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The Journal of Neuroscience, March 24, 2004, 24(12):2974-2982; doi:10.1523/JNEUROSCI.3432-03.2004

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Behavioral/Systems/Cognitive
Oxytocin Attenuates Stress-Induced c-fos mRNA Expression in Specific Forebrain Regions Associated with Modulation of Hypothalamo–Pituitary–Adrenal Activity

Richard J. Windle,^2 * Yvonne M. Kershaw,^1 * Nola Shanks,¹ Susan A. Wood,¹ Stafford L. Lightman,¹ and Colin D. Ingram^1,3

¹University Research Centre for Neuroendocrinology, University of Bristol, Bristol Royal Infirmary, Bristol BS2 8HW, United Kingdom, ²University of Nottingham, Human and Clinical Sciences Research Centre, Queen's Medical Centre, Nottingham NG7 2UH, United Kingdom, and ³School of Neurology, Neurobiology, and Psychiatry, University of Newcastle, Royal Victoria Infirmary, Newcastle upon Tyne NE1 4LP, United Kingdom

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.

Key words: oxytocin; HPA axis; ventrolateral septum; ACTH; vasopressin; paraventricular nucleus; corticosterone; amygdala; hippocampus; restraint stress; c-fos; immediate-early gene; limbic; thalamus; septum; corticotrophin-releasing factor

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Received July 22, 2003; revised December 22, 2003; accepted December 23, 2003.

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