Dorsal CA1 lesions of the hippocampus impact mating tactics in prairie voles by shifting non-monogamous males’ use of space to resemble monogamous males
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ABSTRACT:
SUBMITTER: Sailer L
PROVIDER: S-EPMC10925758 | biostudies-literature | 2024 Jan
REPOSITORIES: biostudies-literature
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Project description:Despite significant evidence that opioids are involved in attachment by mediating social reward and motivation, the role of opioids in the formation of adult social attachments has not been explored. We used the socially monogamous prairie vole (Microtus ochrogaster) to explore the role of endogenous opioids in social bonding by examining partner preference formation in female prairie voles. We hypothesized that ?-opioid receptors (MORs) in the striatum have a critical role in partner preference formation. We therefore predicted that peripheral administration of an opioid receptor antagonist would inhibit partner preference formation, and more specifically, that ?-opioid selective receptor blockade within the striatum would inhibit partner preference formation. To test our hypotheses, we first administered the non-selective opioid antagonist naltrexone peripherally to females during an 18-h cohabitation with a male and later tested the female with a partner preference test (PPT). Females showed a dose schedule-dependent decrease in partner preference in the PPT, with females in the continuous dose group displaying stranger preferences. Next, we administered microinjections of the MOR selective antagonist D-Phe-Cys-Tyr-D-Trp-Arg-Thr-Pen-Thr-NH2 (CTAP) into either the nucleus accumbens shell (NAS) or the caudate-putamen (CP) immediately before a 24-h cohabitation with a male, and later tested the female with a PPT. Females receiving CTAP into the CP, but not the NAS, showed no preference in the PPT, indicating an inhibition of partner preference formation. We show here for the first time that MORs modulate partner preference formation in female prairie voles by acting in the CP.
| S-EPMC3176565 | biostudies-literature
Project description:The opiate system has long been implicated in the rewarding properties of social interactions. In particular, the μ-opioid receptor (MOR) mediates multiple forms of social attachment, including the attachment of offspring to the mother and social bonding between mates. We have previously shown that MOR in the caudate-putamen is involved in partner preference formation in monogamous prairie voles. Here, using in situ hybridization and receptor autoradiography, we mapped in detail the distribution of MOR mRNA and ligand binding in monogamous prairie vole brains and compared MOR binding density with that of promiscuous meadow vole brains. Comparison of MOR binding in these closely related species with distinctly different social behavior revealed that while the distribution of MOR is similar, prairie voles have significantly higher densities of MOR than meadow voles in a majority of regions in the forebrain, including the caudate-putamen, nucleus accumbens shell, lateral septum and several thalamic nuclei, including the anteroventral and anteromedial thalamic nuclei. These differences in MOR expression between prairie and meadow voles could potentially contribute to species differences in behavior, including social attachment.
| S-EPMC4327842 | biostudies-literature
Project description:Monogamous prairie voles (Microtus ochrogaster) form mating-based pair bonds. Although wild prairie voles rarely re-pair following loss of a partner, laboratory studies have shown that previous pairing and mating does not negate the ability to form a new partner preference. However, little is known about how prior bond experience may alter the trajectory and display of a new pair bond. In the present study, we disrupted an initial pair bond by separating partners and then varied the amount of time before a new partner was introduced. We assessed how separation time affected the stability of partner preference over time and influenced decision-making in male voles performing a head-to-head partner preference test in which they chose between the first and second partner. We found that the ability to consistently display a preference for the second partner, supplanting the initial pair bond, depended on how long the test animal was separated from their first partner. Prior bonding experience also shaped the subsequent effects of mating on partner preference. Partner preference strength was sensitive to latency to mate with the second partner but not the first partner, irrespective of separation time. These results suggest that the ability to form a consistent, strong preference for a new partner after an initial pair bond depends upon the amount of time that has passed since separation from the first partner. These results provide valuable insight into how social bonds are dynamically shaped by prior social experience and identify variables that contribute to recovery from partner loss and the ability to form a new pair bond. They also delineate a behavioral trajectory essential for future work examining the hormonal and genetic changes that enable recovery from partner loss.
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Project description:Environmental risk factors contribute to autism spectrum disorders (ASD) etiology. In particular, prenatal exposure to the highly teratogenic anticonvulsant valproic acid (VPA) significantly increases ASD prevalence. Although significant discoveries on the embryopathology of VPA have been reported, its effects on the ability to form enduring social attachment-characteristic of ASD but uncommonly displayed by rats and mice-remains unknown. We aimed to examine the effects of prenatal VPA exposure in the social, monogamous prairie voles (Microtus ochrogaster). Compared to prenatal vehicle-exposed controls, prenatal VPA-exposed prairie voles had lower body weight throughout postnatal development, engaged in fewer social affiliative behaviors in a familial context, exhibited less social interactions with novel conspecifics, and showed enhanced anxiety-like behavior. Along these behavioral deficits, prenatal VPA exposure downregulated prefrontal cortex vasopressin receptor (V1aR) and methyl CpG-binding protein 2 (MeCP2) mRNA expression, but did not alter spine density in adults. Remarkably, adult social bonding behaviors, such as partner preference formation and selective aggression, were not disrupted by prenatal VPA exposure. Collectively, these studies suggest that, in this animal model, VPA alters only certain behavioral domains such as sex-naive anxiety and affiliative behaviors, but does not alter other domains such as social bonding with opposite sex individuals.
| S-EPMC6385222 | biostudies-literature
Project description:Formation of long-term pair-bonds is a complex process, involving multiple neural circuits and is context- and experience-dependent. While laboratory studies using prairie voles have identified the involvement of several neural mechanisms, efforts to translate these findings into predictable field outcomes have been inconsistent at best. Here we test the hypothesis that inhibition of oestrogen receptor alpha (ERα) in the medial amygdala of male prairie voles would significantly increase the expression of social monogamy in the field. Prairie vole populations of equal sex ratio were established in outdoor enclosures with males bred for high levels of ERα expression and low levels of prosocial behaviour associated with social monogamy. Medial amygdala ERα expression was knocked down in half the males per population. Knockdown males displayed a greater degree of social monogamy in five of the eight behavioural indices assessed. This study demonstrates the robust nature of ERα in playing a critical role in the expression of male social monogamy in a field setting.
| S-EPMC8334872 | biostudies-literature
Project description:Traumatic events such as natural disasters, violent crimes, tragic accidents, and war, can have devastating impacts on social relationships, including marital partnerships. We developed a single prolonged stress (SPS) paradigm, which consisted of restraint, forced swimming, and ether anesthesia, to establish an animal model relevant to post-traumatic stress disorder. We applied a SPS paradigm to a monogamous rodent, the prairie vole (Microtus ochrogaster) in order to determine whether a traumatic event affects the establishment of pair bonds. We did not detect effects of the SPS treatment on anhedonic or anxiety-like behavior. Sham-treated male voles huddled with their partner females, following a 6day cohabitation, for a longer duration than with a novel female, indicative of a pair bond. In contrast, SPS-treated voles indiscriminately huddled with the novel and partner females. Interestingly, the impairment of pair bonding was rescued by oral administration of paroxetine, a selective serotonin reuptake inhibitor (SSRI), after the SPS treatment. Immunohistochemical analyses revealed that oxytocin immunoreactivity (IR) was significantly decreased in the supraoptic nucleus (SON), but not in the paraventricular nucleus (PVN), 7days after SPS treatment, and recovered 14days after SPS treatment. After the presentation of a partner female, oxytocin neurons labeled with Fos IR was significantly increased in SPS-treated voles compared with sham-treated voles regardless of paroxetine administration. Our results suggest that traumatic events disturb the formation of pair bond possibly through an interaction with the serotonergic system, and that SSRIs are candidates for the treatment of social problems caused by traumatic events. Further, a vole SPS model may be useful for understanding mechanisms underlying the impairment of social bonding by traumatic events.
| S-EPMC5226121 | biostudies-literature
Project description:In many socially monogamous species, individuals form long-term pair bonds and males mate guard females. Such behavior is thought to help secure intra-pair fertilizations, the result of intra-pair copulations (IPCs), and ensure paternity. However, socially monogamous males are also often opportunistic and seek additional mating opportunities with other females, leaving their partner unguarded. The success associated with a male's decision to seek more mates over guarding his partner might be impacted by the activity of other males, specifically the proportion of other males leaving their territories to seek extra-pair copulations (EPCs). The amount of EPC-seeking males can impact the likelihood of a given male encountering an unguarded paired female, but also of being cuckolded (losing IPCs). It remains unclear under which conditions it is optimal to stay and guard or seek EPCs. Using field data from socially monogamous prairie voles (Microtus ochrogaster) to generate parameters, we used optimal performance modeling (Monte Carlo simulations) to ask when is it most reproductively advantageous for a bonded male to seek EPCs, despite the risk of losing IPCs. We defined three types of males: exclusive mating bonded males (true residents), non-exclusive mating bonded residents (roving residents), and unpaired males (wanderers). We first modeled the success of an individual male living in a context that incorporated only true and roving residents. We next added wandering males to this model. Finally, we considered the effects of including wandering males and unpaired females in our model. For all contexts, we found that as EPC-seeking in the population increases, the potential reproductive benefit for seeking EPCs increasingly outpaces the rate of cuckolding. In other words, we observe a shift in optimal strategy from true residents to rovers among paired males. Our models also demonstrate that reproductive fitness is likely to remain constant, despite the shift toward obtaining success via EPCs over IPCs. Our results show the dynamic nature of reproductive decision-making, and demonstrate that alternative reproductive decisions yield subtle but important differences despite appearing as balanced strategies.
| S-EPMC8248529 | biostudies-literature
Project description:An Infinium microarray platform (GPL28271, HorvathMammalMethylChip40) was used to generate DNA methylation data from several tissues from prairie voles (Microtus ochrogaster). Ear, liver, and brain samples from the Cornell University prairie vole colony were collected from 48 male and female prairie voles at various life stages: neonatal (<1 month old), sub-adult (2-4 months old), mature adult (4-10 months old), and middle aged/old adult (>10 months old). The pair bonded male and female prairie voles used in our study cohabitated with their partners for several months and produced at least three generations of litters. Animals were euthanized via rapid decapitation, their tissues rapidly extracted and frozen on dry ice before being stored at -80C until further processing for genomic DNA extraction. Brains were coronally sectioned and brain regions from the pair bonding circuit (PBC) were micro-dissected and pooled for each animal. The PBC brain regions included the prefrontal cortex, nucleus accumbens, lateral septum, ventral pallidum, and medial amygdala, and ventral tegmental area. Genomic DNA was isolated and purified using the phenol-chloroform extraction and ethanol precipitation method. A total of 144 tissue samples were collected and processed for DNA methylation analysis. Tissues: Brain, Ear, Liver
2023-08-07 | GSE174758 | GEO
Project description:Loss of a partner can have severe effects on mental health. Here we explore the neural mechanisms underlying increased passive stress-coping, indicative of depressive-like behavior, following the loss of the female partner in the monogamous male prairie vole. We demonstrate that corticotropin-releasing factor receptor 2 (CRFR2) in the nucleus accumbens shell mediates social loss-induced passive coping. Further, we show that partner loss compromises the oxytocin system through multiple mechanisms. Finally, we provide evidence for an interaction of the CRFR2 and oxytocin systems in mediating the emotional consequences of partner loss. Our results suggest that chronic activation of CRFR2 and suppression of striatal oxytocin signaling following partner loss result in an aversive emotional state that may share underlying mechanisms with bereavement. We propose that the suppression of oxytocin signaling is likely adaptive during short separations to encourage reunion with the partner and may have evolved to maintain long-term partnerships. Additionally, therapeutic strategies targeting these systems should be considered for treatment of social loss-mediated depression.
| S-EPMC4698175 | biostudies-literature
Project description:Pair bonds powerfully modulate health, which becomes particularly important when facing the detrimental effects of aging. To examine the impact of aging on relationship formation and response to loss, we examined behavior in naive 6-, 12-, and 18-month male and female prairie voles, a monogamous species that forms mating-based pair bonds. We found that older males (18-months) bonded quicker than younger voles, while similarly aged female voles increased partner directed affiliative behaviors. Supporting sex differences in bonding behaviors, we found that males were more likely to sample both partner and stranger voles while females were more likely to display partner preference during the initial 20 min of the test. We also found that male voles of all ages show enduring bonding behavior despite four weeks of partner separation while females show an overall decrease in partner-directed affiliation, including an erosion of partner preference in 12-month females. Finally, we found that the number of oxytocin, but not vasopressin, cells in the paraventricular hypothalamus increased at 18 months of age. These results establish prairie voles as a novel model to study the effects of normal and abnormal aging on pair bonding.
| S-EPMC11602381 | biostudies-literature