Gonadal Steroid Modulation of Stress-Induced Hypothalamo-Pituitary-Adrenal Activity and Anxiety Behavior: Role of Central Oxytocin

Intracerebroventricular administration of oxytocin reduces anxiety behavior and hypothalamo-pituitary-adrenal (HPA) responses to stress in female rats. Similar changes are seen in late-pregnant rats, and oxytocin-sensitive pathways may mediate these effects. This study investigated anxiety behavior...

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Bibliographic Details
Published in:Endocrinology (Philadelphia) 2006-05, Vol.147 (5), p.2423-2431
Main Authors: Windle, Richard J, Gamble, Lisa E, Kershaw, Yvonne M, Wood, Susan A, Lightman, Stafford L, Ingram, Colin D
Format: Article
Language:English
Subjects:
Adrenal Glands - pathology
Animals
Anxiety
Biological and medical sciences
Female
Fundamental and applied biological sciences. Psychology
Humans
Hypothalamus - metabolism
Hypothalamus - pathology
Ligands
Neurotransmitter Agents
Oxytocin - metabolism
Pituitary Gland - pathology
Pregnancy
Pregnancy, Animal
Progesterone - metabolism
Rats
Rats, Sprague-Dawley
Receptors, Oxytocin - metabolism
RNA, Messenger - metabolism
Steroids - metabolism
Time Factors
Vertebrates: endocrinology
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Summary:Intracerebroventricular administration of oxytocin reduces anxiety behavior and hypothalamo-pituitary-adrenal (HPA) responses to stress in female rats. Similar changes are seen in late-pregnant rats, and oxytocin-sensitive pathways may mediate these effects. This study investigated anxiety behavior and stress responses using a gonadal steroid model of late pregnancy, which is known to increase endogenous oxytocin expression. Compared with continuous progesterone treatment, 3-d withdrawal of progesterone after 11-d treatment of ovariectomized rats with estradiol and progesterone resulted in increased binding of the oxytocin receptor ligand [125I]d(CH2)5[Tyr(Me)2,Thr4,Tyr-NH29]ornithine vasotocin in selective forebrain regions, including the ventrolateral septum and ventromedial hypothalamus. Behavior in the elevated plus-maze indicated that progesterone withdrawal had an anxiolytic effect, and this was associated with lower levels of c-fos mRNA expression in the ventral hippocampus, an area previously shown to be sensitive to oxytocin. In other groups of animals, the plasma corticosterone response to a psychological stress (10 min of 114 dB white noise) was significantly attenuated by this steroid manipulation. Furthermore, simultaneous infusion of the selective oxytocin receptor antagonist desGlyNH2, d(CH2)5[Tyr(Me)2,Thr4]OVT during the period of progesterone withdrawal reversed this attenuation of noise-induced HPA activation, indicating a role for endogenous oxytocin in this effect. Thus, mimicking the steroid profile of late pregnancy leads to a reduction in anxiety behavior and attenuates HPA activity induced by mild stress. These effects appear to be mediated through the involvement of central oxytocin neurotransmission.
ISSN:0013-7227
1945-7170
DOI:10.1210/en.2005-1079