scholarly journals Prolonged partner separation erodes nucleus accumbens transcriptional signatures of pair bonding in male prairie voles

2021 ◽  
Author(s):  
Julie M Sadino ◽  
Xander G Bradeen ◽  
Conor J Kelly ◽  
Deena M Walker ◽  
Zoe R Donaldson
Keyword(s):  
Nucleus Accumbens ◽  
Pair Bond ◽  
Pair Bonding ◽  
Partner Preference ◽  
Same Sex ◽  
Prairie Voles ◽  
Pair Bonds ◽  
Transcriptional Changes ◽  
Opposite Sex ◽  
Over Time

The loss of a spouse is often cited as the most traumatic event in a person's life. However, for most people, the severity of grief and its maladaptive effects subside over time via an understudied adaptive process. Like humans, socially monogamous prairie voles (Microtus ochrogaster) form opposite-sex pair bonds, and upon partner separation, show behavioral and neuroendocrine stress phenotypes that diminish over time. Eventually, they can form a new bond, a key indicator of adapting to the loss of their partner. Thus, prairie voles provide an ethologically-relevant model for examining neuromolecular changes that emerge following partner separation for adapting to loss. Here, we test the hypothesis that extended partner separation diminishes pair bond-associated behaviors (partner preference and selective aggression) and causes pair bond transcriptional signatures to erode. Pairs were cohoused for 2 weeks and then either remained paired or were separated for 48hrs or 4wks before collecting fresh nucleus accumbens tissue for RNAseq. In a separate cohort, we assessed partner preference and selective aggression at these time points. Surprisingly, pair bond-associated behaviors persist despite prolonged separation and are similar between same-sex and opposite-sex paired voles. In contrast, we found that opposite-sex pair bonding, as compared with same-sex pairing, led to changes in accumbal transcription that were stably maintained as long as animals remained paired but eroded following prolonged partner separation. Eroded genes are primarily associated with gliogenesis and myelination, suggesting a previously undescribed role for glia in maintaining pair bonds and adapting to partner loss. We further reasoned that relevant neuronal transcriptional changes may have been masked by the prominent transcriptional signals associated with glia. Thus, we pioneered neuron-specific translating ribosomal affinity purification in voles. Neuronally-enriched transcriptional changes revealed dopaminergic-, mitochondrial-, and steroid hormone signaling-associated gene clusters whose expression patterns are sensitive to acute pair bond disruption and loss adaptation. Together, our results suggest that partner separation results in erosion of transcriptomic signatures of pair bonding despite core behavioral features of the bond remaining intact, revealing potential molecular processes central to priming a vole to be able to form a new bond.

scholarly journals How prior pair-bonding experience affects future bonding behavior in monogamous prairie voles

2020 ◽  
Author(s):  
Kelsey J. Harbert ◽  
Matteo Pellegrini ◽  
Katelyn M. Gordon ◽  
Zoe R. Donaldson
Keyword(s):  
Preference Test ◽  
Pair Bond ◽  
Valuable Insight ◽  
Partner Preference ◽  
Prairie Voles ◽  
Separation Time ◽  
Pair Bonds ◽  
Preference Strength ◽  
The Stability ◽  
Insight Into

AbstractMonogamous 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.

scholarly journals A neuronal signature for monogamous reunion

2020 ◽  
Vol 117 (20) ◽  
pp. 11076-11084 ◽  
Author(s):  
Jennifer L. Scribner ◽  
Eric A. Vance ◽  
David S. W. Protter ◽  
William M. Sheeran ◽  
Elliott Saslow ◽  
...  
Keyword(s):  
Nucleus Accumbens ◽  
Bond Strength ◽  
Bond Formation ◽  
Pair Bonding ◽  
Prairie Voles ◽  
Neuronal Dynamics ◽  
Neuronal Ensemble ◽  
Novel Approach ◽  
Over Time

Pair-bond formation depends vitally on neuromodulatory signaling within the nucleus accumbens, but the neuronal dynamics underlying this behavior remain unclear. Using 1-photon in vivo Ca2+ imaging in monogamous prairie voles, we found that pair bonding does not elicit differences in overall nucleus accumbens Ca2+ activity. Instead, we identified distinct ensembles of neurons in this region that are recruited during approach to either a partner or a novel vole. The partner-approach neuronal ensemble increased in size following bond formation, and differences in the size of approach ensembles for partner and novel voles predict bond strength. In contrast, neurons comprising departure ensembles do not change over time and are not correlated with bond strength, indicating that ensemble plasticity is specific to partner approach. Furthermore, the neurons comprising partner and novel-approach ensembles are nonoverlapping while departure ensembles are more overlapping than chance, which may reflect another key feature of approach ensembles. We posit that the features of the partner-approach ensemble and its expansion upon bond formation potentially make it a key neuronal substrate associated with bond formation and maturation.

scholarly journals Social experience alters oxytocinergic modulation in the nucleus accumbens of female prairie voles

2021 ◽  
Author(s):  
Amelie M Borie ◽  
Sena Agezo ◽  
Parker Lunsford ◽  
Arjen J Boender ◽  
Ji-Dong Guo ◽  
...  
Keyword(s):  
Nucleus Accumbens ◽  
Synaptic Transmission ◽  
De Novo ◽  
Sexual Experience ◽  
Social Experience ◽  
Oxytocin Receptor ◽  
Pair Bond ◽  
Receptor Signaling ◽  
Pair Bonding ◽  
Prairie Voles

Social relationships are dynamic and evolve with shared and personal experiences. Whether the functional role of social neuromodulators also evolves with experience to shape the trajectory of relationships is unknown. We utilized pair bonding in the socially monogamous prairie voles as an example of socio-sexual experience that dramatically alters behaviors displayed toward other individuals. We investigated oxytocin-dependent modulation of excitatory synaptic transmission in the nucleus accumbens as a function of pair bonding status. We found that an oxytocin receptor agonist decreases the amplitude of spontaneous Excitatory Postsynaptic Currents (EPSCs) in sexually naive virgin, but not pair-bonded, female voles, while it increases the amplitude of electrically evoked EPSCs in paired voles, but not in virgins. This oxytocin-dependent potentiation of synaptic transmission relies on the de novo coupling between oxytocin receptor signaling and endocannabinoid CB1 receptor signaling in pair bonded voles. Blocking CB1 receptors after pair bond formation increases the occurrence of a specific form of social rejection - defensive upright response - that is displayed towards the partner but not towards a novel individual. Altogether, our results demonstrate that oxytocin's action in the nucleus accumbens is changed through social experience in a way that regulates the trajectory of social interactions as the relationship with the partner unfolds, potentially promoting the maintenance of a pair bond by inhibiting aggressive responses. These results provide a mechanism by which social experience and context shift oxytocinergic signaling to impact neural and behavioral responses to social cues.

scholarly journals CRF receptors in the nucleus accumbens modulate partner preference in prairie voles

2007 ◽  
Vol 51 (4) ◽  
pp. 508-515 ◽  
Author(s):  
Miranda M. Lim ◽  
Yan Liu ◽  
Andrey E. Ryabinin ◽  
Yaohui Bai ◽  
Zuoxin Wang ◽  
...  
Keyword(s):  
Nucleus Accumbens ◽  
Partner Preference ◽  
Prairie Voles

Interpersonal Neural Synchronization during Interpersonal Touch Underlies Affiliative Pair Bonding between Romantic Couples

2020 ◽  
Author(s):  
Yuhang Long ◽  
Lifen Zheng ◽  
Hui Zhao ◽  
Siyuan Zhou ◽  
Yu Zhai ◽  
...  
Keyword(s):  
Near Infrared ◽  
Vocal Communication ◽  
Romantic Love ◽  
Pair Bonding ◽  
Romantic Couples ◽  
Functional Near Infrared Spectroscopy ◽  
Neural Synchronization ◽  
Interpersonal Touch ◽  
Pair Bonds ◽  
Opposite Sex

Abstract Interpersonal touch plays a key role in creating and maintaining affiliative pair bonds in romantic love. However, the neurocognitive mechanism of interpersonal touch in affiliative pair bonding remains unclear. Here, we hypothesized that interpersonal neural synchronization (INS) during interpersonal touch underlies affiliative pair bonding between romantic couples. To test this hypothesis, INS between heterosexual romantic couples and between opposite-sex friends was measured using functional near-infrared spectroscopy-based hyperscanning, while the pairs of participants touched or vocally communicated with each other. The results showed significantly greater INS between the mentalizing and sensorimotor neural systems of two members of a pair during interpersonal touch than during vocal communication between romantic couples but not between friends. Moreover, touch-induced INS was significantly correlated with the self-reported strength of romantic love. Finally, the results also showed that men’s empathy positively modulated the association between touch-induced INS increase and the strength of romantic love. These findings support the idea that INS during interpersonal touch underlies affiliative pair bonding between romantic couples and suggest that empathy plays a modulatory role in the neurocognitive mechanism of interpersonal touch in affiliative pair bonding.

scholarly journals Effects of Alcohol Consumption on Pair Bond Maintenance and Potential Neural Substrates in Female Prairie Voles

2019 ◽  
Vol 54 (4) ◽  
pp. 353-360 ◽  
Author(s):  
Andre T Walcott ◽  
Andrey E Ryabinin
Keyword(s):  
Drinking Water ◽  
Alcohol Consumption ◽  
Biological Effects ◽  
Intimate Partner ◽  
Partner Preference ◽  
Drinking Alcohol ◽  
Prairie Voles ◽  
Pair Bonds ◽  
Intimate Partner Relationships ◽  
Partner Relationships

Abstract Aims Discordant heavy alcohol use is a risk factor for disruption of intimate partner relationships. Modeling these relationships in prairie voles indicates that biological effects of alcohol can contribute to this risk. In particular, alcohol consumption disrupted an established preference for a female partner in male prairie voles if the partner was drinking water, but not if the partner was drinking alcohol. The current study investigated the effects of alcohol consumption on pair bonds in female prairie voles. Methods Female and male prairie voles established pair bonds during 1 week of cohabitation. Following cohabitation, females and their partners were put into mesh-divided cages where they were given access to 10% ethanol and water or only water for 1 week. Pair bonds in female prairie voles were tested using the partner preference test (PPT). Following the PPT, we examined oxytocin, vasopressin and FosB immunoreactivity across several brain regions. Results Female prairie voles consumed more alcohol if their male partner was also drinking alcohol, but not if their partner was drinking water. During PPT, females preferred their partner over a stranger, regardless of their partner’s drinking status. Alcohol consumption decreased oxytocin immunoreactivity in the paraventricular nucleus of the hypothalamus and increased FosB immunoreactivity in the centrally projecting Edinger–Westphal nucleus. Conclusions Established partner preference in female prairie voles is resistant to alcohol consumption. This finding suggests that the risk for disruption of intimate partner relationships in females is not mediated by a decreased motivation to be with their partners.

scholarly journals Mate Attentiveness, Seasonal Timing of Breeding and Long-term Pair Bonding in the House Finch (Carpodacus mexicanus)

Behaviour ◽  
2004 ◽  
Vol 141 (1) ◽  
pp. 1-13 ◽  
Author(s):  
Geoffrey Hill ◽  
Kevin McGraw
Keyword(s):  
Pair Bond ◽  
Egg Laying ◽  
Carpodacus Mexicanus ◽  
Timing Of Breeding ◽  
Pair Bonding ◽  
House Finches ◽  
Breeding Date ◽  
Pair Bonds ◽  
Term Pair

AbstractIn seasonally breeding birds, natural selection favors individuals that begin breeding earlier in a year because they produce more or higher quality offspring than those that begin breeding later. Among the factors that influence the timing of breeding, which include the age, health, competitive ability, or mate quality of individuals, is the longevity of the pair bond, with birds that remain mated across years initiating breeding earlier in the season than newly formed pairs. The behavioural interactions between pair members that may facilitate long-term pair bonding and early breeding onset have infrequently been studied, however. Here we report the relationship between male-female affiliative behaviour, pair-bond duration, and breeding date in house finches (Carpodacus mexicanus), a short-lived, socially monogamous passerine species in which the duration of pair bonds is highly variable within and among seasons. Finches that initiated breeding earliest in the season were those that had bred with one another in previous years. Early breeding males from returning pairs maintained significantly closer contact with their mate during the first egg-laying period of the year than did males from late-breeding, newly formed pairs. Similarly, early-breeding females from returning pairs followed their mate more closely in nest-vicinity flights during the fertile period than females from late-breeding, newly formed pairs. These results suggest that attributes of and interactions between both pair members may help to maintain stable breeding pairs and influence the timing of breeding in seasonally nesting, short-lived songbirds. Rather than advertising for or seeking extra-pair fertilization opportunities, high-quality pairs of finches may invest heavily in their mate to secure the pair bond and ensure high intrapair reproductive success.

Familiarity and gender influence social preferences in prairie voles (Microtus ochrogaster)

1997 ◽  
Vol 75 (2) ◽  
pp. 295-301 ◽  
Author(s):  
A. Courtney DeVries ◽  
Camron L. Johnson ◽  
C. Sue Carter
Keyword(s):  
Social Preference ◽  
Social Preferences ◽  
Group Cohesion ◽  
Gonadal Hormones ◽  
Microtus Ochrogaster ◽  
Same Sex ◽  
Prairie Voles ◽  
Male And Female ◽  
Sex Preferences ◽  
Opposite Sex

The physiological mechanisms influencing group cohesion and social preferences are largely unstudied in prairie voles (Microtus ochrogaster). In nature, prairie vole family groups usually consist of an adult male and female breeding pair, one or more litters of their offspring, and occasionally unrelated adults. Pair bonds, defined by heterosexual preferences, develop in male and female prairie voles following cohabitation or mating. However, social preferences between members of the same sex also may be important to the maintenance of communal groups. In the present study we compared the development of social preferences for conspecific strangers of the same sex versus preferences for the opposite sex, and examined the effect of the gonadal status of the stimulus animal on initial social preference. The present study revealed that reproductively naive males, but not females, showed initial preferences for partners of the opposite sex. In both sexes preferences for the opposite sex were not influenced by the presence or absence of gonadal hormones. Heterosexual and same-sex preferences for a familiar individual formed following 24 h of nonsexual cohabitation in both males and females. Male and female same-sex preferences, however, were no longer stable when the stranger in the preference test was of the opposite sex to the experimental animal. The development of same-sex preferences may help to maintain group cohesion, but same-sex preferences formed by cohabitation do not withstand the challenge of an opposite-sex stranger.

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