A comparison of the effects of male pheromone priming and optogenetic inhibition of accessory olfactory bulb forebrain inputs on the sexual behavior of estrous female mice

Abstract

Previous research has shown that repeated testing with a stimulus male is required for ovariectomized, hormone-primed female mice to become sexually receptive (show maximal lordosis quotients; LQs) and that drug-induced, epigenetic enhancement of estradiol receptor function accelerated the improvement in LQs otherwise shown by estrous females with repeated testing. We asked whether pre-exposure to male pheromones (‘pheromone priming’) would also accelerate the improvement in LQs with repeated tests and whether optogenetic inhibition of accessory olfactory bulb (AOB) projection neurons could inhibit lordosis in sexually experienced estrous female mice. In Experiment 1, repeated priming with soiled male bedding failed to accelerate the progressive improvement in LQs shown by estrous female mice across 5 tests, although the duration of each lordosis response and females’ investigation of male body parts during the first test was augmented by such priming. In Experiment 2, acute optogenetic inhibition of AOB inputs to the forebrain during freely moving behavioral tests significantly reduced LQs, suggesting that continued AOB signaling to the forebrain during mating is required for maximal lordotic responsiveness even in sexually experienced females. Our results also suggest that pheromonal stimulation, by itself, cannot substitute for the full complement of sensory stimulation received by estrous females from mounting males that normally leads to the progressive improvement in their LQs with repeated testing.

DREADD‐induced silencing of the medial amygdala reduces the preference for male pheromones and the expression of lordosis in estrous female mice

“…Sexually naïve estrous female mice initially show a surprisingly low level of lordosis when first paired with a stud male, but become progressively more receptive with repeated testing (Thompson & Edwards, ; Laroche et al ., ,b; Bonthuis et al ., ; Ismail et al ., ; McCarthy et al ., ). Our results show that the progressive improvement in LQs normally observed after repeated testing with a stud male was significantly attenuated by CNO‐induced bilateral silencing of neurons in the Me.…”

“…This previous study using rats corroborates the current finding that disrupting Me activity had little or no effect on receptivity in sexually experienced estrous female mice. Our results contrast, however, with the results of our recent study showing that acute optogenetic inhibition of activity in AOB mitral cell projections to the Me significantly reduced LQs in sexually experienced estrous female mice (McCarthy et al ., ).…”

“…This result further highlights the role of the Me in processing pheromonal stimuli that facilitate courtship behavior in female mice. Optogenetic silencing of the projection neurons from the AOB to the Me in sexually experienced females also reduced lordosis (McCarthy et al ., ). This result suggests that chemosensory inputs to the Me from the AOB are required for female mice to show full receptivity even after the prior receipt of mating experience.…”

“…Numerous previous studies found that sexually naïve estrous female mice initially show low levels of lordosis in response to male mounting, whereas progressively higher levels of receptivity are displayed over repeated test days with a stud male (Thompson & Edwards, ; Laroche et al ., ,b; Bonthuis et al ., ; Ismail et al ., ; McCarthy et al ., ). Repeated pairing with a stud male as well as s.c. injections of estradiol benzoate and progesterone in the correct sequence is required for sexually naïve ovariectomized female mice to show full blown copulatory behaviors.…”

Female Reproductive Behavior

“…Some have shown no changes in darts and lordosis behavior upon MeA lesions Clark, 2006, Kondo andSakuma, 2005), while others found increases in lordosis intensity and paracopulatory behaviors (Polston and Erskine, 2001, Masco and Carrer, 1980, Rajendren and Moss, 1993, thereby suggesting an inhibitory role of the MeA during copulation. To cause even more confusion, when the state-of-the-art technique optogenetics was used in mice to silence the specific projections from the olfactory system to the MeA, sexually experiences female mice showed reduced levels of lordosis responses (McCarthy et al, 2017a). This would suggest that chemosensory inputs from the olfactory areas are required to show full receptivity in female mice.…”