Aldosterone acts upon mineralocorticoid receptors (MR) in the brain to increase blood pressure and sympathetic nerve activity but the mechanisms are still poorly understood. We hypothesized that aldosterone increases sympathetic nerve activity by upregulating the renin-angiotensin system (RAS) and oxidative stress in the brain, as it does in peripheral tissues. In Sprague-Dawley rats, aldosterone (ALDO) or vehicle (VEH) was infused for one week via an intracerebroventricular (ICV) cannula, while RU28318 (selective MR antagonist), tempol (superoxide dismutase mimetic), losartan (angiotensin type-1 receptor (AT1-R) antagonist) or VEH was infused via a second ICV cannula. After one week of ICV ALDO, plasma norepinephrine was increased and mean arterial pressure was slightly elevated, but heart rate was unchanged. These effects were ameliorated by ICV infusion of RU28318, tempol or losartan. ALDO increased gene expression of AT1-R and angiotensin converting enzyme (ACE) mRNA in hypothalamic tissue. RU28318 minimized and tempol prevented the increase in AT1-R mRNA; RU28318 prevented the increased in ACE mRNA. Losartan had no effect on AT1-R or ACE mRNA. Immunohistochemistry revealed ALDO-induced increases in dihydroethidium staining (indicating oxidative stress) and Fra-like activity (indicating neuronal excitation) in neurons of the hypothalamic paraventricular nucleus (PVN). RU28318 prevented the increases in superoxide and Fra-like activity in PVN; tempol and losartan minimized these effects. Acute ICV infusions of sarthran (AT1-R antagonist) or tempol produced greater sympatho-inhibition in ALDO-treated than VEH-treated rats. Thus, aldosterone increases key elements of brain RAS and induces oxidative stress in the hypothalamus. Aldosterone may increase sympathetic nerve activity by these mechanisms.