GABAergic inhibition is weakened or converted into excitation in the oxytocin and vasopressin neurons of the lactating rat

Lee, Seung Won; Kim, Young Beom; Kim, Jeong Sook; Kim, Woong Bin; Kim, Yoon Sik; Han, Hee Chul; Colwell, Christopher S.; Cho, Young-Wuk; Kim, Yang In

doi:10.1186/s13041-015-0123-0

Cited by 39 publications

(34 citation statements)

References 41 publications

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“…We also found significant elevation of Gabra2, a gene encoding a subunit for the GABA A receptor. Plasticity at inhibitory synapses is strongly modulated by expression, localization, and function of GABA A receptors (Mele, Leal, & Duarte, 2016), which mediate inhibition onto magnocellular and parvocellular neurons and play a key role in their adaptive responses following stimulation (Bali & Kovacs, 2003;Lee et al, 2015). Elevation of Gabra2 following loss of BDNF signaling is consistent with previous reports demonstrating that BDNF is a robust modulator of synaptic inhibition and GABA A receptors (Brunig, Penschuck, Berninger, Benson, & Fritschy, 2001;Jovanovic, Thomas, Kittler, Smart, & Moss, 2004;Tanaka, Saito, & Matsuki, 1997) and can reduce inhibitory synaptic drive on neuroendocrine cells by decreasing GABA A surface expression (Hewitt & Bains, 2006).…”

Section: Bdnf Modulates Plasticity Genes In Oxt Neuronssupporting

confidence: 88%

BDNF-TrkB signaling in oxytocin neurons contributes to maternal behavior

Maynard

Hobbs

Phan

et al. 2018

Preprint

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Abstract:Brain-derived neurotrophic factor (Bdnf) transcription is controlled by several promoters, which drive expression of multiple transcripts encoding an identical protein. We previously reported that BDNF derived from promoters I and II is highly expressed in hypothalamus and is critical for regulating aggression in male mice. Here we report that BDNF loss from these promoters causes reduced sexual receptivity and impaired maternal care in female mice, which is concomitant with decreased oxytocin (Oxt) expression during development. We identify a novel link between BDNF signaling, oxytocin, and maternal behavior by demonstrating that ablation of TrkB selectively in OXT neurons partially recapitulates maternal care impairments observed in BDNF-deficient females. Using translating ribosome affinity purification and RNA-sequencing we define a molecular profile for OXT neurons and delineate how BDNF signaling impacts gene pathways critical for structural and functional plasticity. Our findings highlight BDNF as a modulator of sexually-dimorphic hypothalamic circuits that govern female-typical behaviors.peer-reviewed)

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Section: Bdnf Modulates Plasticity Genes In Oxt Neuronssupporting

confidence: 88%

BDNF-TrkB signaling in oxytocin neurons contributes to maternal behavior

Maynard

Hobbs

Phan

et al. 2018

Preprint

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“…Remarkably, during lactation, GABA inhibition of oxytocin neurones is converted into excitation (Lee et al . ). Hence, prolactin could potentially excite oxytocin neurones in lactating rats via GABA release from arcuate nucleus TH neurones.…”

Section: Discussionmentioning

confidence: 97%

“…(Romano et al 2013) and have recently been shown to directly inhibit paraventricular nucleus neurons via GABA release (Zhang & van den Pol, 2016). Remarkably, during lactation, GABA inhibition of oxytocin neurones is converted into excitation (Lee et al 2015). Hence, prolactin could potentially excite oxytocin neurones in lactating rats via GABA release from arcuate nucleus TH neurones.…”

Section: Mechanisms Of Prolactin Actions On Oxytocin Neuronesmentioning

confidence: 99%

Prolactin regulation of oxytocin neurone activity in pregnancy and lactation

Augustine

Ladyman

Bouwer

et al. 2017

The Journal of Physiology

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Secretion of prolactin for milk synthesis and oxytocin for milk secretion is required for successful lactation. In virgin rats, prolactin inhibits oxytocin neurones but this effect would be counterproductive during lactation when secretion of both hormones is required for synthesis and delivery of milk to the newborn. Hence, we determined the effects of intracerebroventricular (i.c.v.) prolactin on oxytocin neurones in urethane-anaesthetised virgin, pregnant and lactating rats. Prolactin (2 μg) consistently inhibited oxytocin neurones in virgin and pregnant rats (by 1.9 ± 0.4 and 1.8 ± 0.5 spikes s , respectively), but not in lactating rats; indeed, prolactin excited six of 27 oxytocin neurones by >1 spike s in lactating rats but excited none in virgin or pregnant rats (χ = 7.2, P = 0.03). Vasopressin neurones were unaffected by prolactin (2 μg) in virgin rats but were inhibited by 1.1 ± 0.2 spikes s in lactating rats. Immunohistochemistry showed that i.c.v. prolactin increased oxytocin expression in virgin and lactating rats and increased signal transducer and activator of transcription 5 phosphorylation to a similar extent in oxytocin neurones of virgin and lactating rats. Western blotting showed that i.c.v. prolactin did not affect phosphorylation of extracellular regulated kinase 1 or 2, or of Akt in the supraoptic or paraventricular nuclei of virgin or lactating rats. Hence, prolactin inhibition of oxytocin neurones is lost in lactation, which might allow concurrent elevation of prolactin secretion from the pituitary gland and activation of oxytocin neurones for synthesis and delivery of milk to the newborn.

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Section: Importance Of Inhibitory Inputmentioning

confidence: 99%

“…77 Two other studies have indicated that the direction of GABA actions can change from inhibition to excitation under conditions of chronic hyperactivation of vasopressin secretion,78,79 and one has reported a change affecting both oxytocin and vasopressin cells during lactation 80. This inhibitory effect can be blocked by microdialysis of the GABA antagonist bicuculline onto the supraoptic nucleus 73 (Figure 2), as can inhibition arising from stimulation of the arcuate nucleus.…”

mentioning

confidence: 98%

The osmoresponsiveness of oxytocin and vasopressin neurones: Mechanisms, allostasis and evolution

Leng

Russell

2019

J Neuroendocrinology

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In the rat supraoptic nucleus, every oxytocin cell projects to the posterior pituitary, and is involved both in reflex milk ejection during lactation and in regulating uterine contractions during parturition. All are also osmosensitive, regulating natriuresis. All are also regulated by signals that control appetite, including the neural and hormonal signals that arise from the gut after food intake and from the sites of energy storage. All are also involved in sexual behaviour, anxiety‐related behaviours and social behaviours. The challenge is to understand how a single population of neurones can coherently regulate such a diverse set of functions and adapt to changing physiological states. Their multiple functions arise from complex intrinsic properties that confer sensitivity to a wide range of internal and environmental signals. Many of these properties have a distant evolutionary origin in multifunctional, multisensory neurones of Urbilateria, the hypothesised common ancestor of vertebrates, insects and worms. Their properties allow different patterns of oxytocin release into the circulation from their axon terminals in the posterior pituitary into other brain areas from axonal projections, as well as independent release from their dendrites.

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GABAergic inhibition is weakened or converted into excitation in the oxytocin and vasopressin neurons of the lactating rat

Cited by 39 publications

References 41 publications

BDNF-TrkB signaling in oxytocin neurons contributes to maternal behavior

BDNF-TrkB signaling in oxytocin neurons contributes to maternal behavior

Prolactin regulation of oxytocin neurone activity in pregnancy and lactation

The osmoresponsiveness of oxytocin and vasopressin neurones: Mechanisms, allostasis and evolution

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