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Cited by 345Neuroendocrine regulation and behaviorStress Responses and CortisolNeuropeptides and Animal Physiology

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

Wotjak, C.T., Ganster, J., Kohl, G., Holsboer, F., Landgraf, R., Engelmann, M.·1998·Neuroscience
DOI 10.1016/s0306-4522(97)00683-0
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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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  • Stress affects both central and peripheral oxytocin secretion, but in rats swim stress increases hypothalamic and plasma oxytocin, whereas novelty stress increases CSF but not plasma oxytocin.

    “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]

  • Because the links between central and peripheral oxytocin are not fully understood, it is unclear whether plasma levels reflect central activity of the system, although studies in humans and animals point to coordination between central and peripheral levels.

    “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

  • Peripheral and central concentrations of oxytocin are simultaneously raised during forced swimming stress in rats, suggesting a coordinated release of oxytocin into central and peripheral areas.

    “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

  • Although rodent studies show oxytocin release in response to non-social stressors, few human or non-human primate studies have done so.

    “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

  • Both animal and recent human studies suggest that central and peripheral activity of the oxytocinergic system is coordinated.

    “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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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.
ORCID
Venue
Neuroscience
Publisher
Elsevier BV
Published
1998-08
Volume
85
Issue
4
Pages
1209-1222
ISSN
0306-4522 (ISSN-L)
DOI
10.1016/s0306-4522(97)00683-0
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
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Neuroscience (publishedVersion)
  • PubMed (publishedVersion)
  • Max Planck Institute for Plasma Physics (submittedVersion)
  • MPG.PuRe (Max Planck Society) (submittedVersion)
Topics
  • Social Sciences › Psychology › Social Psychology › 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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