Oxytocin induces morphological plasticity in the adult hypothalamo-neurohypophysial system

Theodosis, Dionysia T.; Montagnese, Catherine M.; Rodriguez, F.; Vincent, Jean‐Didier; Poulain, Daniel

doi:10.1038/322738a0

Cited by 185 publications

(84 citation statements)

References 13 publications

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“…One may speculate that this 625 slow release could alter cellular metabolism by releasing intracellular mediators or growth factors which could ulti mately affect secretion, receptor expression and/or behav ior. Indeed, there is evidence that intraperitoneal injec tion of HS causes rapid morphological changes in the SON [40], Likewise, central infusion of OT produces changes in glial arrangement, that is, a retraction in glial processes and an uncovering of synaptic elements [7], It is surprising that TTX administered into the SON reduced basal plasma VP levels and completely abolished the response to a systemic osmotic stimulus. Intraperito neal HS would be expected to increase neurosecretion from both SON [41.42] and PVN [42] neurons.…”

Section: Discussionmentioning

confidence: 99%

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Effects of Tetrodotoxin on Osmotically Stimulated Central and Peripheral Vasopressin and Oxytocin Release

Ludwig

Callahan

Morris³

1995

Neuroendocrinology

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Tetrodotoxin (TTX) was used to (1) distinguish between axonal and dendritic/ somatic release of vasopressin (VP) and oxytocin (OT) within the supraoptic nucleus (SON) and (2) to determine whether neuronal inputs trigger intranuclear peptide release in the response to osmotic stimulation. Microdialysis was used to administer TTX (10^-6 M or 10^–4M) bilaterally into the SON with simultaneous monitoring of central and peripheral peptide release and mean arterial pressure in urethane-anesthetized male rats. Osmotic stimuli were given via the microdialysis probe (1 M NaCl-artificial CSF) or injected intraperitoneally (3.5 M NaCl; 600 µl/100 g b.w.) SON perfusion with TTX did not alter basal intranuclear VP or OT release or the intranuclear peptide response to direct NaCl stimulation of the SON. However, TTX treatment abolished the effect of peripheral osmotic stimulation on central peptide release. Basal plasma peptide levels were significantly reduced by TTX, e.g. decreases of 94.8 and 75.8% for VP and OT, respectively. TTX also blocked the peripheral endocrine and cardiovascular reponses to both modes of osmotic stimulation. The TTX insensitivity of directly stimulated intranuclear release suggests non-synaptic peptide release from dendrites and/or cell bodies. The ability of TTX to abolish the central peptide response to systemic osmotic stimulation demonstrates that intranuclear release is a part of a cascade produced by osmotic activation of multisynaptic pathways.

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Section: Discussionmentioning

confidence: 99%

“…into the extracellular space of the hypothalamic supraop tic (SON) and paraventricular nuclei (PVN) [1][2][3][4][5][6]. The locally released peptides may be involved in plastic neu ronal rearrangement [7], autoregulatory mechanisms [8][9][10]. autonomic regulation [3,11] and behavioral modifi cation [12].…”

Section: Introductionmentioning

confidence: 99%

Effects of Tetrodotoxin on Osmotically Stimulated Central and Peripheral Vasopressin and Oxytocin Release

Ludwig

Callahan

Morris³

1995

Neuroendocrinology

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“…PSA-NCAM can be considered, therefore, as a permissive factor to allow cells to undergo remodeling whenever the proper stimulus intervenes. In the hypothalamic magnocellular nuclei, one such stimulus is oxytocin itself because its intracerebroventricular application in normal animals induced morphological changes similar to those observed under physiological stimulation (Theodosis et al, 1986). In other neuronal systems capable of similar morphological remodeling (for review, see Theodosis and Poulain, 1993) and which also express PSA-NCAM (Bonfanti et al, 1992), other inductive factors must intervene.…”

Section: Discussionmentioning

confidence: 99%

Cell Surface Expression of Polysialic Acid on NCAM Is a Prerequisite for Activity-Dependent Morphological Neuronal and Glial Plasticity

et al. 1999

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Polysialic acid (PSA) on the extracellular domain of the neural cell adhesion molecule (NCAM) reduces cell adhesion and is considered an important regulator of cell surface interactions. The hypothalamo-neurohypophysial system (HNS), whose glia, neurons, and synapses undergo striking, reversible morphological changes in response to physiological stimulation, expresses high levels of PSA-NCAM throughout life. Light and electron microscopic immunocytochemistry in normal rats and rats in which cell transport was blocked with colchicine showed that PSA-NCAM is expressed in both HNS neurons and glia, particularly at the level of astrocytic processes that envelop neuronal profiles and can undergo remodeling. Moreover, we confirmed that the overall levels of PSA-NCAM were not greatly altered by stimulation (lactation and chronic salt ingestion). Nevertheless, PSA is essential to morphological plasticity. Using comparative ultrastructural analysis, we found that, after specific enzymatic removal of PSA from NCAM by microinjection of endoneuraminidase close to the hypothalamic magnocellular nuclei in vivo, there was no apparent withdrawal of astrocytic processes nor any increase in synaptic contacts normally induced by lactation and dehydration. Our observations demonstrate, therefore, that expression of PSA on cell surfaces in the adult HNS is indispensable to its capacity for activity-dependent morphological neuronal-glial and synaptic plasticity. The carbohydrate PSA on NCAM can thus be considered a necessary permissive factor to allow neuronal and glial remodeling to occur whenever the proper inductive stimulus intervenes.

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“…In fine, it facilitates firing of its own neurons and therefore, neurohypophyseal release into the peripheral circulation. It is therefore not too surprising that intracerebroventricular infusion of the peptide, presumably mimicking this central release, induced neuronal-glial and synaptic changes in the SON similar to those detected under physiological stimulation (80). This particular action of central OT is receptor mediated because it can be mimicked by a close analog, 4-Th-OT, whereas peptides like VP or cholecystokinin have no effect.…”

Section: Ot Induces Morphological Plasticitymentioning

confidence: 99%

Remodeling of astrocytes, a prerequisite for synapse turnover in the adult brain? Insights from the oxytocin system of the hypothalamus

Theodosis¹,

Trailin²,

Poulain³

2006

American Journal of Physiology-Regulatory, Integrative and Comp

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Theodosis, Dionysia T., Andrei Trailin, and Dominique A. Poulain. Remodeling of astrocytes, a prerequisite for synapse turnover in the adult brain? Insights from the oxytocin system of the hypothalamus. Am J Physiol Regul Integr Comp Physiol 290: R1175-R1182, 2006; doi:10.1152/ajpregu.00755.2005.-Neurons, including their synapses, are generally ensheathed by fine processes of astrocytes, but this glial coverage can be altered under different physiological conditions that modify neuronal activity. Changes in synaptic connectivity accompany astrocytic transformations so that an increased number of synapses are associated with reduced astrocytic coverage of postsynaptic elements, whereas synaptic numbers are reduced on reestablishment of glial coverage. A system that exemplifies activity-dependent structural synaptic plasticity in the adult brain is the hypothalamo-neurohypophysial system, and in particular, its oxytocin component. Under strong, prolonged activation (parturition, lactation, chronic dehydration), extensive portions of somatic and dendritic surfaces of magnocellular oxytocin neurons are freed of intervening astrocytic processes and become directly juxtaposed. Concurrently, they are contacted by an increased number of inhibitory and excitatory synapses. Once stimulation is over, astrocytic processes again cover oxytocinergic surfaces and synaptic numbers return to baseline levels. Such observations indicate that glial ensheathment of neurons is of consequence to neuronal function, not only directly, for example by modifying synaptic transmission, but indirectly as well, by preparing neuronal surfaces for synapse turnover.NEURONS, GLIA, AND SYNAPTIC inputs are not static elements because they undergo dynamic transformations. This can take place under normal physiological conditions and highlights the adult nervous system's remarkable capacity to undergo restructuring to meet particular functional requirements. A change in the morphology of neurons, and especially of afferent inputs controlling their activity, can have important consequences on their respective functions. These modifications are often accompanied by remodeling of adjacent glia, which has further impact on neuronal activity by modifying the immediate extracellular microenvironment, thereby influencing synaptic and volume transmission.The hypothalamo-neurohypophysial system (HNS), and in particular, its oxytocinergic component, is a familiar model for this kind of morphological neuronal and glial plasticity (57,76). Oxytocin (OT) neurons accumulate in well-defined regions in the hypothalamus, the supraoptic (SON), and paraventricular (PVN) nuclei, and release OT mainly from axon terminals in the neurohypophysis to act as a neurohormone in vital functions like parturition, lactation, and osmotic regulation. Critical for this systemic secretion is the concomitant exocytotic release of the peptide from somata and dendrites of OT neurons themselves in the SON and PVN. This central release facilitates the synchronous high-frequency activity of...

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Oxytocin induces morphological plasticity in the adult hypothalamo-neurohypophysial system

Cited by 185 publications

References 13 publications

Effects of Tetrodotoxin on Osmotically Stimulated Central and Peripheral Vasopressin and Oxytocin Release

Effects of Tetrodotoxin on Osmotically Stimulated Central and Peripheral Vasopressin and Oxytocin Release

Cell Surface Expression of Polysialic Acid on NCAM Is a Prerequisite for Activity-Dependent Morphological Neuronal and Glial Plasticity

Remodeling of astrocytes, a prerequisite for synapse turnover in the adult brain? Insights from the oxytocin system of the hypothalamus

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