Hyperexcited limbic neurons represent sexual satiety and reduce mating motivation

Zhou, Xiaojuan; Li, Ang; Mi, Xue; Li, Yixuan; Ding, Zhaoyi; An, Min; Chen, Yalan; Li, Wei; Tao, Xianming; Chen, Xinfeng; Li, Ying

doi:10.1126/science.abl4038

Cited by 30 publications

(18 citation statements)

References 42 publications

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“…Activation of the glutamatergic axonal terminals from the BLA in the adlBNST increased the time spent in the open arm in the elevated plus maze test and decreased the respiratory rate in mice (Kim et al, 2013). In the posterior BNST, we also observed CR‐expressing neurons located in the ifBNST and trBNST; these subnuclei are associated with sexually dimorphic and social behaviours (Herbison, 1995; Makinson et al, 2015; Zhou et al, 2023).…”

Section: Discussionmentioning

confidence: 65%

Whole‐brain connectivity to the bed nucleus of the stria terminalis calretinin‐expressing interneurons in male mice

Zhu,

Tao,

Huang

et al. 2023

Eur J of Neuroscience

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The bed nucleus of the stria terminalis (BNST) is a neuropeptide‐enriched brain region that modulates a wide variety of emotional behaviours and states, including stress, anxiety, reward and social interaction. The BNST consists of diverse subregions and neuronal ensembles; however, because of the high molecular heterogeneity within BNST neurons, the mechanisms through which the BNST regulates distinct emotional behaviours remain largely unclear. Prior studies have identified BNST calretinin (CR)‐expressing neurons, which lack neuropeptides. Here, employing virus‐based cell‐type‐specific retrograde and anterograde tracing systems, we mapped the whole‐brain monosynaptic inputs and axonal projections of BNST CR‐expressing neurons in male mice. We found that BNST CR‐expressing neurons received inputs mainly from the amygdalopiriform transition area, central amygdala and hippocampus and moderately from the medial preoptic area, basolateral amygdala, paraventricular thalamus and lateral hypothalamus. Within the BNST, plenty of input neurons were primarily located in the oval and interfascicular subregions. Furthermore, numerous BNST CR‐expressing neuronal boutons were observed within the BNST but not in other brain regions, thus suggesting that these neurons are a type of interneuron. These results will help further elucidate the neuronal circuits underlying the elaborate and distinct functions of the BNST.

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Section: Discussionmentioning

confidence: 65%

Whole‐brain connectivity to the bed nucleus of the stria terminalis calretinin‐expressing interneurons in male mice

Zhu,

Tao,

Huang

et al. 2023

Eur J of Neuroscience

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“…Female mice avoid sexual interaction with a male animal after mating completion for hours and even days, suggesting a persistent changes in the animal’s behavior (McGill and Coughlin, 1970; Zhou et al, 2023). How the MPOA regulate this persistent change in female sexual motivation is unclear.…”

Section: Resultsmentioning

confidence: 99%

“…Reactivation of these neurons result in suppression of female sexual motivation. We propose that MPOA together with other neural substrates such as the BNST (Zhou et al, 2023), encode a negative feedback signal that sustains low sexual motivation state after the completion of mating in female mice. Here, we will further discuss how sensory inputs contribute to the mating completion response in the MPOA, how MPOA represents appetitive behavior and mating completion signal and how these neurons work in concert with other sexual behavior related hypothalamic regions.…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, artificial stimulation of the vagina or the clitoris of the female rat was further shown to induce c-Fos expression in the MPOA in a similar fashion as mating completion, indicating that at least tactile sensory input can be conveyed to this brain area (Parada et al, 2010; Pfaus et al, 1996). Ejaculation from vasectomized male animals were sufficient to suppress sexual behavior suggesting that at least chemical components from the testis is not necessary for this effect (Zhou et al, 2023). A recent study has shown that mechanical stretch induces serotonergic activity in the dorsal raphe, which resembles changes after mating completion, suggesting that stretch sensation is mediating mating completion signal to the brain (Troconis et al, 2023).…”

Section: Discussionmentioning

confidence: 99%

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Post-Mating Inhibition of Female Sexual Drive via Heterogeneous Neuronal Ensembles in the Medial Preoptic Area

Ishii,

Hashikawa,

Chea

et al. 2023

Preprint

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SUMMARYThe completion of mating acutely suppresses sexual motivation in male mice. In contrast, relatively little is known about how the completion of mating affects sexual motivation and sexual behavior in female mice. How the brain responds to completion of mating is also unclear. Here, by using self-paced mating assay, we first demonstrate that female mice show decreased sexual motivation after the completion of mating. By using brain-wide analysis of activity-dependent labeling, we next pin-pointed the medial preoptic area as a brain region strongly responding to mating completion. Furthermore, using freely movingin vivocalcium imaging to compare neural activity of inhibitory and excitatory neurons in the medial preoptic area, we revealed that a subset of neurons responds significantly and specifically to mating completion but not to appetitive or consummatory behaviors. While there were excitatory and inhibitory neurons that showed positive response to the completion of mating, the response magnitude as well as the proportion of neurons responding to the event was significantly larger in the inhibitory neuron population. Next, by unbiased classification of their responses, we also found a subpopulation of neurons that increase their activity late after the onset of the completion of mating. These neurons were all inhibitory indicating that the completion of mating induces a prolonged inhibitory activity in the medial preoptic area. Lastly, we found that chemogenetic activation of medial preoptic area neurons that respond to mating completion, but not to appetitive behaviors, was sufficient to suppress female sexual motivation. Together, our data illuminate the importance of medial preoptic area as a brain node which encodes a negative signal that sustains low sexual motivation state after the completion of mating in female mice.HighlightsFemale mice show decreased sexual motivation after mating completion.A subset of MPOA neurons respond specifically to mating completion.Mating completion evokes persistent activity in MPOA inhibitory neurons.Activation of a subset of MPOA neurons is sufficient to suppress female sexual motivation.

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“…Moreover, Piezo2 Hoxb8 females paired with C57Bl/6 males also engaged in premating behavior, including male mounting attempts (fig. S5B), but Piezo2 Hoxb8 females adopted a sit-rejection posture, preventing intromission ( 37 ). These data show that mechanosensation plays a substantial role in productive mating and exposes dimorphic need for PIEZO2 and gentle touch in sexual function.…”

Section: Severely Impaired Sexual Function In Mice Lacking Piezo2mentioning

confidence: 99%

PIEZO2 and perineal mechanosensation are essential for sexual function

Lam,

von Buchholtz,

Falgairolle

et al. 2023

Science

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Despite the potential importance of genital mechanosensation for sexual reproduction, little is known about how perineal touch influences mating. We explored how mechanosensation affords exquisite awareness of the genitals and controls reproduction in mice and humans. Using genetic strategies and in vivo functional imaging, we demonstrated that the mechanosensitive ion channel PIEZO2 (piezo-type mechanosensitive ion channel component 2) is necessary for behavioral sensitivity to perineal touch. PIEZO2 function is needed for triggering a touch-evoked erection reflex and successful mating in both male and female mice. Humans with complete loss of PIEZO2 function have genital hyposensitivity and experience no direct pleasure from gentle touch or vibration. Together, our results help explain how perineal mechanoreceptors detect the gentlest of stimuli and trigger physiologically important sexual responses, thus providing a platform for exploring the sensory basis of sexual pleasure and its relationship to affective touch.

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Hyperexcited limbic neurons represent sexual satiety and reduce mating motivation

Cited by 30 publications

References 42 publications

Whole‐brain connectivity to the bed nucleus of the stria terminalis calretinin‐expressing interneurons in male mice

Whole‐brain connectivity to the bed nucleus of the stria terminalis calretinin‐expressing interneurons in male mice

Post-Mating Inhibition of Female Sexual Drive via Heterogeneous Neuronal Ensembles in the Medial Preoptic Area

PIEZO2 and perineal mechanosensation are essential for sexual function

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