Brain Oxytocin Inhibits Basal and Stress‐Induced Activity of the Hypothalamo‐Pituitary‐Adrenal Axis in Male and Female Rats: Partial Action Within the Paraventricular Nucleus

Neumann, Inga D.; Wigger, A.; Torner, Luz; Holsboer, Florian; Landgraf, Rainer

doi:10.1046/j.1365-2826.2000.00442.x

Cited by 394 publications

(281 citation statements)

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“…The demonstration of matinginduced release of OT within the PVN points toward the possibility of direct OT effects within the PVN (13,27), a brain region integrating inputs from other stress-related brain sites and regulating anxiety (9,27,32). Also, we may consider OT diffusion to remote regions (2) after local release in the PVN, as well as mating-induced OT release from axonal terminals originating within the PVN and projecting to other brain sites, such as the amygdala.…”

Section: Discussionmentioning

confidence: 99%

“…A major site of both OT synthesis and release within the brain is the hypothalamic paraventricular nucleus (PVN) (2), a region integrating behavioral and neuroendocrine stress responses (9). In male rats and mice, OT is an important regulator of sexual function (10), of anxiety (11), and of stress-coping circuitries (12)(13)(14). Moreover, in humans, intranasal OT was recently described to promote trust (15), and to reduce the level of anxiety (16), possibly at the level of the amygdala (17).…”

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confidence: 99%

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Centrally released oxytocin mediates mating-induced anxiolysis in male rats

Waldherr

Neumann

2007

Proc. Natl. Acad. Sci. U.S.A.

240

173

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Sexual activity and mating are accompanied by a high level of arousal, whereas anecdotal and experimental evidence demonstrate that sedation and calmness are common phenomena in the postcoital period in humans. These remarkable behavioral consequences of sexual activity contribute to a general feeling of well being, but underlying neurobiological mechanisms are largely unknown. Here, we demonstrate that sexual activity and mating with a receptive female reduce the level of anxiety and increase risk-taking behavior in male rats for several hours. The neuropeptide oxytocin has been shown to exert multiple functions in male and female reproduction, and to play a key role in the regulation of emotionality after its peripheral and central release, respectively. In the present study, we reveal that oxytocin is released within the brain, specifically within the hypothalamic paraventricular nucleus, of male rats during mating with a receptive female. Furthermore, blockade of the activated brain oxytocin system by central administration of an oxytocin receptor antagonist immediately after mating prevents the anxiolytic effect of mating, while having no effect in nonmated males. These findings provide direct evidence for an essential role of an activated brain oxytocin system mediating the anxiolytic effect of mating in males.black-white box ͉ elevated plus maze ͉ paraventricular nucleus ͉ risk-taking behavior ͉ anxiety T he neuropeptide oxytocin (OT) is a well acknowledged neuromodulator/neurotransmitter of the brain regulating emotionality, stress coping, and prosocial behaviors (1-3). In females, high activity of the brain OT system has been linked to the fine-tuned regulation of parturition and milk letdown (4), to the performance of maternal behaviors (3), and to the low stress response characteristic for the peripartum period (5, 6). Importantly, behavioral and physiological actions of intracerebral OT are not limited to females, because OT synthesis, local OT release, and OT receptor binding have also been demonstrated in the male brain (2, 7, 8). A major site of both OT synthesis and release within the brain is the hypothalamic paraventricular nucleus (PVN) (2), a region integrating behavioral and neuroendocrine stress responses (9). In male rats and mice, OT is an important regulator of sexual function (10), of anxiety (11), and of stress-coping circuitries (12)(13)(14). Moreover, in humans, intranasal OT was recently described to promote trust (15), and to reduce the level of anxiety (16), possibly at the level of the amygdala (17). With respect to sexual activity, preclinical (18) and human (19) research has shown elevated OT secretion into the blood during mating behavior and orgasm, respectively. Additionally, increased OT levels have been described in the cerebrospinal fluid after mating in rats (20), which is indicative of stimulation of the OT system (21).In combination, these findings lead us to hypothesize that mating results in reduced anxiety-related behavior, possibly mediated by an elevation in local...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Centrally released oxytocin mediates mating-induced anxiolysis in male rats

Waldherr

Neumann

2007

Proc. Natl. Acad. Sci. U.S.A.

240

173

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“…Furthermore, ELS has long-lasting effects on the development of the oxytocinergic system, in which the secretion of oxytocin (OXT) inhibits both basal and stress-induced HPA axis activity (Neumann et al, 2000). Intranasal administration of OXT attenuates cortisol stress responses.…”

Section: Introductionmentioning

confidence: 99%

Amygdala–Hippocampal Connectivity Changes During Acute Psychosocial Stress: Joint Effect of Early Life Stress and Oxytocin

Fan

Pestke

Feeser

et al. 2015

Neuropsychopharmacol

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Previous evidence shows that acute stress changes both amygdala activity and its connectivity with a distributed brain network. Early life stress (ELS), especially emotional abuse (EA), is associated with altered reactivity to psychosocial stress in adulthood and moderates or even reverses the stress-attenuating effect of oxytocin (OXT). The neural underpinnings of the interaction between ELS and OXT remain unclear, though. Therefore, we here investigate the joint effect of ELS and OXT on transient changes in amygdala-centered functional connectivity induced by acute psychosocial stress, using a double-blind, randomized, placebo-controlled, within-subject crossover design. Psychophysiological interaction analysis in the placebo session revealed stress-induced increases in functional connectivity between amygdala and medial prefrontal cortex, posterior cingulate cortex, putamen, caudate and thalamus. Regression analysis showed that EA was positively associated with stress-induced changes in connectivity between amygdala and hippocampus. Moreover, hierarchical linear regression showed that this positive association between EA and stress-induced amygdala-hippocampal connectivity was moderated after the administration of intranasal OXT. Amygdala-hippocampal connectivity in the OXT session correlated negatively with cortisol stress responses. Our findings suggest that altered amygdala-hippocampal functional connectivity during psychosocial stress may have a crucial role in the altered sensitivity to OXT effects in individuals who have experienced EA in their childhood.

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“…We therefore monitored the dynamics of local oxytocin release during the maternal defense test within both the PVN and the CeA using intracerebral microdialysis. The PVN and CeA were examined because of their roles in emotional and neuroendocrine stress responses (Gray et al, 1989;Feldman and Weidenfeld, 1995; Herman and Cullinan, 1997; Neumann et al, 2000a;Vyas et al, 2003;Salome et al, 2004) including anxiety (Liebsch et al, 1995;Bale et al, 2001;Davis and Whalen, 2001), maternal behavior, and aggression (Insel and Harbaugh, 1989;Elliott et al, 2001;Lubin et al, 2003;Bosch et al, 2004). We also compared the behavioral consequences of manipulating local oxytocin actions by retrodialysis of either an oxytocin receptor antagonist or of synthetic oxytocin.…”

Section: Introductionmentioning

confidence: 99%

Brain Oxytocin Correlates with Maternal Aggression: Link to Anxiety

Bosch

Meddle²,

Beiderbeck³

et al. 2005

J. Neurosci.

379

307

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The oxytocinergic system is critically involved in the regulation of maternal behavior, which includes maternal aggression. Because aggression has been linked to anxiety, we investigated the maternal aggression and the role of brain oxytocin in lactating Wistar rats selectively bred for high anxiety-related behavior (HAB) or low anxiety-related behavior (LAB) during the 10 min maternal defense test. HAB dams displayed more maternal aggression against a virgin intruder compared with LAB dams, resulting in more defensive behavior and higher anxiety of HAB-defeated virgins. The different levels of aggression were accompanied by opposite oxytocin release patterns within the paraventricular nucleus (PVN; HAB, increase; LAB, decrease). ]OVT) into the PVN or CeA reduced maternal aggression of HAB dams, whereas infusion of synthetic oxytocin into the PVN tended to increase aggression toward the intruder in LAB dams. There were no significant differences in oxytocin receptor mRNA expression or oxytocin receptor binding between lactating HAB and LAB dams. Therefore, differences in intracerebral release patterns of oxytocin, rather than differences at the level of oxytocin receptors, are critical for the regulation of maternal aggressive behavior.

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Brain Oxytocin Inhibits Basal and Stress‐Induced Activity of the Hypothalamo‐Pituitary‐Adrenal Axis in Male and Female Rats: Partial Action Within the Paraventricular Nucleus

Cited by 394 publications

References 81 publications

Centrally released oxytocin mediates mating-induced anxiolysis in male rats

Centrally released oxytocin mediates mating-induced anxiolysis in male rats

Amygdala–Hippocampal Connectivity Changes During Acute Psychosocial Stress: Joint Effect of Early Life Stress and Oxytocin

Brain Oxytocin Correlates with Maternal Aggression: Link to Anxiety

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