Pair Bonding

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Zuoxin Wang - One of the best experts on this subject based on the ideXlab platform.

  • neuropeptidergic regulation of Pair Bonding and stress buffering lessons from voles
    Hormones and Behavior, 2015
    Co-Authors: Kyle L Gobrogge, Zuoxin Wang
    Abstract:

    This article is part of a Special Issue "SBN 2014". Interpersonal attachment is a critical component of the human experience. Pair-Bonding ameliorates the severity of several mental and physical diseases. Thus, a better understanding of how the central nervous system responds to and encodes social-buffering during stress is a valuable research enterprise. The prairie vole (Microtus ochrogaster), as a laboratory animal model, provides the gold standard for the investigation of the neurobiology underlying attachment. Furthermore, emerging research in voles, additional laboratory rodents, transgenic mice, primates, and humans has provided novel insight into the neurochemical mechanisms underlying the therapeutic effects of social bonds reducing anxiety, depression, and drug abuse liability. In the present review, we highlight the work from this burgeoning field and focus on the role(s) of the neuropeptides oxytocin (OT), vasopressin (AVP), and corticotrophin releasing hormone (CRH) mediating stress buffering. Together, the data suggest that OT underlies social Bonding to reduce stress-induced psychological illness while AVP and CRH facilitate arousal to enhance autonomic reactivity, increasing susceptibility to adverse mental and physical health.

  • the neurobiology of Pair Bonding insights from a socially monogamous rodent
    Frontiers in Neuroendocrinology, 2011
    Co-Authors: Kimberly A Young, Kyle L Gobrogge, Yan Liu, Zuoxin Wang
    Abstract:

    The formation of enduring relationships between adult mates (i.e., Pair bonds) is an integral aspect of human social behavior and has been implicated in both physical and psychological health. However, due to the inherent complexity of these bonds and the relative rarity with which they are formed in other mammalian species, we know surprisingly little about their underlying neurobiology. Over the past few decades, the prairie vole (Microtus ochrogaster) has emerged as an animal model of Pair Bonding. Research in this socially monogamous rodent has provided valuable insight into the neurobiological mechanisms that regulate Pair Bonding behaviors. Here, we review these studies and discuss the neural regulation of three behaviors inherent to Pair Bonding: the formation of partner preferences, the subsequent development of selective aggression toward unfamiliar conspecifics, and the bi-parental care of young. We focus on the role of vasopressin, oxytocin, and dopamine in the regulation of these behaviors, but also discuss the involvement of other neuropeptides, neurotransmitters, and hormones. These studies may not only contribute to the understanding of Pair Bonding in our own species, but may also offer insight into the underlying causes of social deficits noted in several mental health disorders.

  • anterior hypothalamic vasopressin regulates Pair Bonding and drug induced aggression in a monogamous rodent
    Proceedings of the National Academy of Sciences of the United States of America, 2009
    Co-Authors: Kyle L Gobrogge, Larry J Young, Yan Liu, Zuoxin Wang
    Abstract:

    After Pair-Bonding, male prairie voles (Microtus ochrogaster) display aggression toward novel females but not toward their female partner. Here we show that this selective aggression in Pair-bonded male prairie voles is associated with increased release of vasopressin (AVP) in the anterior hypothalamus (AH). Pharmacological activation of AVP-V1a receptors (V1aR) in the AH induced selective aggression in sexually naive males, whereas V1aR blockade diminished selective aggression in Pair-bonded males. Pair-bonded males also showed an increased density in V1aR binding in the AH compared to their sexually naive counterparts and overexpression of V1aR in the AH, by viral vector-mediated gene transfer, facilitated aggression toward novel females. These data demonstrate that AH-AVP is both necessary and sufficient in the regulation of selective aggression associated with Pair-Bonding. In the second part of this study, we examined the effects of amphetamine (AMPH) exposure on female-directed aggression and revealed the potential role of AH-AVP underlying this behavior. Repeated AMPH administration in sexually naive male prairie voles enhanced V1aR expression in the AH and induced aggression toward a familiar or unfamiliar female. In addition, this AMPH-induced aggression was blocked by intra-AH administration of a V1aR antagonist. Together, our data reveal a socioneurobiological mechanism, highlighting a critical role of AH-AVP in the regulation of aggression induced by Pair-Bonding or drug experience in socially monogamous male prairie voles.

  • neurochemical regulation of Pair Bonding in male prairie voles
    Physiology & Behavior, 2004
    Co-Authors: Zuoxin Wang, Brandon J Aragona
    Abstract:

    Pair Bonding represents social attachment between mates and is common among monogamous animals. The prairie vole (Microtus ochrogaster) is a monogamous rodent in which mating facilitates Pair bond formation. In this review, we first discuss how prairie voles have been used as an excellent model for neurobiological studies of Pair Bonding. We then primarily focus on male prairie voles to summarize recent findings from neuroanatomical, neurochemical, cellular, molecular, and behavioral studies implicating vasopressin (AVP), oxytocin (OT), and dopamine (DA) in the regulation of Pair Bonding. Possible interactions among these neurochemicals in the regulation of Pair Bonding, the brain areas important for Pair bond formation, and potential sexually dimorphic mechanisms underlying Pair Bonding are also discussed. As analogous social bonds are formed by humans, investigation of the neurochemical regulation of Pair bond formation in prairie voles may be beneficial for our understanding of the mechanisms associated with normal and abnormal social behaviors in humans.

  • the neurobiology of Pair Bonding
    Nature Neuroscience, 2004
    Co-Authors: Larry J Young, Zuoxin Wang
    Abstract:

    A neurobiological model for Pair-bond formation has emerged from studies in monogamous rodents. The neuropeptides oxytocin and vasopressin contribute to the processing of social cues necessary for individual recognition. Mesolimbic dopamine is involved in reinforcement and reward learning. Concurrent activation of neuropeptide and dopamine receptors in the reward centers of the brain during mating results in a conditioned partner preference, observed as a Pair bond. Differential regulation of neuropeptide receptor expression may explain species differences in the ability to form Pair bonds. These and other studies discussed here have intriguing implications for the neurobiology of social attachment in our own species.

Catherine A. Marler - One of the best experts on this subject based on the ideXlab platform.

  • Pair Bonding leads to convergence in approach behavior to conspecific vocalizations in california mice peromyscus californicus
    PLOS ONE, 2021
    Co-Authors: Patrick K Monari, Nathaniel S Rieger, Kamryn Hartfield, Juliette Schefelker, Catherine A. Marler
    Abstract:

    Pair-Bonding allows for division of labor across behavioral tasks such as protecting a territory, caring for pups or foraging for food. However, how these labor divisions are determined, whether they are simply intrinsic differences in the individual’s behavior or a coordinated behavioral response by the Pair, remains unknown. We used the monogamous, biparental and territorial California mouse (Peromyscus californicus) to study how behavioral approach to an aggressive vocal stimulus in a novel environment was affected by Pair-Bonding. Using a three-chambered vocal playback paradigm, we first measured the amount of time individuals spent in close proximity to aggressive bark vocalizations. We found that animals could be categorized as either approachers or avoiders. We then Paired individuals based on their initial approach behavior to an opposite sex individual who displayed either similar or different approach behaviors. These Pairs were then retested for approach behavior as a dyad 10–11 days post-Pairing. This test found that Pairs showed convergence in their behavioral responses, such that Pairs who were mismatched in their approach behaviors became more similar, and Pairs that were matched remained so. Finally, we analyzed the ultrasonic vocalizations (USV) produced and found that Pairs produced significantly more USVs than individuals. Importantly, increased USV production correlated with increasing behavioral convergence of Pairs. Taken together, this study shows that Pair-bonded animals alter their approach behaviors to coordinate their response with their partner and that vocal communication may play a role in coordinating these behavioral responses. Overall, our findings indicate that Pair-Bonding generates an emergent property in Pairs, adjusting their combined approach behavior towards a new aggressive stimulus representing a potential challenge to the bonded Pair. Such findings may be broadly important for social Bonding in other social systems.

  • changes in behavior and ultrasonic vocalizations during Pair Bonding and in response to an infidelity challenge in monogamous california mice
    Frontiers in Ecology and Evolution, 2018
    Co-Authors: Joshua D. Pultorak, Sarah J. Alger, Steven O. Loria, Aaron M. Johnson, Catherine A. Marler
    Abstract:

    Despite recent exciting research about Pair Bonding, little is known about how mammalian vocalizations change with the initiation and maintenance of Pair Bonding in monogamous species. Moreover, even less is known about the significance of Pair bond resilience in the face of social challenges. In the strictly monogamous California mouse (Peromyscus californicus), we measured changes in ultrasonic vocalizations (USV) and other behaviors within male-female dyads over the course of Pair Bonding and characterized associations of USVs with affiliation and aggression. After one week of cohabitation, Pairs exhibited decreased aggression and “bark” USVs, and increased “simple sweep” and “sustained vocalization” (SV) USV types. Accordingly, the number of barks was associated with aggression, whereas the number of simple sweeps and the number, call duration and bout size of SVs corresponded with affiliation. We then experimentally assessed the impact of an infidelity challenge (one week cohabitation with an unfamiliar, opposite-sex, extra-Pair individual) for both sexes on Pair social behavior, acoustic behavior, and reproductive success. The infidelity challenge temporarily disrupted Pair bond interactions during Pair reunion, independent of which sex experienced the infidelity challenge, via both increases in aggression and barks, and a stunting of affiliation and SVs, compared to control Pairs. Pair reproductive success, in the form of birth latency, litter size, pup survival and birth weight, did not differ between infidelity challenge Pairs and controls. The quality of Pair interactions, however, was associated with reproductive success: aggression during Pair reunion across all Pairs was associated with a lower likelihood of successfully producing a litter. Similarly, among infidelity challenge Pairs, but not the controls, there was a positive association between Pair affiliation and paternal care, and a negative association between Pair aggression and paternal care. Overall, the infidelity challenge revealed a weak negative effect on reproductive success, but we speculate, based on our results, that greater resiliency of a Pair bond can moderate negative effects of a social challenge.

  • Changes in Behavior and Ultrasonic Vocalizations During Pair Bonding and in Response to an Infidelity Challenge in Monogamous California Mice
    'Frontiers Media SA', 2018
    Co-Authors: Joshua D. Pultorak, Catherine A. Marler, Sarah J. Alger, Steven O. Loria, Aaron M. Johnson
    Abstract:

    Despite recent exciting research about Pair Bonding, little is known about how mammalian vocalizations change with the initiation and maintenance of Pair Bonding in monogamous species. Moreover, even less is known about the significance of Pair bond resilience in the face of social challenges. In the strictly monogamous California mouse (Peromyscus californicus), we measured changes in ultrasonic vocalizations (USV) and other behaviors within male-female dyads over the course of Pair Bonding and characterized associations of USVs with affiliation and aggression. After 1 week of cohabitation, Pairs exhibited decreased aggression and “bark” USVs, and increased “simple sweep” and “sustained vocalization” (SV) USV types. Accordingly, the number of barks was associated with aggression, whereas the number of simple sweeps and the number, call duration and bout size of SVs corresponded with affiliation. We then experimentally assessed the impact of an infidelity challenge (1 week cohabitation with an unfamiliar, opposite-sex, extra-Pair individual) for both sexes on Pair social behavior, acoustic behavior, and reproductive success. The infidelity challenge temporarily disrupted Pair bond interactions during Pair reunion, independent of which sex experienced the infidelity challenge, via both increases in aggression and barks, and a stunting of affiliation and SVs, compared to control Pairs. Pair reproductive success, in the form of birth latency, litter size, pup survival and birth weight, did not differ between infidelity challenge Pairs and controls. The quality of Pair interactions, however, was associated with reproductive success: aggression during Pair reunion across all Pairs was associated with a lower likelihood of successfully producing a litter. Similarly, among infidelity challenge Pairs, but not the controls, there was a positive association between Pair affiliation and paternal care, and a negative association between Pair aggression and paternal care. Overall, the infidelity challenge revealed a weak negative effect on reproductive success, but we speculate, based on our results, that greater resiliency of a Pair bond can moderate negative effects of a social challenge

  • Table_1_Changes in Behavior and Ultrasonic Vocalizations During Pair Bonding and in Response to an Infidelity Challenge in Monogamous California Mice.XLSX
    2018
    Co-Authors: Joshua D. Pultorak, Sarah J. Alger, Steven O. Loria, Aaron M. Johnson, Catherine A. Marler
    Abstract:

    Despite recent exciting research about Pair Bonding, little is known about how mammalian vocalizations change with the initiation and maintenance of Pair Bonding in monogamous species. Moreover, even less is known about the significance of Pair bond resilience in the face of social challenges. In the strictly monogamous California mouse (Peromyscus californicus), we measured changes in ultrasonic vocalizations (USV) and other behaviors within male-female dyads over the course of Pair Bonding and characterized associations of USVs with affiliation and aggression. After 1 week of cohabitation, Pairs exhibited decreased aggression and “bark” USVs, and increased “simple sweep” and “sustained vocalization” (SV) USV types. Accordingly, the number of barks was associated with aggression, whereas the number of simple sweeps and the number, call duration and bout size of SVs corresponded with affiliation. We then experimentally assessed the impact of an infidelity challenge (1 week cohabitation with an unfamiliar, opposite-sex, extra-Pair individual) for both sexes on Pair social behavior, acoustic behavior, and reproductive success. The infidelity challenge temporarily disrupted Pair bond interactions during Pair reunion, independent of which sex experienced the infidelity challenge, via both increases in aggression and barks, and a stunting of affiliation and SVs, compared to control Pairs. Pair reproductive success, in the form of birth latency, litter size, pup survival and birth weight, did not differ between infidelity challenge Pairs and controls. The quality of Pair interactions, however, was associated with reproductive success: aggression during Pair reunion across all Pairs was associated with a lower likelihood of successfully producing a litter. Similarly, among infidelity challenge Pairs, but not the controls, there was a positive association between Pair affiliation and paternal care, and a negative association between Pair aggression and paternal care. Overall, the infidelity challenge revealed a weak negative effect on reproductive success, but we speculate, based on our results, that greater resiliency of a Pair bond can moderate negative effects of a social challenge.

  • Pair Bonding prevents reinforcing effects of testosterone in male California mice in an unfamiliar environment
    Proceedings. Biological sciences, 2014
    Co-Authors: Xin Zhao, Catherine A. Marler
    Abstract:

    Testosterone (T) can be released by stimuli such as social interactions, and thereby influence future social behaviours. Because the reinforcing effects of T can induce preferences for specific environmental locations, T has the potential to alter behaviour through space use. In a monogamous species, this T pulse may contribute differently to space use in sexually naive (SN) and Pair-bonded (PB) males: SN males may be more likely to explore new areas to set up a territory than PB males, which are more likely to defend an existing, established territory. In this study, we test for variation in T-driven space use by examining variation in the formation of conditioned place preferences (CPPs) in SN and PB male California mice. In the three-chambered CPP apparatus, subcutaneous administrations of physiological levels of T were used to repeatedly condition SN and PB males to a side chamber, which is an unfamiliar/neutral environment. The final tests revealed that T-induced CPPs in the side chamber are developed in SN, but not PB males. This study fills a gap in our knowledge about plasticity in the rewarding nature of T pulses, based on past social experience.

Karen L. Bales - One of the best experts on this subject based on the ideXlab platform.

  • neonatal exposure to the d1 agonist skf38393 inhibits Pair Bonding in the adult prairie vole
    Behavioural Pharmacology, 2011
    Co-Authors: Caroline M Hostetler, Brandon J Aragona, Shanna L Harkey, Tarin Krzywosinski, Karen L. Bales
    Abstract:

    The monogamous prairie vole displays developmental sensitivity to early pharmacological manipulation in a number of species-typical social behaviors. The long-term consequences of altering the neonatal dopamine system are not well characterized. This study examined whether early manipulation of the dopamine system, a known mediator of adult prairie vole social behavior, during neonatal development would affect adult aggressive and attachment behaviors. Eight-day-old pups were given a single treatment with either 1 mg/kg of SKF38393 (D1 agonist), quinpirole (D2 agonist), SCH23390 (D1 antagonist), eticlopride (D2 antagonist), or saline vehicle. As adults, animals received tests for intrasexual aggression and partner preference. Activation of D1-like receptors in pups imPaired partner preference formation, but had no effect on aggression. Other neonatal treatments had no effect on their behavior as adults. To determine whether D1 activation in pups induced changes in dopamine receptor expression, we performed autoradiography on striatal tissue from a second cohort of saline-treated and SKF38393-treated animals. Although sex differences were observed, we found no treatment differences in D1 or D2 receptor binding in any striatal subregion. This study shows that exposure to a single early pharmacological alteration of dopamine receptor activity may have long-term effects on the social behavior of prairie voles.

  • Intranasal vasopressin affects Pair Bonding and peripheral gene expression in male Callicebus cupreus
    Genes brain and behavior, 2011
    Co-Authors: Michael R. Jarcho, Sally P Mendoza, William A Mason, X. Yang, Karen L. Bales
    Abstract:

    Arginine vasopressin (AVP) is a neuropeptide hormone and neurotransmitter that has peripheral functions in water regulation, and central functions in the stress response and social Bonding in male rodents. In this study, we investigated the role of AVP in partner preference behavior in a monogamous primate, the coppery titi monkey (Callicebus cupreus). Seven titi males each received three intranasal treatments: saline, low AVP (40 IU) and high AVP (80 IU) in random order, 1 week apart. They experienced a series of stimulus exposures to their female partner, a female stranger and an empty cage. Males were more likely to contact the stimulus and do so faster when either female stimulus was present. When pretreated with saline, males contacted the stranger more frequently than their partner; when pretreated with the high dosage of AVP, males contacted their partner more frequently than the stranger. We used microarray to measure peripheral changes in gene expression associated with intranasal AVP and found reduced expression of several genes coding for proinflammatory cytokines. The data presented here suggest that intranasally administered AVP has both central influences on social behavior and peripheral influences on inflammation in a nonhuman primate.

  • costs of Pair Bonding and paternal care in male prairie voles microtus ochrogaster
    Physiology & Behavior, 2009
    Co-Authors: Joshua C Campbell, Julie A. Van Westerhuyzen, Kevin D Laugero, Caroline M Hostetler, Justin D Cohen, Karen L. Bales
    Abstract:

    The direct costs of paternal care are relatively well documented in primates, however little research has explored these effects in monogamous rodents. The present study examines the long-term effects that Pairing and parenting have on male prairie voles. We hypothesized that there would be a significant weight loss over the course of Pairing and parenting, presumably from the energetic demands that accompany these changes in social condition. In a longitudinal study, we followed ten male prairie voles through being housed with their brother; Paired with a female; and caring for three consecutive litters. We found a significant drop in bodyweight across time, with maximum weight loss near the weaning of the first litter. At that same time, feeding increased, leading to possible recovery in weight; however, leptin levels dropped precipitously across time and did not recover. Corticosterone did not change significantly across time points, and overall activity levels also did not vary significantly over the course of the study. In addition, newly Paired males showed a significant increase in preference for a 2% sucrose solution during a three-hour test, indicating a metabolic need for more calories. A cross-sectional study confirmed leptin and corticosterone findings, and showed significant loss of subcutaneous (inguinal) fat in males that had cared for a litter of pups, when compared to males housed with their brothers or newly Paired males. These results suggest that cohabitation with a female, and caring for pups, all have costs for male prairie voles.

  • neural correlates of Pair Bonding in a monogamous primate
    Brain Research, 2007
    Co-Authors: Karen L. Bales, William A Mason, Ciprian Catana, Simon R Cherry, Sally P Mendoza
    Abstract:

    The neurobiology of social Bonding, despite its relevance to human mental health, has been studied primarily in rodents. In this study we used position emission tomography (PET), registered with structural magnetic resonance imaging (MRI) to investigate central glucose uptake in 17 males of a monogamous primate species, the titi monkey (Callicebus cupreus). Twelve Pair-bonded males (including six with a lesion of the prefrontal cortex) and five lone males were scanned. The five lone males were re-scanned 48 h after Pairing with a female. Significant differences in glucose uptake were found between males in long-term Pair-bonds and lone males in areas including the nucleus accumbens, ventral pallidum, medial preoptic area, medial amygdala, and the supraoptic nucleus of the hypothalamus. In Paired before and after comparisons, males showed significant changes following Pairing in the right nucleus accumbens and ventral pallidum but not in other areas. Lesioned males showed significantly higher uptake in the posterior cingulate cortex than all other males. These results indicate some basic similarities between rodents and primates in the formation and maintenance of selective social bonds, but emphasize the importance of studying long-term maintenance in addition to short-term formation of social bonds.

  • Oxytocin has dose-dependent developmental effects on Pair-Bonding and alloparental care in female prairie voles
    Hormones and behavior, 2007
    Co-Authors: Karen L. Bales, Julie A. Van Westerhuyzen, Antoniah D. Lewis-reese, Nathaniel Grotte, Jalene A. Lanter, C. Sue Carter
    Abstract:

    The present study examines the developmental consequences of neonatal exposure to oxytocin on adult social behaviors in female prairie voles (Microtus ochrogaster). Female neonates were injected within 24 h of birth with isotonic saline or one of four dosages of oxytocin (OT). As adults, females were tested in an elevated plus-maze paradigm (a measure of anxiety and exploratory behavior), and for alloparental behavior and partner preferences. At 2 mg/kg OT, females took longer to approach pups, but were the only group to form a statistically significant within-group partner preference. At 4 mg/kg OT, females retrieved pups significantly more frequently but no longer displayed a partner preference; while females treated developmentally with 8 mg/kg spent significantly more time in side-to-side contact with a male stranger than any other treatment group. OT may have broad developmental consequences, but these effects are not linear and may both increase and decrease the propensity to display behaviors such as Pair-Bonding.

Brandon J Aragona - One of the best experts on this subject based on the ideXlab platform.

  • Aversive motivation and the maintenance of monogamous Pair Bonding
    Reviews in the Neurosciences, 2013
    Co-Authors: Shanna L. Resendez, Brandon J Aragona
    Abstract:

    Social bonds are important for human health and well-being, and a crucial component of these bonds is the ability to maintain a bond once it has been formed. Importantly, although bond maintenance is required for social attachments, very little is known about the neural mechanisms that mediate this behavior. Recently, laboratory studies utilizing the socially monogamous prairie vole (an excellent animal model for the neurobiology of selective social attachment), have allowed the neural correlates of selective social attachment to begin to unfold. These studies have identified that the activation of both motivational and hedonic processing systems, which mediate other natural rewards, is also important for mediating social behaviors that are characteristic of an established Pair bond. These social behaviors include appetitive and positive social interactions with a potential mating partner in sexually naïve prairie voles, the avoidance of novel conspecifics (and sometimes aggressive rejection) that characterizes the established Pair bond and, finally, an aversion towards partner separation. The following review will discuss how a balance between opposing endogenous opioid systems - positive (mu-opiod receptors) and aversive (kappa-opioid receptors) - provide essential hedonic signaling that guides socially motivated behaviors.

  • neonatal exposure to the d1 agonist skf38393 inhibits Pair Bonding in the adult prairie vole
    Behavioural Pharmacology, 2011
    Co-Authors: Caroline M Hostetler, Brandon J Aragona, Shanna L Harkey, Tarin Krzywosinski, Karen L. Bales
    Abstract:

    The monogamous prairie vole displays developmental sensitivity to early pharmacological manipulation in a number of species-typical social behaviors. The long-term consequences of altering the neonatal dopamine system are not well characterized. This study examined whether early manipulation of the dopamine system, a known mediator of adult prairie vole social behavior, during neonatal development would affect adult aggressive and attachment behaviors. Eight-day-old pups were given a single treatment with either 1 mg/kg of SKF38393 (D1 agonist), quinpirole (D2 agonist), SCH23390 (D1 antagonist), eticlopride (D2 antagonist), or saline vehicle. As adults, animals received tests for intrasexual aggression and partner preference. Activation of D1-like receptors in pups imPaired partner preference formation, but had no effect on aggression. Other neonatal treatments had no effect on their behavior as adults. To determine whether D1 activation in pups induced changes in dopamine receptor expression, we performed autoradiography on striatal tissue from a second cohort of saline-treated and SKF38393-treated animals. Although sex differences were observed, we found no treatment differences in D1 or D2 receptor binding in any striatal subregion. This study shows that exposure to a single early pharmacological alteration of dopamine receptor activity may have long-term effects on the social behavior of prairie voles.

  • neurochemical regulation of Pair Bonding in male prairie voles
    Physiology & Behavior, 2004
    Co-Authors: Zuoxin Wang, Brandon J Aragona
    Abstract:

    Pair Bonding represents social attachment between mates and is common among monogamous animals. The prairie vole (Microtus ochrogaster) is a monogamous rodent in which mating facilitates Pair bond formation. In this review, we first discuss how prairie voles have been used as an excellent model for neurobiological studies of Pair Bonding. We then primarily focus on male prairie voles to summarize recent findings from neuroanatomical, neurochemical, cellular, molecular, and behavioral studies implicating vasopressin (AVP), oxytocin (OT), and dopamine (DA) in the regulation of Pair Bonding. Possible interactions among these neurochemicals in the regulation of Pair Bonding, the brain areas important for Pair bond formation, and potential sexually dimorphic mechanisms underlying Pair Bonding are also discussed. As analogous social bonds are formed by humans, investigation of the neurochemical regulation of Pair bond formation in prairie voles may be beneficial for our understanding of the mechanisms associated with normal and abnormal social behaviors in humans.

  • The prairie vole (Microtus ochrogaster): an animal model for behavioral neuroendocrine research on Pair Bonding.
    ILAR journal, 2004
    Co-Authors: Brandon J Aragona, Zuoxin Wang
    Abstract:

    Pair bond formation has been investigated much less than many other social behaviors, perhaps in part because traditional laboratory mice and rats do not exhibit this behavior. However, Pair Bonding is common among monogamous animals such as the prairie vole (Microtus ochrogaster) .I n this review, we discuss how the prairie vole has been used as a model system to investigate the neurobiology of Pair Bonding. Descriptions include neuroanatomical differences between monogamous and non-monogamous voles, as well as how manipulations of vasopressin, oxytocin, dopamine, and corticosterone systems affect Pair bond formation. Also summarized are potential interactions among these systems that regulate Pair Bonding, and the extent of sexual dimorphism in underlying mechanisms. Pair Bonding in prairie voles is an excellent model system for studying central processing of social information. Understanding the mechanisms underlying this behavior may provide important insights into human disorders associated with imPaired social functioning.

Larry J Young - One of the best experts on this subject based on the ideXlab platform.

  • Oxytocin receptor antagonist reverses the blunting effect of Pair Bonding on fear learning in monogamous prairie voles
    Hormones and behavior, 2020
    Co-Authors: Yu Hirota, Larry J Young, Aki Arai, Yoji Osako, Kazunari Yuri, Shinichi Mitsui
    Abstract:

    Social relationships among spouses, family members, and friends are known to affect physical and mental health. In particular, long-lasting bonds between socio-sexual partners have profound effects on cognitive, social, emotional, and physical well-being. We have previously reported that Pair Bonding in monogamous prairie voles (Microtus ochrogaster) is prevented by a single prolonged stress (SPS) paradigm, which causes behavioral and endocrine symptoms resembling post-traumatic stress disorder (PTSD) patients in rats (Arai et al., 2016). Since fear memory function is crucial for anxiety-related disorders such as PTSD, we investigated the effects of Pair Bonding on fear learning in prairie voles. We applied an SPS paradigm to male prairie voles after the cohabitation with a male (cage-mate group) or female (Pair-bonded group). The cage-mate group, but not the Pair-bonded group, showed enhanced fear response in a contextual fear conditioning test following the SPS treatment. Immunohistochemical analyses revealed that cFos-positive cells in the central amygdala were increased in the Pair-bonded group after the contextual fear conditioning test and that oxytocin immunoreactivity in the paraventricular nucleus of the hypothalamus was significantly higher in the Pair-bonded group than the cage-mate group. This Pair-Bonding dependent blunting of fear memory response was confirmed by a passive avoidance test, another fear-based learning test. Interestingly, intracerebroventricular injection of an oxytocin receptor antagonist 30 min before the passive avoidance test blocked the blunting effect of Pair Bonding on fear learning. Thus, Pair Bonding between socio-sexual partners results in social buffering in the absence of the partner, blunting fear learning, which may be mediated by oxytocin signaling.

  • neural mechanisms of mother infant Bonding and Pair Bonding similarities differences and broader implications
    Hormones and Behavior, 2016
    Co-Authors: Michael Numan, Larry J Young
    Abstract:

    This article is part of a Special Issue "Parental Care". Mother-infant Bonding is a characteristic of virtually all mammals. The maternal neural system may have provided the scaffold upon which other types of social bonds in mammals have been built. For example, most mammals exhibit a polygamous mating system, but monogamy and Pair Bonding between mating partners occur in ~5% of mammalian species. In mammals, it is plausible that the neural mechanisms that promote mother-infant Bonding have been modified by natural selection to establish the capacity to develop a selective bond with a mate during the evolution of monogamous mating strategies. Here we compare the details of the neural mechanisms that promote mother-infant Bonding in rats and other mammals with those that underpin Pair bond formation in the monogamous prairie vole. Although details remain to be resolved, remarkable similarities and a few differences between the mechanisms underlying these two types of bond formation are revealed. For example, amygdala and nucleus accumbens-ventral pallidum (NA-VP) circuits are involved in both types of bond formation, and dopamine and oxytocin actions within NA appear to promote the synaptic plasticity that allows either infant or mating partner stimuli to persistently activate NA-VP attraction circuits, leading to an enduring social attraction and Bonding. Further, although the medial preoptic area is essential for maternal behavior, its role in Pair Bonding remains to be determined. Our review concludes by examining the broader implications of this comparative analysis, and evidence is provided that the maternal care system may have also provided the basic neural foundation for other types of strong social relationships, beyond Pair Bonding, in mammals, including humans.

  • neurobiological mechanisms of social attachment and Pair Bonding
    Current opinion in behavioral sciences, 2015
    Co-Authors: Zachary V Johnson, Larry J Young
    Abstract:

    Species have evolved diverse social behavior and mating strategies in response to selective forces in their environments. While promiscuity is the predominant mating strategy across most vertebrate taxa, convergent evolution of monogamous mating systems has occurred multiple times across distant lineages. Monogamous behavior is thought to be facilitated by a neurobiological capacity to form and maintain selective social attachments, or Pair bonds, with a mating partner. The neural mechanisms of Pair Bonding behavior have been investigated most rigorously in Microtine rodents, which exhibit diverse social organizations. These studies have highlighted mesolimbic dopamine pathways, social neuropeptides (oxytocin and vasopressin), and other neural systems as integral factors in the formation, maintenance, and expression of Pair bonds.

  • anterior hypothalamic vasopressin regulates Pair Bonding and drug induced aggression in a monogamous rodent
    Proceedings of the National Academy of Sciences of the United States of America, 2009
    Co-Authors: Kyle L Gobrogge, Larry J Young, Yan Liu, Zuoxin Wang
    Abstract:

    After Pair-Bonding, male prairie voles (Microtus ochrogaster) display aggression toward novel females but not toward their female partner. Here we show that this selective aggression in Pair-bonded male prairie voles is associated with increased release of vasopressin (AVP) in the anterior hypothalamus (AH). Pharmacological activation of AVP-V1a receptors (V1aR) in the AH induced selective aggression in sexually naive males, whereas V1aR blockade diminished selective aggression in Pair-bonded males. Pair-bonded males also showed an increased density in V1aR binding in the AH compared to their sexually naive counterparts and overexpression of V1aR in the AH, by viral vector-mediated gene transfer, facilitated aggression toward novel females. These data demonstrate that AH-AVP is both necessary and sufficient in the regulation of selective aggression associated with Pair-Bonding. In the second part of this study, we examined the effects of amphetamine (AMPH) exposure on female-directed aggression and revealed the potential role of AH-AVP underlying this behavior. Repeated AMPH administration in sexually naive male prairie voles enhanced V1aR expression in the AH and induced aggression toward a familiar or unfamiliar female. In addition, this AMPH-induced aggression was blocked by intra-AH administration of a V1aR antagonist. Together, our data reveal a socioneurobiological mechanism, highlighting a critical role of AH-AVP in the regulation of aggression induced by Pair-Bonding or drug experience in socially monogamous male prairie voles.

  • oxytocin vasopressin and Pair Bonding implications for autism
    Philosophical Transactions of the Royal Society B, 2006
    Co-Authors: Elizabeth A D Hammock, Larry J Young
    Abstract:

    Understanding the neurobiological substrates regulating normal social behaviours may provide valuable insights in human behaviour, including developmental disorders such as autism that are characterized by pervasive deficits in social behaviour. Here, we review the literature which suggests that the neuropeptides oxytocin and vasopressin play critical roles in modulating social behaviours, with a focus on their role in the regulation of social Bonding in monogamous rodents. Oxytocin and vasopressin contribute to a wide variety of social behaviours, including social recognition, communication, parental care, territorial aggression and social Bonding. The effects of these two neuropeptides are species-specific and depend on species-specific receptor distributions in the brain. Comparative studies in voles with divergent social structures have revealed some of the neural and genetic mechanisms of social-Bonding behaviour. Prairie voles are socially monogamous; males and females form long-term Pair bonds, establish a nest site and rear their offspring together. In contrast, montane and meadow voles do not form a bond with a mate and only the females take part in rearing the young. Species differences in the density of receptors for oxytocin and vasopressin in ventral forebrain reward circuitry differentially reinforce social-Bonding behaviour in the two species. High levels of oxytocin receptor (OTR) in the nucleus accumbens and high levels of vasopressin 1a receptor (V1aR) in the ventral pallidum contribute to monogamous social structure in the prairie vole. While little is known about the genetic factors contributing to species-differences in OTR distribution, the species-specific distribution pattern of the V1aR is determined in part by a speciesspecific repetitive element, or ‘microsatellite’, in the 5 0 regulatory region of the gene encoding V1aR (avpr1a). This microsatellite is highly expanded in the prairie vole (as well as the monogamous pine vole) compared to a very short version in the promiscuous montane and meadow voles. These species differences in microsatellite sequence are sufficient to change gene expression in cell culture. Within the prairie vole species, intraspecific variation in the microsatellite also modulates gene expression in vitro as well as receptor distribution patterns in vivo and influences the probability of social approach and Bonding behaviour. Similar genetic variation in the human AVPR1A may contribute to variations in human social behaviour, including extremes outside the normal range of behaviour and those found in autism spectrum disorders. In sum, comparative studies in Pair-Bonding rodents have revealed neural and genetic mechanisms contributing to social-Bonding behaviour. These studies have generated testable hypotheses regarding the motivational systems and underlying molecular neurobiology involved in social engagement and social bond formation that may have important implications for the core social deficits characterizing autism spectrum disorders.