Cyclic Regulation of Sensory Perception by a Female Hormone Alters Behavior

Dey, Sandeepa; Chamero, Pablo; Pru, James K.; Chien, Ming-Shan; Ibarra-Soria, Ximena; Spencer, Kathryn R.; Logan, Darren W.; Matsunami, Hiroaki; Peluso, John J.; Stowers, Lisa

doi:10.1016/j.cell.2015.04.052

Cited by 170 publications

(175 citation statements)

References 37 publications

(72 reference statements)

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“…One possible mechanism is to alter sensory inputs to the MeA, at the levels of the VNO and AOB. Indeed, a number of studies have shown that responses of VNO sensory neurons can be modulated by hormones, internal status, and sensory experience in a sex-specific manner (Dey et al, 2015; Halem et al, 2001; Tachikawa et al, 2013; Xu et al, 2016). At the level of the accessory olfactory bulb, mating causes a lasting increase in baseline activity by selective regulation of local inhibition (Binns and Brennan, 2005).…”

Section: Discussionmentioning

confidence: 99%

Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice

Mathis

Grewe

et al. 2017

Cell

209

182

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SUMMARY The medial amygdala (MeA) plays a critical role in processing species- and sex-specific signals that trigger social and defensive behaviors. However, the principles by which this deep brain structure encodes social information is poorly understood. We used a miniature microscope to image the Ca2+ dynamics of large neural ensembles in awake behaving mice and tracked the responses of MeA neurons over several months. These recordings revealed spatially intermingled subsets of MeA neurons with distinct temporal dynamics. The encoding of social information in the MeA differed between males and females and relied on information from both individual cells and neuronal populations. By performing long-term Ca2+ imaging across different social contexts, we found that sexual experience triggers lasting and sex-specific changes in MeA activity, which, in males, involve signaling by oxytocin. These findings reveal basic principles underlying the brain’s representation of social information and its modulation by intrinsic and extrinsic factors.

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Section: Discussionmentioning

confidence: 99%

Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice

Mathis

Grewe

et al. 2017

Cell

209

182

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“…Mice are known to possess irregularities in their estrous cycle, as assessed by vaginal cytology, and are susceptible to interference by environmental and social factors, posing technical challenges not evident in the rat (33). Some of these potential factors affecting mouse reproductive cyclicity are transmitted through the olfactory system (34), a known substrate for progesterone action (35). Variability in the mouse estrous cycle is often addressed by experimental simulations of specific estrous cycle events, including pheromone-activated LH surges and hormone-activated LH surges in ovariectomized mice.…”

Section: Discussionmentioning

confidence: 99%

Rethinking progesterone regulation of female reproductive cyclicity

Kubota

Cui

Dhakal

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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The progesterone receptor (PGR) is a ligand-activated transcription factor with key roles in the regulation of female fertility. Much has been learned of the actions of PGR signaling through the use of pharmacologic inhibitors and genetic manipulation, using mouse mutagenesis. Characterization of rats with a null mutation at the Pgr locus has forced a reexamination of the role of progesterone in the regulation of the female reproductive cycle. We generated two Pgr mutant rat models, using genome editing. In both cases, deletions yielded a null mutation resulting from a nonsense frame-shift and the emergence of a stop codon. Similar to Pgr null mice, Pgr null rats were infertile because of deficits in sexual behavior, ovulation, and uterine endometrial differentiation. However, in contrast to the reported phenotype of female mice with disruptions in Pgr signaling, Pgr null female rats exhibit robust estrous cycles. Cyclic changes in vaginal cytology, uterine histology, serum hormone levels, and wheel running activity were evident in Pgr null female rats, similar to wild-type controls. Furthermore, exogenous progesterone treatment inhibited estrous cycles in wild-type female rats but not in Pgr-null female rats. As previously reported, pharmacologic antagonism supports a role for PGR signaling in the regulation of the ovulatory gonadotropin surge, a result at variance with experimentation using genetic ablation of PGR signaling. To conclude, our findings in the Pgr null rat challenge current assumptions and prompt a reevaluation of the hormonal control of reproductive cyclicity.progesterone | rat | reproductive cycles | PGR T he fundamental elements regulating the female reproductive cycle have been universally accepted for decades and include a hierarchy of control involving the hypothalamic/anterior pituitary/ ovarian axis (1,2). The hypothalamus, through its secretion of gonadotropin-releasing hormone, drives anterior pituitary production of gonadotropins [luteinizing hormone (LH) and folliclestimulating hormone (FSH)], which act on the ovaries to promote follicle development, ovulation, formation of the corpus luteum, and secretion of sex steroid hormones estrogen and progesterone. These two sex steroid hormones possess well-established actions on the female reproductive tract. At the core of the female reproductive cycle is a balance of sex steroid hormone negative and positive feedback regulation of gonadotropin secretion. Both estrogen and progesterone signaling pathways have been implicated in feedback control of gonadotropins and regulation of the female reproductive cycle (3-5). These concepts have been reinforced through phenotypic examination of mice possessing null mutations at either Esr1 or Pgr loci (6-8), and through the use of pharmacologic inhibitors of estrogen and progesterone signaling. Esr1 and Pgr encode the estrogen receptor 1 (also referred to as ER alpha) and progesterone receptor, respectively. These two nuclear receptors mediate many of the actions of estrogen and progesterone on the fe...

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“…For example, ovulating female mice release pheromones to attract males (Haga-Yamanaka et al, 2014), and juvenile females lacking mature gametes release a peptide pheromone to inhibit male courtship behavior (Ferrero et al, 2013). In addition, the ability of female mice to detect attractive male pheromones depends on the ovulation status signaled by a sex hormone (Dey et al, 2015). Similarly, in Drosophila melanogaster only sexually mature females produce 7,11-heptacosadiene (Arienti et al, 2010; Bilen et al, 2013), an aphrodisiac pheromone that promotes male courtship (Antony et al, 1985; Billeter et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

Hormonal Modulation of Pheromone Detection Enhances Male Courtship Success

Lin

Cao

Sethi

et al. 2016

Neuron

106

181

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SUMMARY During the lifespans of most animals, reproductive maturity and mating activity are highly coordinated. In Drosophila melanogaster, for instance, male fertility increases with age and older males are known to have a copulation advantage over young ones. The molecular and neural basis of this age-related disparity in mating behavior is unknown. Here we show that the Or47b odorant receptor is required for the copulation advantage of older males. Notably, the sensitivity of Or47b neurons to a stimulatory pheromone, palmitoleic acid, is low in young males but high in older ones, which accounts for older males’ higher courtship intensity. Mechanistically, this age-related sensitization of Or47b neurons requires a reproductive hormone, juvenile hormone, as well as its binding protein Methoprene-tolerant in Or47b neurons. Together, our study identifies a direct neural substrate for juvenile hormone that permits coordination of courtship activity with reproductive maturity to maximize male reproductive fitness.

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Cyclic Regulation of Sensory Perception by a Female Hormone Alters Behavior

Cited by 170 publications

References 37 publications

Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice

Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice

Rethinking progesterone regulation of female reproductive cyclicity

Hormonal Modulation of Pheromone Detection Enhances Male Courtship Success

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