Summary: Male and female mice usually prefer female companions but switch to preferring males under survival stress, a new study reveals. This behavioral shift is driven by distinct brain circuits involving dopaminergic neurons in the ventral tegmental area.
Male mice show different neural pathways for female and male preferences, while females rely on altered firing patterns to mediate the switch. The researchers introduced a survival threat using a predator scent to observe these changes.
The findings shed light on how socio-sexual preferences adapt for survival and health in mammals. Understanding these neural mechanisms could inform studies on social behavior and stress responses in humans.
Key Facts
- Context-Dependent Preferences: Survival threats trigger a switch in social preferences in male and female mice.
- Distinct Neural Pathways: Male preferences rely on separate brain circuits, while females use altered neuronal firing patterns.
- Adaptive Behavior: Socio-sexual preferences are tied to survival and protective behaviors in mammals.
Source: AAAS
Male and female mice both prefer social interaction with female mice under normal conditions, but both switch to preferring males when their survival is threatened, according to a new study by Anqi Wei and colleagues.
These preferences are mediated by different neuronal circuitry in male and female mice related to dopaminergic neurons in the brain’s ventral tegmental area, the researchers found.
The findings offer a clearer picture of the underlying biology of socio-sexual preferences.
These preferences are essential for successful reproduction, but also play a significant role in protective and supportive behaviors that are vital for health and survival among mammals.
The researchers examined how socio-sexual preferences can be altered by comparing how mice interacted with and without the presence of trimethylthiazoline, a potent smell that mice respond to as a survival threat.
In male mice, neuronal projections from the ventral tegmental area go to the brain’s nucleus accumbens to mediate female socio-sexual preference, but to the medial preoptic area to mediate male preference.
In female mice, the firing pattern of neuronal projections from the ventral tegmental area to the nucleus accumbens mediates the switch to preferring male companions under survival stress.
About this social neuroscience and stress research news
Author: Science Press Package Team
Source: AAAS
Contact: Science Press Package Team – AAAS
Image: The image is credited to Neuroscience News
Original Research: Closed access.
“Sexually dimorphic dopaminergic circuits determine sex preference” by Chunxiang Zhang et al. Science
Abstract
Sexually dimorphic dopaminergic circuits determine sex preference
INTRODUCTION
Innate social behaviors are essential for survival and reproduction. Animals should make correct social decisions (e.g., when, where, how, and with whom) to reach a maximal benefit from social interactions, especially when confronted with conflicts between innate requirements and external threats.
However, how social decisions are convergently encoded by the internal-drive condition and external-environment context remains unclear.
Furthermore, the sex of a social partner is a fundamental component affecting social decision-making. Interactions with individuals of the opposite sex are vital for the innate requirements of mating and reproduction, whereas same-sex social interaction provides social support and facilitates collaboration for shared goals.
However, the neural mechanisms underlying sociosexual preference remain virtually unknown.
RATIONALE
We investigated the sociosexual preference of male and female mice under both normal conditions and when exposed to external threats. By using dual-color fiber photometry Ca2+ recordings and projection-specific chemogenetic and optogenetic manipulations of dopamine (DA) neurons in the ventral tegmental area (VTA), we defined the sexually dimorphic DA circuits responsible for the switching of sociosexual preferences.
RESULTS
Both male and female mice exhibited a preference for social interaction with females but shifted to male preference when facing survival threats mediated via different sensory pathways, such as olfaction [through testing with the stressor trimethylthiazoline (TMT)], vision (contextual fear conditioning), and auditory (cued fear conditioning), indicating the integrated encoding of social decisions in response to innate requirements and external environmental factors.
Using c-Fos staining and photometric Ca2+ recordings, we observed a strong correlation between the excitation of VTADA neurons and the switching of sexual preference when confronted with survival stress.
Chemogenetic activation of VTA dopaminergic (VTADA) neurons facilitated male preference, whereas inhibiting these neurons blocked TMT’s effects on the switching of sexual preference in both sexes, validating the critical role of VTADA neurons in orchestrating the shift in social preference.
Dual-color fiber photometry Ca2+ recordings and projection-specific chemogenetic manipulations demonstrated that sexually dimorphic alterations in VTADA circuits dictate the switching of sociosexual preference in response to external survival threats.
The competition between two VTADA pathways, representing the balance between innate requirements and external threats, was used by males to encode their sexual preferences.
VTADA projections to the nucleus accumbens (NAc) were predominant under normal conditions to promote female preference, whereas projection to the medial preoptic area (mPOA) mediated male preference in response to survival threats.
By contrast, firing-pattern alteration of the VTADA-NAc projection was utilized by females to determine their sexual preference. Female interactions were associated with stronger and faster Ca2+ transients, indicating the occurrence of phasic-like action potential (AP) firings of NAc-projecting VTADA neurons in female mice.
On the other hand, male interactions facilitated by environmental threats were correlated with Ca2+ signals exhibiting slower kinetics, reflecting the sustained tonic-like AP firings of these neurons.
Notably, the phasic firing–like optogenetic excitation of VTADA-NAc terminals resulted in larger transients of DA release, promoting female preference through the enhanced DA-D1R transmission (D1R, type 1 DA receptor).
Conversely, the tonic firing–like excitation of these terminals induced a lower sustained DA release and thus led to male preference through the predominant DA-D2R transmission (D2R, type 2 DA receptor).
CONCLUSION
Both male and female mice exhibit female preference but shift to male preference when confronted with survival threats. The sexually dimorphic alterations in VTADA circuits, including neuronal activity, DA transmission, and circuit integration, play a key role in encoding the switch of sociosexual preference in both sexes.
Our study thus introduces a neural mechanism for understanding how social decisions can be convergently determined by the balance between innate requirements and external survival threats.
