The DOI matches its Crossref record; 72 of the 72 references it cites were found in a registry or an index.
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.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
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]
Citations
Cites
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585
Depression: a new animal model sensitive to antidepressant treatments
PORSOLT, R. D., LE PICHON, M., & JALFRE, M. (1977) · Nature · doi:10.1038/266730a0 · Cited by 4,451
Physiological functions of glucocorticoids in stress and their relation to pharmacological actions
MUNCK, A., GUYRE, P. M., & HOLBROOK, N. J. (1984) · Endocrine Reviews · doi:10.1210/edrv-5-1-25 · Cited by 3,083
Mechanisms of stress: A dynamic overview of hormonal and behavioral homeostasis
Johnson, E. O., Kamilaris, T. C., Chrousos, G. P., & Gold, P. W. (1992) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(05)80175-7 · Cited by 899
The Role of Blood Osmolality and Volume in Regulating Vasopressin Secretion in the Rat
Dunn, F. L., Brennan, T. J., Nelson, A. E., & Robertson, G. L. (1973) · Journal of Clinical Investigation · doi:10.1172/jci107521 · Cited by 687
Vasopressinergic control of pituitary adrenocorticotropin secretion comes of age
Antoni, F. A. (1993) · Frontiers in Neuroendocrinology · doi:10.1006/frne.1993.1004 · Cited by 636
Regulation of the hypothalamic corticotropin-releasing hormone neurosecretory system
Whitnall, M. H. (1993) · Progress in Neurobiology · doi:10.1016/0301-0082(93)90035-q · Cited by 582
Dendrites of hypothalamic magnocellular neurons release neurohypophysial peptides by exocytosis
Pow, D. V., & Morris, J. F. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90091-2 · Cited by 446
Hatton, G. I. (1990) · Progress in Neurobiology · doi:10.1016/0301-0082(90)90017-b · Cited by 439
Determination of Brain Interstitial Concentrations by Microdialysis
Benveniste, H., Hansen, A. J., & Ottosen, N. S. (1989) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1989.tb07252.x · Cited by 403
Roland, B. L., & Sawchenko, P. E. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903320109 · Cited by 334
Oxytocin unlike vasopressin is a stress hormone in the rat.
Lang, R. E., Heil, J. W. E., Ganten, D., Hermann, K., Unger, T., & Rascher, W. (2008) · Neuroendocrinology · doi:10.1159/000123566 · Cited by 304
Ostrowski, N. L., Lolait, S. J., & Young, W. S. (1994) · Endocrinology · doi:10.1210/endo.135.4.7925112 · Cited by 293
Kalsbeek, A., van Heerikhuize, J. J., Wortel, J., & Buijs, R. M. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-17-05555.1996 · Cited by 275
Engelmann, M., Wotjak, C. T., Neumann, I. D., Ludwig, M., & Landgraf, R. (1996) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(95)00059-3 · Cited by 269
Reflex control of magnocellular vasopressin and oxytocin secretion
Cunningham, E. T., & Sawchenko, P. E. (1991) · Trends in Neurosciences · doi:10.1016/0166-2236(91)90032-p · Cited by 266
Pathways to the Secretion of Adrenocorticotropin: A View from the Portal*
Plotsky, P. M. (1991) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1991.tb00231.x · Cited by 259
DISTRIBUTION OF OXYTOCIN AND VASOPRESSIN IN THE RAT SUPRAOPTIC AND PARAVENTRICULAR NUCLEUS
Swaab, D. F., Nijveldt, F., & Pool, C. W. (1975) · Journal of Endocrinology · doi:10.1677/joe.0.0670461 · Cited by 254
Neumann, I., Ludwig, M., Engelmann, M., Pittman, Q. J., & Landgraf, R. (2008) · Neuroendocrinology · doi:10.1159/000126604 · Cited by 236
Wotjak, C. T., Kubota, M., Liebsch, G., Montkowski, A., Holsboer, F., Neumann, I. D., & Landgraf, R. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-23-07725.1996 · Cited by 231
Can the Pituitary Secrete Directly to the Brain? (Affirmative Anatomical Evidence)
Bergland, R. M., & Page, R. B. (1978) · Endocrinology · doi:10.1210/endo-102-5-1325 · Cited by 230
Sawchenko, P. E. (1987) · Journal of Neuroscience · doi:10.1523/jneurosci.07-04-01093.1987 · Cited by 205
GABA-Activated Chloride Channels in Secretory Nerve Endings
Zhang, S. J., & Jackson, M. B. (1993) · Science · doi:10.1126/science.8380942 · Cited by 199
Magnocellular axons in passage through the median eminence release vasopressin
Holmes, M. C., Antoni, F. A., Aguilera, G., & Catt, K. J. (1986) · Nature · doi:10.1038/319326a0 · Cited by 195
Vasopressin and oxytocin: hypothalamic modulators of the stress response: a review
Gibbs, D. M. (1986) · Psychoneuroendocrinology · doi:10.1016/0306-4530(86)90048-x · Cited by 193
Kombian, S. B., Mouginot, D., & Pittman, Q. J. (1997) · Neuron · doi:10.1016/s0896-6273(00)80971-x · Cited by 186
Oxytocin and vasopressin secretion in response to stimuli producing learned taste aversions in rats.
Verbalis, J. G., McHale, C. M., Gardiner, T. W., & Stricker, E. M. (1986) · Behavioral Neuroscience · doi:10.1037//0735-7044.100.4.466 · Cited by 171
Glucocorticoid inhibition of neurohypophysial vasopressin secretion
Raff, H. (1987) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1987.252.4.r635 · Cited by 160
Intracerebral microdialysis: II. mathematical studies of diffusion kinetics
Amberg, G., & Lindefors, N. (1989) · Journal of Pharmacological Methods · doi:10.1016/0160-5402(89)90012-0 · Cited by 156
Neumann, I. D., Koehler, E., Landgraf, R., & Summy‐Long, J. Y. (1994) · Endocrinology · doi:10.1210/endo.134.1.8275928 · Cited by 146
Oxytocin and vasopressin secretion in response to stimuli producing learned taste aversions in rats.
Verbalis, J. G., McHale, C. M., Gardiner, T. W., et al. (1986) · Behavioral Neuroscience · doi:10.1037/0735-7044.100.4.466 · Cited by 146
Lambert, R. C., Moos, F., & Richard, P. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90046-i · Cited by 132
Landgraf, R., & Ludwig, M. (1991) · Brain Research · doi:10.1016/0006-8993(91)90768-q · Cited by 125
Husain, M., Manger, W. M., ROCK, T. W., Weiss, R., & FRANTZ, A. G. (1979) · Endocrinology · doi:10.1210/endo-104-3-641 · Cited by 121
Ostrowski, N. L., Lolait, S. J., & Young, W. S. (1994) · Endocrinology · doi:10.1210/en.135.4.1511 · Cited by 119
Inhibition of the firing of vasopressin neurons by atriopeptin
Standaert, D. G., Cechetto, D. F., Needleman, P., & Saper, C. B. (1987) · Nature · doi:10.1038/329151a0 · Cited by 113
Landgraf, R. (1995) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1995.tb00754.x · Cited by 109
Tasker, J. G., & Dudek, F. E. (1993) · The Journal of Physiology · doi:10.1113/jphysiol.1993.sp019810 · Cited by 104
Simultaneous and independent release of vasopressin and oxytocin in the rat
Kasting, N. W. (1988) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y88-004 · Cited by 104
Schmidt, E. D., Binnekade, R., Janszen, A. W. J. W., & Tilders, F. J. H. (1996) · PubMed · Cited by 100
Korte, S. M., de Kloet, E. R., Buwalda, B., Bouman, S. D., & Bohus, B. (1996) · European Journal of Pharmacology · doi:10.1016/0014-2999(96)00064-7 · Cited by 97
Mason, W. T., Hatton, G. I., Ho, Y. W., Chapman, C., & Robinson, I. C. A. F. (2008) · Neuroendocrinology · doi:10.1159/000124457 · Cited by 96
Buma, P., & Nieuwenhuys, R. (1987) · Neuroscience Letters · doi:10.1016/0304-3940(87)90141-8 · Cited by 94
Hypothalamic action of atrial natriuretic factor to inhibit vasopressin secretion
Samson, W. K., Aguila, M. C., Martinović, J. V., Antunes‐Rodrigues, J., & Norris, M. (1987) · Peptides · doi:10.1016/0196-9781(87)90008-8 · Cited by 90
Schmidt, E. D., Binnekade, R., Janszen, A. W. J. W., & Tilders, F. J. H. (1996) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1996.tb00707.x · Cited by 90
Scala-Guenot, D. D., Strosser, M. T., & Richard, P. (1987) · Neuroscience Letters · doi:10.1016/0304-3940(87)90717-8 · Cited by 87
Corticosterone influences forced swim-induced immobility
Báez, M., & Volosin, M. (1994) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(94)90093-0 · Cited by 80
Patterns of ACTH Secretagog Secretion in Response to Psychological Stimuli
Romero, L. M., & Sapolsky, R. M. (1996) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1996.04441.x · Cited by 77
Engelmann, M., Ludwig, M., & Landgraf, R. (1994) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1994.tb00598.x · Cited by 76
Harbuz, M. S., Jessop, D. S., Lightman, S. L., & Chowdrey, H. S. (1994) · Brain Research · doi:10.1016/0006-8993(94)91707-8 · Cited by 72
Antoni, F. A., Fink, G., & Sheward, W. J. (1990) · Journal of Endocrinology · doi:10.1677/joe.0.1250175 · Cited by 63
Gibbs, D. M. (1985) · Endocrinology · doi:10.1210/endo-116-2-723 · Cited by 61
Sawchenko, P. E., Arias, C., & Mortrud, M. T. (1993) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1993.tb00493.x · Cited by 57
Opioid-Noradrenergic Interactions in the Neurohypophysis
Zhao, B., Chapman, C., & Bicknell, J. (2008) · Neuroendocrinology · doi:10.1159/000124984 · Cited by 55
In vitro Evidence for an Inhibitory Effect of Atrial Natriuretic Peptide on Vasopressin Release
Crandall, M. E., & Gregg, C. M. (2008) · Neuroendocrinology · doi:10.1159/000124684 · Cited by 54
Ludwig, M., Callahan, M. F., & Morris, M. (2008) · Neuroendocrinology · doi:10.1159/000127058 · Cited by 52
Inglis, W. L., & Semba, K. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960422)368:1 · Cited by 49
Ludwig, M., & Landgraf, R. (1992) · Brain Research · doi:10.1016/0006-8993(92)90685-3 · Cited by 46
Repeated microdialysis perfusions: periprobe tissue reactions and BBB permeability
de Lange, E. C. M., Danhof, M., ZURCHER, C., Boer, A. G. D., & Breimer, D. D. (1995) · Brain Research · doi:10.1016/0006-8993(95)01184-x · Cited by 43
γ-Aminobutyric acid regulation of neurohypophysial hormone secretion in male and female rats
Saridaki, E., Carter, D. A., & Lightman, S. L. (1989) · Journal of Endocrinology · doi:10.1677/joe.0.1210343 · Cited by 38
Wotjak, C. T., Kubota, M., Kohl, G., & Landgraf, R. (1996) · Brain Research · doi:10.1016/0006-8993(96)00509-4 · Cited by 32
Initiation of self-grooming in resting rats by local PVH infusion of oxytocin but not α-MSH
van Erp, A. M. M., Kruk, M. R., Semple, D. M., & Verbeet, D. W. P. (1993) · Brain Research · doi:10.1016/0006-8993(93)91494-d · Cited by 31
Suppressive Vasopressin Response to Emotional Stress.
Yagi, K. (1992) · The Japanese Journal of Physiology · doi:10.2170/jjphysiol.42.681 · Cited by 26
Landgraf, R., Kubota, M., Holsboer, F., & Wotjak, C. T. (1995) · Max Planck Institute for Plasma Physics · Cited by 25
Control of Vasopressin Release: An Old But Continuing Story
Share, L. (1996) · Physiology · doi:10.1152/physiologyonline.1996.11.1.7 · Cited by 24
Stressor-specific increase of vasopressin mRNA in paraventricular hypophysiotrophic neurons
Bartanusz, V., Aubry, J., Steimer, T. J., Baffi, J., & Kiss, J. Z. (1994) · Neuroscience Letters · doi:10.1016/0304-3940(94)90232-1 · Cited by 20
Influence of water temperature on heart rate and rectal temperature of swimming rats
Baker, M. A., & Horvath, S. M. (1964) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1964.207.5.1073 · Cited by 19
Liu, H., Wang, Y., Crofton, J. T., Funyu, T., & Share, L. (1996) · Brain Research · doi:10.1016/0006-8993(96)00054-6 · Cited by 18
McKenzie, D. N., Leng, G., & Dyball, R. E. J. (1995) · The Journal of Physiology · doi:10.1113/jphysiol.1995.sp020744 · Cited by 15
Magnusson, Å. M., & Meyerson, B. J. (2008) · Neuroendocrinology · doi:10.1159/000126585 · Cited by 13
Comparison of the Number of Vasopressin‐Producing Hypothalamic Neurons in Rats and Humans
Harding, A., Ng, J. L. F., Halliday, G. M., & Oliver, J. R. (1995) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1995.tb00801.x · Cited by 12
Horn, T. F. W., Malkinson, T. J., Pittman, Q. J., & Landgraf, R. (1994) · Birkhäuser Basel eBooks · doi:10.1007/978-3-0348-7429-8_55 · Cited by 3
Research works printed but not linked: 1
- Hermes, 1996, Inhibitory action of vasopressin on neurons of the rat hypothalamic paraventricular nucleus, Soc. Neurosci. Abstr., 22, 807.16
Cited by
Sorted by citations
The oxytocin receptor system: structure, function, and regulation
Gimpl, G., & Fahrenholz, F. (2001) · Physiological Reviews · doi:10.1152/physrev.2001.81.2.629 · Cited by 3,089
Heinrichs, M., Baumgartner, T., Kirschbaum, C., & Ehlert, U. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00465-7 · Cited by 2,091
Landgraf, R., & Neumann, I. D. (2004) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2004.05.001 · Cited by 1,059
Evoked axonal oxytocin release in the central amygdala attenuates fear response
Knobloch, H. S., Charlet, A., Hoffmann, L. C., Eliava, M., Khrulev, S., Cetin, A. H., Osten, P., Schwarz, M. K., Seeburg, P. H., Stoop, R., et al. (2012) · Neuron · doi:10.1016/j.neuron.2011.11.030 · Cited by 1,049
The oxytocin receptor: from intracellular signaling to behavior
Jurek, B., & Neumann, I. D. (2018) · Physiological Reviews · doi:10.1152/physrev.00031.2017 · Cited by 999
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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
