadotropin-releasing hormone secretion during the estrogen-induced luteinizing hormone surge in ovariectomized ewes
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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
Rubin, B. S. (1994) · Endocrinology · doi:10.1210/en.134.1.467 · Cited by 21 · see citing works
FOS expression in the gonadotropin-releasing hormone (GnRH) neuron does not increase during the ovarian steroid-induced GnRH surge in the rhesus monkey
Witkin, J. W. (1994) · Endocrinology · doi:10.1210/en.135.3.956 · Cited by 15 · see citing works
Untitled work
(1997) · doi:10.1002/(sici)1096-9861(19971201)388:4
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(1999) · doi:10.1002/(sici)1096-9861(19990823)411:2

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Minireview: Kisspeptin/Neurokinin B/Dynorphin (KNDy) Cells of the Arcuate Nucleus: A Central Node in the Control of Gonadotropin-Releasing Hormone Secretion
Lehman, M. N., Coolen, L. M., & Goodman, R. L. (2010) · Endocrinology · doi:10.1210/en.2010-0022 · Cited by 768 · see citing works
Estrogen actions in the brain and the basis for differential action in men and women: a case for sex-specific medicines
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Control of puberty onset and fertility by gonadotropin-releasing hormone neurons
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Self-citation
Characterization of Kiss1 neurons using transgenic mouse models
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Sex differences in circadian timing systems: implications for disease
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The kisspeptin system of the human hypothalamus: sexual dimorphism and relationship with gonadotropin‐releasing hormone and neurokinin B neurons
Hrabovszky, E., Ciofi, P., Vida, B., Horvath, M. C., Keller, E., Caraty, A., Bloom, S. R., Ghatei, M. A., Dhillo, W. S., Liposits, Z., et al. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07239.x · Cited by 314 · see citing works
Emerging insights into hypothalamic‐pituitary‐gonadal axis regulation and interaction with stress signalling
Acevedo‐Rodriguez, A., Kauffman, A. S., Cherrington, B. D., Borges, C. S., Roepke, T. A., & Laconi, M. (2018) · Journal of neuroendocrinology · doi:10.1111/jne.12590 · Cited by 298 · see citing works
“(3) During physiological or psychosocial stresses, activation of the HPG axis and corticotrophin- releasing hormone (CRH) (orange) neurones of the paraventricular nucleus (PVN) will directly impinge on GnRH activity to suppress LH pulsatility.”
GnRH signaling, the gonadotrope and endocrine control of fertility
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Estrogen impairs glucocorticoid dependent negative feedback on the hypothalamic–pituitary–adrenal axis via estrogen receptor alpha within the hypothalamus
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Down‐Regulation of Hypothalamic Kisspeptin and its Receptor, Kiss1r , mRNA Expression is Associated with Stress‐Induced Suppression of Luteinising Hormone Secretion in the Female Rat
Kinsey‐Jones, J. S., Li, X. F., Knox, A. M. I., Wilkinson, E. S., Zhu, X. L., Chaudhary, A. A., Milligan, S. R., Lightman, S. L., & O’Byrne, K. T. (2009) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01807.x · Cited by 196 · see citing works
Circadian Regulation of Kiss1 Neurons: Implications for Timing the Preovulatory Gonadotropin-Releasing Hormone/Luteinizing Hormone Surge
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Circadian Control of Kisspeptin and a Gated GnRH Response Mediate the Preovulatory Luteinizing Hormone Surge
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Neuroanatomy of the kisspeptin signaling system in mammals: comparative and developmental aspects
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Forebrain projections of arcuate neurokinin B neurons demonstrated by anterograde tract-tracing and monosodium glutamate lesions in the rat
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Neuroendocrine control of gonadotropin‐releasing hormone: Pulsatile and surge modes of secretion
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Self-citation
Central and Peripheral Effects of RFamide-Related Peptide-3 on Luteinizing Hormone and Prolactin Secretion in Rats
Anderson, G. M., Relf, H.-L., Rizwan, M. Z., & Evans, J. J. (2009) · Endocrinology · doi:10.1210/en.2008-1359 · Cited by 157 · see citing works
Evidence for Suprachiasmatic Vasopressin Neurones Innervating Kisspeptin Neurones in the Rostral Periventricular Area of the Mouse Brain: Regulation by Oestrogen
Vida, B., Deli, L., Hrabovszky, E., Kalamatianos, T., Caraty, A., Coen, C. W., Liposits, Z., & Kalló, I. (2010) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2010.02045.x · Cited by 156 · see citing works
Identification of prolactin-sensitive GABA and kisspeptin neurons in regions of the rat hypothalamus involved in the control of fertility
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Expression of ESR1 in Glutamatergic and GABAergic Neurons Is Essential for Normal Puberty Onset, Estrogen Feedback, and Fertility in Female Mice
Cheong, R. Y., Czieselsky, K., Porteous, R., & Herbison, A. E. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.1776-15.2015 · Cited by 114 · see citing works
Self-citation
Coming of age in the Kisspeptin Era: Sex differences, development, and puberty
Kauffman, A. S. (2010) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2010.01.017 · Cited by 106 · see citing works
The Role of Kisspeptin and RFamide‐Related Peptide‐3 Neurones in the Circadian‐Timed Preovulatory Luteinising Hormone Surge
Khan, A. R., & Kauffman, A. S. (2012) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02162.x · Cited by 99 · see citing works
Estrogen Permits Vasopressin Signaling in Preoptic Kisspeptin Neurons in the Female Mouse
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Roles for Oestrogen Receptor β in Adult Brain Function
Handa, R. J., Ogawa, S., Wang, J. M., & Herbison, A. E. (2012) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02206.x · Cited by 97 · see citing works
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Differential actions of prolactin on electrical activity and intracellular signal transduction in hypothalamic neurons
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Corticosterone Blocks Ovarian Cyclicity and the LH Surge via Decreased Kisspeptin Neuron Activation in Female Mice
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The Neurosteroid Progesterone Underlies Estrogen Positive Feedback of the LH Surge
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Developmental Exposure to Ethinylestradiol Affects Reproductive Physiology, the GnRH Neuroendocrine Network and Behaviors in Female Mouse
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Ovulatory Response, and Plasma Concentrations of Luteinizing Hormone and Progesterone Following Administration of Synthetic Mammalian or Chicken Luteinizing Hormone-Releasing Hormone Relative to the First or Second Ovulation in the Sequence of the Domestic Hen
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Suppression of Ovulation in the Rat by an Orally Active Antagonist of Luteinizing Hormone-Releasing Hormone
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Peripheral Estrogen Levels During the Laying Cycle of the Hen (Gallus domesticus)
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Authors: Herbison, A. E.
Affiliations: University of Otago (NZ)
Corresponding author: Herbison, Allan E.
ORCID: Herbison, Allan E.
Venue: Brain Research Reviews
Publisher: Elsevier BV
Published: 2008-03
Volume: 57
Issue: 2
Pages: 277-287
ISSN: 0165-0173 (ISSN-L)
DOI: 10.1016/j.brainresrev.2007.05.006
PMC: PMC6116895
OpenAlex: W1986934594
Cited by: 351
References: 120
Citations by year: 2026: 9 · 2025: 9 · 2024: 9 · 2023: 23 · 2022: 18 · 2021: 17 · 2020: 19 · 2019: 11 · 2018: 16 · 2017: 6 · 2016: 13 · 2015: 22 · 2014: 21 · 2013: 25 · 2012: 24
FWCI: 3.87
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Brain Research Reviews (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: Wellcome Trust (063216)
Royal Society
Royal Society Te Apārangi
Health Research Council of New Zealand
Marsden Fund
Topics: Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
Keywords: estrogen positive feedback, GnRH neurons, estrogen receptor alpha, GnRH surge, ovulation, anteroventral periventricular nucleus, median preoptic nucleus, kisspeptin neurons, follicular phase
MeSH terms: Animals, Estrogens, Female, Gonadotropin-Releasing Hormone, Neural Pathways, Neurons, Ovulation, Preoptic Area, Neurotransmitter Agents, Third Ventricle, Feedback, Physiological, Mice, Rats

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

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Estrogen positive feedback to gonadotropin-releasing hormone (GnRH) neurons in the rodent: The case for the rostral periventricular area of the third ventricle (RP3V)

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