Enhancement of the luteinising hormone surge by male olfactory signals is associated with anteroventral periventricular Kiss1 cell activation in female rats

Watanabe, Yousuke; Ikegami, Kana; Ishigaki, Ren; Ieda, Nahoko; Uenoyama, Yoshihisa; Maeda, Kei‐ichiro; Tsukamura, Hiroko; Inoue, N.

doi:10.1111/jne.12505

Cited by 22 publications

(20 citation statements)

References 57 publications

(114 reference statements)

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“…Consistent with this, a recent study in female rats (ovariectomised and implanted with preovulatory oestradiol levels) demonstrated increased AVPV and limbic (but not ARC) kisspeptin neuronal Fos expression following exposure to male-soiled bedding [33]. Furthermore, these female rats showed enhanced LH surges compared to female rats exposed to clean or female-soiled bedding, therefore providing functional relevance [33].…”

Section: Kisspeptin and Olfactionsupporting

confidence: 68%

“…Moreover, an even greater increase in RP3V kisspeptin neuronal Fos expression was observed in female wild-type mice exposed to male urinary odours (compared to female oestrous urine or control water) [32]. Consistent with this, a recent study in female rats (ovariectomised and implanted with preovulatory oestradiol levels) demonstrated increased AVPV and limbic (but not ARC) kisspeptin neuronal Fos expression following exposure to male-soiled bedding [33]. Furthermore, these female rats showed enhanced LH surges compared to female rats exposed to clean or female-soiled bedding, therefore providing functional relevance [33].…”

Section: Kisspeptin and Olfactionsupporting

confidence: 66%

“…1). Kisspeptin signalling is required for male olfactory partner preference [30], is enhanced by opposite-sex urinary odours [32,33], modulates mate preference [31], enhances auditory-reproductive behaviour [34], dampens fear responses [36], modulates anxiety [31,36,42], has antidepressant-like effects [40,44], and triggers erections [51]. Furthermore, in healthy heterosexual men, kisspeptin enhances limbic and paralimbic brain activity specifically in response to visual-evoked sexual and romantic stimuli and these enhancements correlate with behavioural measures including sexual aversion, reward, and mood [40].…”

Section: Discussionmentioning

confidence: 99%

“…This included the anterior and posterior cingulate, amygdala, thalamus, and globus pallidus, which are all implicated in romantic, maternal, and unconditional love [53][54][55][56] and consistent with structures known to be involved in kisspeptin signalling in humans [19,20] and rodents [10,15,21,23,24]. Interestingly, kisspeptins enhanced activation of the amygdala in response to bonding images correlated with improved positive mood [40], a Sexual behaviours -Enhances limbic and paralimbic brain activity with correlations to reward, sexual aversion, and positive mood (H) [40] -Triggers erections (R) [51] Fear -Reduces fear responses (Z) [36][37][38]43] Social behaviours -MeA kisspeptin neurone apposition with dopaminergic and vasopressinergic neurones (R) [24] Audition -Male rodent ultrasonic vocalisations increase female ARC kisspeptin activity which correlates to the duration of female searching for male (R) [34] Mood -Antidepressant-like effects (R, H) [40,44] -Anxiolytic effects (R, Z) [31,36] -Anxiogenic effects (R) [42] Olfaction -Kisspeptin anatomical framework (R, H) [24] -Kiss1r and MeA Kiss1 roles in male olfactory partner preference (R) [30,31] -Opposite-sex urinary odours stimulate RP3V and limbic kisspeptin neurones and enhance LH surge (R) [32,33] Kisspeptin signalling potential mechanism that may contribute to the desire to bond with a partner.…”

Section: Kisspeptin and Sexual Processingmentioning

confidence: 99%

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Emerging Roles of Kisspeptin in Sexual and Emotional Brain Processing

Comninos

Dhillo

2017

Neuroendocrinology

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The emergence of kisspeptin as a crucial regulator of the hypothalamo-pituitary-gonadal (HPG) axis over the last 14 years has answered many questions as to the control of reproductive hormone secretion from the hypothalamus. More recently, the role of kisspeptin outside the HPG axis has received increasing attention in the hope of delineating the pathways linking various sensory and social behaviours to reproduction. These studies, in a range of species from zebrafish to humans, have identified a role for kisspeptin in behavioural networks related to reproduction including olfaction, audition, fear, anxiety, mood, and sexual arousal. The available evidence suggests that extrahypothalamic kisspeptin signalling encourages positive aspects of emotional and sexual brain processing in a presumed drive towards reproduction and ultimately maintenance of the species at a population level. In this review, we examine these studies, which collectively propose that kisspeptin may integrate sexual and emotional brain processing with the control of the HPG axis.

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Section: Kisspeptin and Olfactionsupporting

confidence: 68%

Section: Kisspeptin and Olfactionsupporting

confidence: 66%

Section: Discussionmentioning

confidence: 99%

Section: Kisspeptin and Sexual Processingmentioning

confidence: 99%

See 2 more Smart Citations

Emerging Roles of Kisspeptin in Sexual and Emotional Brain Processing

Comninos

Dhillo

2017

Neuroendocrinology

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“…However, the neuronal and molecular basis of processing pheromone signals appears to be sexually dimorphic. In female rats, male odours lead to activation of AVPV Kiss neurons coincident with elevated LH and increased sexual behaviour [41]. Similarly, in mice, male urine leads to the activation of AVPV Kiss neurons and increased lordosis behaviour in females [42].…”

Section: Discussionmentioning

confidence: 99%

Medial Amygdala Kiss1 Neurons Mediate Female Pheromone Stimulation of Luteinizing Hormone in Male Mice

et al. 2018

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Background/Aims: The medial amygdala (MeA) responds to olfactory stimuli and alters reproductive physiology. However, the neuronal circuit that relays signals from the MeA to the reproductive axis remains poorly defined. This study aimed to test whether MeA kisspeptin (MeA^Kiss) neurons in male mice are sensitive to sexually relevant olfactory stimuli and transmit signals to alter reproductive physiology. We also investigated whether MeA^Kiss neurons have the capacity to elaborate glutamate and GABA neurotransmitters and potentially contribute to reproductive axis regulation. Methods: Using female urine as a pheromone stimulus, MeA^Kiss neuronal activity was analysed and serum luteinizing hormone (LH) was measured in male mice. Next, using a chemogenetic approach, MeA^Kiss neurons were bi-directionally modulated to measure the effect on serum LH and evaluate the activation of the preoptic area. Lastly, using in situ hybridization, we identified the proportion of MeA^Kiss neurons that express markers for GABAergic (Vgat) and glutamatergic (Vglut2) neurotransmission. Results: Male mice exposed to female urine showed a two-fold increase in the number of c-Fos-positive MeA^Kiss neurons concomitant with raised LH. Chemogenetic activation of MeA^Kiss neurons significantly increased LH in the absence of urine exposure, whereas inhibition of MeA^Kiss neurons did not alter LH. In situ hybridization revealed that MeA^Kiss neurons are a mixed neuronal population in which 71% express Vgat mRNA, 29% express Vglut2 mRNA, and 6% express both. Conclusions: Our results uncover, for the first time, that MeA^Kiss neurons process sexually relevant olfactory signals to influence reproductive hormone levels in male mice, likely through a complex interplay of neuropeptide and neurotransmitter signalling.

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Intrinsic links among sex, emotion, and reproduction

Yang

Comninos

Dhillo

2018

Cell. Mol. Life Sci.

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Species survival is dependent on successful reproduction. This begins with a desire to mate, followed by selection of a partner, copulation and in monogamous mammals including humans, requires emotions and behaviours necessary to maintain partner bonds for the benefit of rearing young. Hormones are integral to all of these stages and not only mediate physiological and endocrine processes involved in reproduction, but also act as neuromodulators within limbic brain centres to facilitate the expression of innate emotions and behaviours required for reproduction. A significant body of work is unravelling the roles of several key hormones in the modulation of mood states and sexual behaviours; however, a full understanding of the integration of these intrinsic links among sexual and emotional brain circuits still eludes us. This review summarises the evidence to date and postulates future directions to identify potential psycho-neuroendocrine frameworks linking sexual and emotional brain processes with reproduction.

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Enhancement of the luteinising hormone surge by male olfactory signals is associated with anteroventral periventricular Kiss1 cell activation in female rats

Cited by 22 publications

References 57 publications

Emerging Roles of Kisspeptin in Sexual and Emotional Brain Processing

Emerging Roles of Kisspeptin in Sexual and Emotional Brain Processing

Medial Amygdala <b><i>Kiss1</i></b> Neurons Mediate Female Pheromone Stimulation of Luteinizing Hormone in Male Mice

Intrinsic links among sex, emotion, and reproduction

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