Structural plasticity in the hypothalamic supraoptic nucleus at lactation affects oxytocin-, but not vasopressin-secreting neurones

Theodosis, Dionysia T.; Chapman, David; Montagnese, Catherine M.; Poulain, Daniel; Morris, John F.

doi:10.1016/0306-4522(86)90038-2

Cited by 165 publications

(88 citation statements)

References 23 publications

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“…During the reproductive cycle, structural plasticity in the hypothalamic system leads to retraction of glial cells and hypertrophy of neurons (Theodosis et al, 1986;Theodosis and Poulain, 1993;Hatton, 1997). Oliet et al (2001) showed that regulation of synaptic release of glutamate within the SON is under control of metabotropic glutamate receptors and proposed that this type of retrograde signaling is sensitive to the extent of glial withdrawal.…”

Section: Regulation Of Somatodendritic Release During Lactationmentioning

confidence: 99%

Somatodendritic Secretion in Oxytocin Neurons Is Upregulated during the Female Reproductive Cycle

Kock¹,

Wierda²,

Bosman³

et al. 2003

J. Neurosci.

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During the female reproductive cycle, hypothalamic oxytocin (OT) neurons undergo sharp changes in excitability. In lactating mammals, bursts of electrical activity of OT neurons result in the release of large amounts of OT in the bloodstream, which causes milk ejection. One hypothesis is that OT neurons regulate their own firing activity and that of nearby OT neurons by somatodendritic release of OT. In this study, we show that OT neuron activity strongly reduces inhibitory synaptic transmission to these neurons. This effect is blocked by antagonists of both adenosine and OT receptors and is mimicked by OT application. Inhibition of soluble N-ethylmaleimide-sensitive factor attachment protein receptor complex formation by tetanus toxin completely blocked the stimulation-induced reduction in inhibitory input, as did the calcium chelator BAPTA. During lactation, the readily releasable pool of secretory vesicles in OT cell bodies was doubled, and calcium currents were upregulated. This resulted in an increased inhibition of GABAergic synaptic transmission by somatodendritic release during lactation compared with the adult virgin stage. These results demonstrate that somatodendritic release is augmented during lactation, which is a novel form of plasticity to change the strength of synaptic transmission.

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Section: Regulation Of Somatodendritic Release During Lactationmentioning

confidence: 99%

Somatodendritic Secretion in Oxytocin Neurons Is Upregulated during the Female Reproductive Cycle

Kock¹,

Wierda²,

Bosman³

et al. 2003

J. Neurosci.

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“…Since there are major morphological changes in the SON during lactation, including an increase in the number of synapses and an increase in neurone-toneurone appositions (see Theodosis et al 1986a), we looked to see if the increases in [K+]. induced by antidromic stimulation were different in virgin and lactating rats.…”

Section: Differences Between Virgin and Lactating Ratsmentioning

confidence: 99%

“…10A, lies along the floor of the hypothalamus; it is up to about 250 ,um by 400 ,um in the coronal plane and 2 mm long. It contains, in roughly equal numbers, the cell bodies of vasopressin cells and oxytocin cells, named after the hormones that they secrete from their axon terminals in the neurohypophysis (Rhodes, Morrell & Pfaff, 1981; Theodosis, Chapman, Montagnese, Poulain & Morris, 1986a). The oxytocin neurones, whose cell bodies are distributed singly and in small clusters through the SON, are involved in the milk ejection reflex.…”

Section: Introductionmentioning

confidence: 99%

“…During the period from parturition to weaning, when there are extensive morphological changes in the SON, there is an increase in the number and areas of these appositions, where glial processes are absent over areas of up to 20 ,m in diameter and the surface membranes of oxytocin cells directly face other oxytocin cells across an extracellular cleft of apparently normal width ( Fig. lOB; Theodosis et al 1986a). Since glial cells in some tissues are known to clear excess [K+]o (see Orkand, 1986), their absence over these areas might result in unusual changes in [K+]0.…”

Section: Introductionmentioning

confidence: 99%

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Extracellular K+ in the supraoptic nucleus of the rat during reflex bursting activity by oxytocin neurones.

Coles

Poulain

1991

The Journal of Physiology

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SUMMARY1. We have investigated changes in extracellular potassium concentration [K+]o in the supraoptic nucleus of lactating rats and in particular those that occur during the intense burst of firing by the oxytocin neurones involved in the milk ejection reflex.2. Double-barrelled K+-selective microelectrodes containing a highly selective sensor based on valinomycin were lowered through the exposed cortex towards the supraoptic nucleus (SON) of female rats anaesthetized with urethane. The mean resting [K+]o in the hypothalami of five rats was 2-4 mM, S.D. = 0-3 mM.

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“…The most striking feature of such an anatomical reorganization is a pronounced and specific reduction of astrocytic coverage of OT neurons and their synapses, a remodeling that does not affect the VP system Theodosis et al, 1986). Analysis of synaptic transmission in the SON of lactating and dehydrated rats demonstrated that such an anatomical modification of the glial environment of OT neurons leads to increased levels of ambient glutamate, presumably resulting from a deficient transport of the excitatory amino acid (Oliet et al, 2001;Boudaba et al, 2003).…”

Section: Glia-dependent Switch In Gluk1 Activity In Lactating Ratsmentioning

confidence: 99%

Glia-Dependent Switch of Kainate Receptor Presynaptic Action

Bonfardin

Fossat²,

Theodosis³

et al. 2010

J. Neurosci.

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Presynaptic kainate receptors (KARs) exert a modulatory action on transmitter release. This effect can be switched from facilitation to inhibition by an increased concentration of KAR agonists. We here report that activation of presynaptic GluK1-containing KARs facilitates GABA release on oxytocin and vasopressin neurons in the supraoptic nucleus of the hypothalamus. Increase in ambient levels of glutamate associated with the physiological reduction of astrocytic coverage of oxytocin neurons in lactating rats switches this KARmediated facilitation to inhibition of GABAergic transmission. This effect was reproduced in both oxytocin and vasopressin neurons of virgin rats when glutamate transporters were blocked pharmacologically, thereby establishing that enhanced levels of extracellular glutamate induce the switch in KAR-mediated action. The facilitation of GABA release was inhibited with philanthotoxin, a Ca 2ϩ -permeable KAR antagonist, suggesting that this effect was associated with an ionotropic mode of action. Conversely, KAR-mediated inhibition was compromised in the presence of U73122, a phospholipase C inhibitor, in agreement with the involvement of a metabotropic pathway. We thus reveal that physiological astrocytic plasticity modifies the mode of action of presynaptic KARs, thereby inversing their coupling with GABA release.

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Structural plasticity in the hypothalamic supraoptic nucleus at lactation affects oxytocin-, but not vasopressin-secreting neurones

Cited by 165 publications

References 23 publications

Somatodendritic Secretion in Oxytocin Neurons Is Upregulated during the Female Reproductive Cycle

Somatodendritic Secretion in Oxytocin Neurons Is Upregulated during the Female Reproductive Cycle

Extracellular K+ in the supraoptic nucleus of the rat during reflex bursting activity by oxytocin neurones.

Glia-Dependent Switch of Kainate Receptor Presynaptic Action

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