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Dissociated central and peripheral release of vasopressin, but not oxytocin, in response to repeated swim stress: New insights into the secretory capacities of peptidergic neurons
Abstract
To investigate the effects of an ethologically-relevant stressor on central and peripheral release of arginine vasopressin and oxytocin, we forced adult male Wistar rats to swim for 10 min and simultaneously measured the release of the two peptides (i) within the hypothalamic supraoptic and paraventricular nuclei (by means of the microdialysis technique) and (ii) into the blood (by chronically-implanted jugular venous catheters). Forced swimming caused a significant rise in the release of arginine vasopressin and oxytocin within both the supraoptic nuclei (four-fold and three-fold, respectively) and the paraventricular nuclei (three-fold and four- to five-fold, respectively). Release patterns measured before, during and after repeated stress exposure on three consecutive days indicated that, at the level of the hypothalamus, the two neuropeptides are critically involved in the rats' stress response in a peptide-, locus- and stress-specific manner. Particularly, despite a general reduction of the recovery of the microdialysis probes over the time, the release of arginine vasopressin within the paraventricular nuclei and of oxytocin within the supraoptic nuclei tended to increase upon repeated stress exposure. Measurement of plasma peptide concentrations revealed that the central release of oxytocin was accompanied by a secretion of this peptide into the systemic circulation. In contrast, arginine vasopressin, assayed in the same plasma samples, failed to respond to the stressor. The latter finding is consistent with a dissociated release of the neuropeptide from different parts of a single neuron (soma/dendrites vs axon terminals). It provides evidence that under physiological conditions plasma hormone levels do not necessarily reflect the secretory activity of central components of the respective neuropeptidergic system.
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In the citing paper
“Stress affects both central and peripheral secretion of oxytocin-but while swim stress in rats increases oxytocin release in the hypothalamus and into plasma (82), novelty stress increases CSF but not plasma concentrations (83).”
From Intranasal Oxytocin: Myths and Delusions (2016) · cites this paper as [82]
In the citing paper
“Because the links between central and peripheral OT are not fully understood, it is not clear whether plasma levels reflect central activity of the system, although studies in both humans and animals point to coordination between central and peripheral levels (Burri et al., 2008; Wotjak et al., 1998).”
From Oxytocin during the initial stages of romantic attachment: Relations to couples’ interactive reciprocity (2012) · cites this paper as Wotjak et al., 1998
In the citing paper
“From the functional side, Wotjak et al. (1998) demonstrated that peripheral and central concentrations of oxytocin are simultaneously raised during forced swimming stress, suggesting a coordinated release of oxytocin into central and peripheral areas.”
From Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review (2014) · cites this paper as Wotjak et al., 1998
In the citing paper
“Indeed, although rodent studies show oxytocin release in response to non-social stressors (e.g., Wotjak et al., 1998), few human—or non-human primate—studies have done so (see Sanders et al., 1990).”
From Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review (2014) · cites this paper as Wotjak et al., 1998
In the citing paper
“Although the relationship between central and peripheral OT levels is not fully understood, both animal (29,66) and recent human (39) studies suggest that central and peripheral activity of the oxytocinergic system is coordinated.”
From Oxytocin and the development of parenting in humans (2010) · cites this paper as [66]
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Metadata
- Authors
- Wotjak, C. T., Ganster, J., Kohl, G., Holsboer, F., Landgraf, R., & Engelmann, M.
- Affiliations
- Max Planck Society (DE)
- Max Planck Institute of Psychiatry (DE)
- Corresponding author
- Engelmann, M.
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 1998-08
- Volume
- 85
- Issue
- 4
- Pages
- 1209-1222
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W1999753672
- Cited by
- 345
- References
- 70
- Citations by year
- 2026: 1 · 2024: 3 · 2023: 8 · 2022: 9 · 2021: 10 · 2020: 12 · 2019: 18 · 2018: 17 · 2017: 15 · 2016: 15 · 2015: 16 · 2014: 16 · 2013: 17 · 2012: 18
- FWCI
- 18.68
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Max Planck Institute for Plasma Physics (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- vasopressin, oxytocin, forced swim stress, repeated stress exposure, supraoptic nucleus, hypothalamic paraventricular nucleus, neuropeptide release, plasma hormone levels, peptidergic neurons, stress response
- MeSH terms
- Animals, Central Nervous System, Corticosterone, Corticotropin-Releasing Hormone, Male, Neurons, Neuropeptides, Osmolar Concentration, Oxytocin, Peripheral Nerves, Stress, Psychological, Swimming, Vasopressins, Rats, Wistar, Microdialysis, Lactic Acid, Rats
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