Periodic Remodeling in a Neural Circuit Governs Timing of Female Sexual Behavior

Inoue, Shuichiro; Yang, Renzhi; Tantry, Adarsh; Davis, Chung-ha O.; Yang, Taehong; Knoedler, Joseph R.; Wei, Yichao; Adams, Eliza L.; Thombare, Shivani; Golf, Samantha Rose; Neve, Rachael L.; Tessier‐Lavigne, Marc; Ding, Jun; Shah, Nirao M.

doi:10.1016/j.cell.2019.10.025

Cited by 97 publications

(110 citation statements)

References 93 publications

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“…For example, Golgi associated olfactory signaling regulator (GFY), which is expressed in both the VNO and the main olfactory epithelium (MOE) throughout development in mice (Kaneko-Goto et al 2013); or receptor transporter protein 2 (RTP2), which enhances the response of olfactory receptors (OR) and previously reported to be specific of olfactory neurons (Saito et al 2004). Furthermore, two prolactin and one androgen related-genes were also VNO-specific, but no other reproductive-related genes were found, which is consistent with the well-known expression of these genes in endocrine tissues and neural circuits (Inoue et al 2019).…”

Section: Vomeronasal-specific Gene Expressionsupporting

confidence: 85%

A comprehensive analysis of vomeronasal organ transcriptome reveals variable gene expression depending on age and function in rabbits

Villamayor¹,

Robledo

Fernandez³

et al. 2020

Preprint

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The vomeronasal organ (VNO) is a chemosensory organ specialized in the detection of pheromones and consequently the regulation of behavioural responses mostly related to reproduction. VNO shows a broad variation on its organization, functionality and gene expression in vertebrates, and although the species analyzed to date have shown very specific features, its expression patterns have only been well-characterized in mice. Despite rabbits represent a model of chemocommunication, unfortunately no genomic studies have been performed on VNO of this species to date. The capacity of VNO to detect a great variety of different stimuli suggests a large number of genes with complex organization to support this function. Here we provide the first comprehensive gene expression analysis of the rabbit VNO through RNA-seq across different sexual maturation stages. We characterized the VNO transcriptome, updating the number of the two main vomeronasal receptor (VR) families, 129 V1R and 70 V2R. Among others, the expression of transient receptor potential channel 2 (TRPC2), a crucial cation channel generating electrical responses to sensory stimulation in vomeronasal neurons, along with the specific expression of some fomyl-peptide receptors and H2-Mv genes, both known to have specific roles in the VNO, revealed a the particular gene expression repertoire of this organ, but also its singularity in rabbits. Moreover, juvenile and adult VNO transcriptome showed consistent differences, which may indicate that these receptors are tuned to fulfill specific functions depending on maturation age. We also identified VNO-specific genes, including most VR and TRPC2, thus confirming their functional association with the VNO. Overall, these results represent the genomic baseline for future investigations which seek to understand the genetic basis of behavioural responses canalized through the VNO.HIGHLIGHTSFirst description of the rabbit vomeronasal organ (VNO) transcriptomeVNO contains a unique gene repertoire depending on the speciesHigh fluctuation of the VNO gene expression reveals changes dependent on age and specific functionsMost vomeronasal-receptors (VR) and transient receptor potential channel 2 (TRPC2) genes are VNO-specificReproduction-related genes shows a wide expression pattern

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Section: Vomeronasal-specific Gene Expressionsupporting

confidence: 85%

A comprehensive analysis of vomeronasal organ transcriptome reveals variable gene expression depending on age and function in rabbits

Villamayor¹,

Robledo

Fernandez³

et al. 2020

Preprint

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“…Our results also reveal striking effects of aggression training on dendritic spine morphology among VMHvl Esr1 neurons, although we cannot be certain whether the secondary dendritic branches where we observe this phenomenon receive synaptic input from AHiPM. Other recent studies have identified structural plasticity among VMHvl PR -derived axons innervating hypothalamic targets in females, which are mediated by changes in sex steroids during estrus (128). The present work, together with these other studies, begins to provide a view of the acute and dynamic changes that can between 1 st and 2 nd pulse, P = 0.3587 between 1 st and 3 rd pulse, P = 0.0028 between 1 st and 4 th pulse, and P = 0.0009 between 1 st and 5th pulse).…”

Section: Discussionmentioning

confidence: 99%

Experience-dependent plasticity in an innate social behavior is mediated by hypothalamic LTP

Stagkourakis

Spigolon

Liu

et al. 2020

Preprint

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All animals can perform certain survival behaviors without prior experience, suggesting a “hard wiring” of underlying neural circuits. Experience, however, can alter the expression of innate behaviors. Where in the brain and how such plasticity occurs remains largely unknown. Previous studies have established the phenomenon of “aggression training,” in which the repeated experience of winning successive aggressive encounters across multiple days leads to increased aggressiveness. Here we show that this procedure also leads to long-term potentiation (LTP) at an excitatory synapse, derived from the Anterior Hippocampus/Posterior Medial amygdala (AHiPM), onto estrogen receptor 1-expressing (Esr1+) neurons in the ventrolateral subdivision of the ventromedial hypothalamus (VMHvl). We demonstrate further that the optogenetic induction of such LTP in vivo facilitates, while optogenetic long-term depression (LTD) diminishes, the behavioral effect of aggression training, implying a causal role for potentiation at AHiPM➔VMHvlEsr1 synapses in mediating the effect of this training. Interestingly, ∼25% of inbred C57BL/6 mice fail to respond to aggression training. We show that these individual differences are correlated both with lower levels of testosterone, relative to mice that respond to such training, and with a failure to exhibit LTP in vivo after aggression training. Administration of exogenous testosterone to such non-aggressive mice restores both behavioral and physiological plasticity in vivo. Together, these findings reveal that LTP at a hypothalamic circuit node mediates a form of experience-dependent plasticity in an innate social behavior, and a potential hormone-dependent basis for individual differences in such plasticity among genetically identical mice.Significance StatementModification of instinctive behaviors occurs through experience, yet the mechanisms through which this happens have remained largely unknown. Recent studies have shown that potentiation of aggression, an innate behavior, can occur through repeated winning of aggressive encounters. Here we show that synaptic plasticity at a specific excitatory input to a hypothalamic cell population is correlated with, and required for, the expression of increasingly higher levels of aggressive behavior following successful aggressive experience. We additionally show that the amplitude and persistence of long-term potentiation at this synapse are influenced by serum testosterone, administration of which can normalize individual differences among genetically identical inbred mice, in the expression of intermale aggression.

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“…With advances in genetic access to specific cell types, progesterone receptor-expressing neurons in the VMHvl (VMHvl PR ) have emerged as particularly essential for female sexual behavior ( 156 ). Recently, Inoue et al described a VMHvl PR →anteroventral periventricular nucleus (AVPV) circuit which is necessary for female receptivity and exhibits structural remodeling across the estrous cycle ( 157 ). Female VMHvl PR neurons are preferentially active during mating and when investigating males.…”

Section: Medial Hypothalamic Centersmentioning

confidence: 99%

Neural and Hormonal Control of Sexual Behavior

Jennings

Lecea

2020

Endocrinology

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Gonadal hormones contribute to the sexual differentiation of brain and behavior throughout the lifespan, from initial neural patterning to ‘activation’ of adult circuits. Sexual behavior is an ideal system in which to investigate the mechanisms underlying hormonal activation of neural circuits. Sexual behavior is a hormonally regulated, innate social behavior found across species. Although both sexes seek out and engage in sexual behavior, the specific actions involved in mating are sexually dimorphic. Thus, the neural circuits mediating sexual motivation and behavior in males and females are overlapping yet distinct. Furthermore, sexual behavior is strongly dependent on circulating gonadal hormones in both sexes. There has been significant recent progress on elucidating how gonadal hormones modulate physiological properties within sexual behavior circuits with consequences for behavior. Therefore, in this mini-review we review the neural circuits of male and female sexual motivation and behavior from initial sensory detection of pheromones to the extended amygdala and on to medial hypothalamic nuclei and reward systems. We also discuss how gonadal hormones impact the physiology and functioning of each node within these circuits. By better understanding the myriad of ways in which gonadal hormones impact sexual behavior circuits, we can gain a richer and more complete appreciation for the neural substrates of complex behavior.

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Periodic Remodeling in a Neural Circuit Governs Timing of Female Sexual Behavior

Abstract: Highlights d Projection termini of female Pvl neurons in AVPV increase during estrus d Estrogen triggers the increase of Pvl projection termini in AVPV d This structural plasticity increases functional connectivity between Pvl and AVPV

Cited by 97 publications

References 93 publications

A comprehensive analysis of vomeronasal organ transcriptome reveals variable gene expression depending on age and function in rabbits

A comprehensive analysis of vomeronasal organ transcriptome reveals variable gene expression depending on age and function in rabbits

Experience-dependent plasticity in an innate social behavior is mediated by hypothalamic LTP

Neural and Hormonal Control of Sexual Behavior

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