Oxytocin Attenuates Stress-Induced c-fosmRNA Expression in Specific Forebrain Regions Associated with Modulation of Hypothalamo–Pituitary–Adrenal Activity

Richard J. Windle · Yvonne M. Kershaw · Nola M. Shanks · Stafford Louis Lightman · Colin D Ingram

407 citations0/0 files storedJournal of Neuroscience

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Neuroendocrine regulation and behavior Neuropeptides and Animal Physiology Stress Responses and Cortisol

Abstract

We reported previously that the neuropeptide oxytocin attenuates stress-induced hypothalamo-pituitary-adrenal (HPA) activity and anxiety behavior. This study sought to identify forebrain target sites through which oxytocin may mediate its anti-stress effects. Ovariectomized, estradiol-treated rats received intracerebroventricular infusions of oxytocin (1 or 10 ng/hr) or vasopressin (10 ng/hr), and the patterns of neuronal activation after restraint stress were determined by semiquantitative mapping of c-fos mRNA expression. Oxytocin administration significantly attenuated the release of ACTH and corticosterone and the increase in corticotropin-releasing factor mRNA expression in the hypothalamic paraventricular nucleus (PVN) in response to 30 min restraint. Restraint also induced the expression of c-fos mRNA in selective regions of the forebrain, including the PVN, paraventricular thalamic nucleus, habenula, medial amygdala, ventrolateral septum (LSV), most subfields of the dorsal and ventral hippocampus, and piriform and endopiriform cortices. In most cases, this level of gene expression was unaffected by concomitant administration of oxytocin. However, in the PVN, LSV, and throughout all subfields of the dorsal hippocampus, restraint evoked no detectable increase in c-fos mRNA in animals treated with either dose of oxytocin. Vasopressin had no effects on either HPA axis responses or neuronal activation in response to restraint, indicating that the effects were highly peptide selective. These data show that central oxytocin attenuates both the stress-induced neuroendocrine and molecular responses of the HPA axis and that the dorsal hippocampus, LSV, and PVN constitute an oxytocin-sensitive forebrain stress circuit.

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References

1997Central Oxytocin Administration Reduces Stress-Induced Corticosterone Release and Anxiety Behavior in Rats1 2000Brain Oxytocin Inhibits Basal and Stress‐Induced Activity of the Hypothalamo‐Pituitary‐Adrenal Axis in Male and Female Rats: Partial Action Within the Paraventricular Nucleus 2001CNS Region-Specific Oxytocin Receptor Expression: Importance in Regulation of Anxiety and Sex Behavior 1988Localization and pharmacological characterization of high affinity binding sites for vasopressin and oxytocin in the rat brain by light microscopic autoradiography

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