Prelimbic and infralimbic responsivity to amygdala input is modified by gonadal hormones in parallel to low anxiety-like behavior in ovariectomized rats

Abstract

Gonadal hormones may influence sexual activity by reducing anxiety. The basolateral amygdala (BLA) and prelimbic (PL) and infralimbic (IL) cortical regions comprise a loop that is related to fear, anxiety, and social behavior. In female ovariectomized rats, actions of estradiol, progesterone, and sequential estradiol and progesterone administration were explored in the open field test (OFT) and plus maze test (PMT) to evaluate signs of anxiety-like behavior. The three hormonal treatments reduced indicators of anxiety in the PMT but did not influence behavior in the OFT. In the same behaviorally tested rats under urethane anesthesia, single-unit extracellular recordings were obtained from the PL and IL during electrical stimulation of the BLA. The analysis of 250 ms peristimulus histograms showed that BLA stimulation produced two kinds of response. A small group of neurons increased their firing rate after BLA stimulation. Most neurons exhibited a reduction of spiking. Neurons that increased their firing rate after BLA stimulation did not show any difference with the hormonal treatments. In neurons that were inhibited by BLA stimulation, estradiol reduced the neuronal firing rate in the PL and IL, and progesterone alone and the sequential administration of estradiol followed by progesterone administration 24 h later (priming) increased the firing rate during the 240 ms before BLA stimulation. Analyses of responsivity of the PL and IL during electrical stimulation of the BLA indicated that estradiol, progesterone, and estradiol followed by progesterone administration 24 h later (priming) reduced inhibitory actions of the BLA on the PL but not IL. In the BLA-IL connection, progesterone exacerbated the inhibitory response. These findings indicate that anxiolytic actions of estradiol, progesterone, and estradiol followed by progesterone administration 24 h later (priming) correspond to lower BLA-PL responsivity. Actions of progesterone on BLA-IL responsivity appear to contribute to sexual activity by interacting with other forebrain structures that are also related to sexual receptivity.