scholarly journals Emergent intra-pair sex differences and behavioral coordination in pair bonded prairie voles

2021 ◽  
Author(s):  
Liza E. Brusman ◽  
David S. W. Protter ◽  
Allison C. Fultz ◽  
Maya U. Paulson ◽  
Gabriel D. Chapel ◽  
...  

AbstractIn pair bonding animals, coordinated behavior between partners is required for the pair to accomplish shared goals such as raising young. Despite this, experimental designs rarely assess the behavior of both partners within a bonded pair. Thus, we lack an understanding of the interdependent behavioral dynamics between partners that likely facilitate relationship success. To identify intra-pair behavioral correlates of pair bonding, we used socially monogamous prairie voles, a species in which females and males exhibit both overlapping and distinct pair bond behaviors. We tested both partners using social choice and non-choice tests at short- and long-term pairing timepoints. Females developed a preference for their partner more rapidly than males, with preference driven by different behaviors in each sex. Further, as bonds matured, intra-pair behavioral sex differences and coordinated behavior emerged – females consistently huddled more with their partner than males did, and partner huddle time became correlated between partners. When animals were allowed to freely interact with a partner or a novel in sequential free interaction tests, pairs spent more time interacting together than either animal did with a novel. Pair interaction was correlated with female, but not male, behavior. Via a social operant paradigm, we found that pair-bonded females, but not males, are more motivated to access and huddle with their partner than a novel vole. Together, our data indicate that as pair bonds mature, sex differences and coordinated behavior emerge, and that these intra-pair behavioral changes are likely organized and driven by the female animal.

Endocrinology ◽  
2020 ◽  
Vol 162 (2) ◽  
Author(s):  
Meredith K Loth ◽  
Zoe R Donaldson

Abstract Pair bonds represent some of the strongest attachments we form as humans. These relationships positively modulate health and well-being. Conversely, the loss of a spouse is an emotionally painful event that leads to numerous deleterious physiological effects, including increased risk for cardiac dysfunction and mental illness. Much of our understanding of the neuroendocrine basis of pair bonding has come from studies of monogamous prairie voles (Microtus ochrogaster), laboratory-amenable rodents that, unlike laboratory mice and rats, form lifelong pair bonds. Specifically, research using prairie voles has delineated a role for multiple neuromodulatory and neuroendocrine systems in the formation and maintenance of pair bonds, including the oxytocinergic, dopaminergic, and opioidergic systems. However, while these studies have contributed to our understanding of selective attachment, few studies have examined how interactions among these 3 systems may be essential for expression of complex social behaviors, such as pair bonding. Therefore, in this review, we focus on how the social neuropeptide, oxytocin, interacts with classical reward system modulators, including dopamine and endogenous opioids, during bond formation and maintenance. We argue that an understanding of these interactions has important clinical implications and is required to understand the evolution and encoding of complex social behaviors more generally. Finally, we provide a brief consideration of future directions, including a discussion of the possible roles that glia, specifically microglia, may have in modulating social behavior by acting as a functional regulator of these 3 neuromodulatory systems.


2021 ◽  
Author(s):  
Julie M Sadino ◽  
Xander G Bradeen ◽  
Conor J Kelly ◽  
Deena M Walker ◽  
Zoe R Donaldson

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.


2004 ◽  
Vol 82 (10) ◽  
pp. 1667-1671 ◽  
Author(s):  
Nancy G Solomon ◽  
Brian Keane ◽  
Lana R Knoch ◽  
Paula J Hogan

Prairie voles (Microtus ochrogaster (Wagner, 1842)) exhibit behavioral, morphological, and neuroendocrinological traits associated with monogamy and are considered a model system to examine the biological foundations of monogamy in mammals. We examined allelic polymorphism at microsatellite loci to assess mating exclusivity in wild prairie voles sampled in east-central Illinois and found evidence of multiple paternity in five of nine litters (56%) analyzed. Thus, a female in this socially monogamous mammal with extensive mechanisms for pair bonding does not always mate solely with its partner and raises the paradox of why some pair-bonded females mate multiply.


2013 ◽  
Vol 280 (1750) ◽  
pp. 20122396 ◽  
Author(s):  
James D. Klatt ◽  
James L. Goodson

Although many species form socially monogamous pair bonds, relevant neural mechanisms have been described for only a single species, the prairie vole ( Microtus ochrogaster ). In this species, pair bonding is strongly dependent upon the nonapeptides oxytocin (OT) and vasopressin, in females and males, respectively. Because monogamy has evolved many times in multiple lineages, data from additional species are required to determine whether similar peptide mechanisms modulate bonding when monogamy evolves independently. Here we test the hypothesis that OT-like receptor activation is required for pair bond formation in the socially monogamous zebra finch ( Taeniopygia guttata ). Males and females were administered chronic intracerebroventricular infusions of saline or an OT receptor antagonist and were observed twice daily for 3 days in a colony environment. A variety of affiliative, aggressive and other behaviours were quantified. The antagonist produced significant and selective effects on pair bonding (latency to pair; number of sessions paired; stable pairing) and the associated behaviour of allopreening. Importantly, findings for males follow the trends of females; this yields main effects of treatment in two-way ANOVAs, although within-sex analyses are significant only for females. These data provide evidence for both convergent evolution and species diversity in the neuroendocrine mechanisms of pair bonding.


Author(s):  
Catherine E. Barrett ◽  
Larry J. Young

Many psychiatric illnesses, including autism spectrum disorders (ASD), schizophrenia, and depression, are characterized by impaired social cognition and a compromised ability to form social relationships. Although drugs are currently available to treat other symptoms of these disorders, none specifically target the social deficits. In order to develop pharmacotherapies to enhance social functioning, particularly for ASD where social impairment is a core symptom, we must first understand the basic neurobiology underlying complex social behaviors. The socially monogamous prairie vole (Microtus ochrogaster) has been a remarkably useful animal model for exploring the neural systems regulating complex social behaviors, including social bonding. Prairie voles form enduring social bonds between mated partners, or pair bonds, and display a biparental familial structure that is arguably very similar to that of humans. Here we discuss the neural systems underlying social bonding in prairie voles, including the neuropeptides oxytocin and vasopressin, opioids, dopaminergic reward and reinforcement, and stress-related circuitry, as well as the susceptibility of social functioning to early life experiences. We highlight some of the remarkable parallels that have been discovered in humans, and discuss how research in prairie voles has already led to novel therapies to enhance social functioning in ASD.


BMC Genomics ◽  
2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Joel A. Tripp ◽  
Alejandro Berrio ◽  
Lisa A. McGraw ◽  
Mikhail V. Matz ◽  
Jamie K. Davis ◽  
...  

Abstract Background Pair bonding with a reproductive partner is rare among mammals but is an important feature of human social behavior. Decades of research on monogamous prairie voles (Microtus ochrogaster), along with comparative studies using the related non-bonding meadow vole (M. pennsylvanicus), have revealed many of the neural and molecular mechanisms necessary for pair-bond formation in that species. However, these studies have largely focused on just a few neuromodulatory systems. To test the hypothesis that neural gene expression differences underlie differential capacities to bond, we performed RNA-sequencing on tissue from three brain regions important for bonding and other social behaviors across bond-forming prairie voles and non-bonding meadow voles. We examined gene expression in the amygdala, hypothalamus, and combined ventral pallidum/nucleus accumbens in virgins and at three time points after mating to understand species differences in gene expression at baseline, in response to mating, and during bond formation. Results We first identified species and brain region as the factors most strongly associated with gene expression in our samples. Next, we found gene categories related to cell structure, translation, and metabolism that differed in expression across species in virgins, as well as categories associated with cell structure, synaptic and neuroendocrine signaling, and transcription and translation that varied among the focal regions in our study. Additionally, we identified genes that were differentially expressed across species after mating in each of our regions of interest. These include genes involved in regulating transcription, neuron structure, and synaptic plasticity. Finally, we identified modules of co-regulated genes that were strongly correlated with brain region in both species, and modules that were correlated with post-mating time points in prairie voles but not meadow voles. Conclusions These results reinforce the importance of pre-mating differences that confer the ability to form pair bonds in prairie voles but not promiscuous species such as meadow voles. Gene ontology analysis supports the hypothesis that pair-bond formation involves transcriptional regulation, and changes in neuronal structure. Together, our results expand knowledge of the genes involved in the pair bonding process and open new avenues of research in the molecular mechanisms of bond formation.


1988 ◽  
Vol 44 (6) ◽  
pp. 691-697 ◽  
Author(s):  
C.Sue Carter ◽  
Diane M. Witt ◽  
E.Gregory Thompson ◽  
Kathy Carlstead

2005 ◽  
Vol 28 (2) ◽  
pp. 290-291 ◽  
Author(s):  
Lynn Carol Miller ◽  
William C. Pedersen ◽  
Anila Putcha-Bhagavatula

Across mammals, when fathers matter, as they did for hunter-gatherers, sex-similar pair-bonding mechanisms evolve. Attachment fertility theory can explain Schmitt's and other findings as resulting from a system of mechanisms affording pair-bonding in which promiscuous seeking is part. Departures from hunter-gatherer environments (e.g., early menarche, delayed marriage) can alter dating trajectories, thereby impacting mating outside of pair-bonds.


2020 ◽  
Author(s):  
Yuhang Long ◽  
Lifen Zheng ◽  
Hui Zhao ◽  
Siyuan Zhou ◽  
Yu Zhai ◽  
...  

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.


2019 ◽  
Vol 54 (4) ◽  
pp. 353-360 ◽  
Author(s):  
Andre T Walcott ◽  
Andrey E Ryabinin

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.


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