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oxytocin and social relationships: from attachment to bond disruption.social relationships throughout life are vital for well-being and physical and mental health. a significant amount of research in animal models as well as in humans suggests that oxytocin (ot) plays an important role in the development of the capacity to form social bonds, the mediation of the positive aspects of early-life nurturing on adult bonding capacity, and the maintenance of social bonding. here, we focus on the extensive research on a socially monogamous rodent model organism, the prair ...201728812266
localization of oxytocin receptors in the prairie vole (microtus ochrogaster) neocortex.early experience and social context interact to alter the phenotype of complex social behaviors. these early experiences can also result in alterations to cortical organization and connections. given the ability of the neuropeptide oxytocin (ot) to modulate social and reproductive behavior, ot is likely involved in these cortical processes. however, little is known about the distribution of ot and ot receptors (otr) within the neocortex. using autoradiographic and neuroanatomical techniques, we ...201728214580
the neuroendocrinology of love.romantic love could be considered as a collection of activities associated with the acquisition and retention of emotions needed to survive and reproduce. these emotions change the individual's behavioural strategies in a way that will increase the likelihood of achieving these goals. love may be defined as an emergent property of an ancient cocktail of neuropeptides and neurotransmitters. it appears that lust, attachment and attraction appear to be distinct but intertwined processes in the brai ...201727366726
the neurobiology of pair bond formation, bond disruption, and social buffering.enduring social bonds play an essential role in human society. these bonds positively affect psychological, physiological, and behavioral functions. here, we review the recent literature on the neurobiology, particularly the role of oxytocin and dopamine, of pair bond formation, bond disruption, and social buffering effects on stress responses, from studies utilizing the socially monogamous prairie vole (microtus ochrogaster).201627290660
bold fmri in awake prairie voles: a platform for translational social and affective neuroscience.the advancement of neuroscience depends on continued improvement in methods and models. here, we present novel techniques for the use of awake functional magnetic resonance imaging (fmri) in the prairie vole (microtus ochrogaster) - an important step forward in minimally-invasive measurement of neural activity in a non-traditional animal model. imaging neural responses in prairie voles, a species studied for its propensity to form strong and selective social bonds, is expected to greatly advance ...201627238726
habitat fragmentation, vole population fluctuations, and the rompa hypothesis: an experimental test using model landscapes.increased habitat fragmentation leads to smaller size of habitat patches and to greater distance between patches. the rompa hypothesis (ratio of optimal to marginal patch area) uniquely links vole population fluctuations to the composition of the landscape. it states that as rompa decreases (fragmentation increases), vole population fluctuations will increase (including the tendency to display multi-annual cycles in abundance) because decreased proportions of optimal habitat result in greater po ...201627136035
chronic social isolation enhances reproduction in the monogamous prairie vole (microtus ochrogaster).chronic stressors are generally considered to disrupt reproduction and inhibit mating. here we test the hypothesis that a chronic stressor, specifically social isolation, can facilitate adaptive changes that enhance/accelerate reproductive effort. in general, monogamous species display high levels of prosociality, delayed sexual maturation, and greater parental investment in fewer, higher quality offspring compared with closely related polygynous species. we predicted that chronic social isolati ...201626939085
the protective effects of social bonding on behavioral and pituitary-adrenal axis reactivity to chronic mild stress in prairie voles.positive social interactions may protect against stress. this study investigated the beneficial effects of pairing with a social partner on behaviors and neuroendocrine function in response to chronic mild stress (cms) in 13 prairie vole pairs. following 5 days of social bonding, male and female prairie voles were exposed to 10 days of cms (mild, unpredictable stressors of varying durations, for instance, strobe light, white noise, and damp bedding), housed with either the social partner (paired ...201728276805
non-contact automatic respiration monitoring in restrained rodents.prairie voles are socially monogamous rodents that form social bonds similar to those seen in primates. social behavior investigation in these species, that include studying their breathing regulation, can provide us with an invaluable psychological model to understand social and emotional functions in both animals and humans. there have been several studies associated with the respiratory pattern of these species in the state of fear-induced defense. however, non-invasive measurement methods em ...201628269378
empathy in prairie voles: is this the consolation prize?although it is well known that humans and great apes are capable of engaging in consolation, an affiliative behavior directed toward distressed individuals, it has largely been assumed that this form of empathy was restricted to species possessing more complex cognitive functions. recently, however, burkett and colleagues (science, 351, 375-378, 2016) have provided intriguing evidence that consolation behavior may be present in a socially monogamous rodent, the prairie vole. they also provide da ...201627443192
alcohol suppresses tonic gabaa receptor currents in cerebellar granule cells in the prairie vole: a neural signature of high-alcohol-consuming genotypes.evidence indicates that the cerebellum plays a role in genetic predilection to excessive alcohol (ethanol [etoh]) consumption in rodents and humans, but the molecular mechanisms mediating such predilection are not understood. we recently determined that etoh has opposite actions (enhancement or suppression) on tonic gabaa receptor (gabaa r) currents in cerebellar granule cells (gcs) in low- and high-etoh-consuming rodents, respectively, and proposed that variation in gc tonic gabaa r current res ...201627426857
methamphetamine consumption inhibits pair bonding and hypothalamic oxytocin in prairie voles.methamphetamine (ma) abuse has been linked to violence, risk-taking behaviors, decreased sexual inhibition, and criminal activity. it is important to understand mechanisms underlying these drug effects for prevention and treatment of ma-associated social problems. previous studies have demonstrated that experimenter-administered amphetamine inhibits pair bonding and increases aggression in monogamous prairie voles. it is not currently known whether similar effects on social behaviors would be ob ...201627380172
variation in the oxytocin receptor gene predicts brain region-specific expression and social attachment.oxytocin (oxt) modulates several aspects of social behavior. intranasal oxt is a leading candidate for treating social deficits in patients with autism spectrum disorder, and common genetic variants in the human oxtr gene are associated with emotion recognition, relationship quality, and autism spectrum disorder. animal models have revealed that individual differences in oxtr expression in the brain drive social behavior variation. our understanding of how genetic variation contributes to brain ...201626893121
dopamine and opioid systems interact within the nucleus accumbens to maintain monogamous pair bonds.prairie vole breeder pairs form monogamous pair bonds, which are maintained through the expression of selective aggression toward novel conspecifics. here, we utilize behavioral and anatomical techniques to extend the current understanding of neural mechanisms that mediate pair bond maintenance. for both sexes, we show that pair bonding up-regulates mrna expression for genes encoding d1-like dopamine (da) receptors and dynorphin as well as enhances stimulated da release within the nucleus accumb ...201627371827
neurochemical mediation of affiliation and aggression associated with pair-bonding.the neuropeptides vasopressin and corticotropin-releasing factor facilitate, while serotonin inhibits, aggression. how the brain is wired to coordinate interactions between these functionally opposed neurotransmitters to control behavioral states is poorly understood.201727129413
paternal deprivation affects social behaviors and neurochemical systems in the offspring of socially monogamous prairie voles.early life experiences, particularly the experience with parents, are crucial to phenotypic outcomes in both humans and animals. although the effects of maternal deprivation on offspring well-being have been studied, paternal deprivation (pd) has received little attention despite documented associations between father absence and children health problems in humans. in the present study, we utilized the socially monogamous prairie vole (microtus ochrogaster), which displays male-female pair bondi ...201727998780
effects of acute corticosterone treatment on male prairie voles (microtus ochrogaster): territorial aggression does not accompany induced social preference.corticosterone (cort) is a stress-related steroid hormone found in vertebrates, and is known to interact with behavior. in the socially monogamous prairie vole (microtus ochrogaster), acute stress and specifically acute cort administration have been shown to facilitate male social preference for a familiar female, and this effect has been described as facilitation of the monogamous pair bond. it is possible, however, that the effects of stress on social preference may initially represent a short ...201627841456
oxytocin-dependent consolation behavior in rodents.consolation behavior toward distressed others is common in humans and great apes, yet our ability to explore the biological mechanisms underlying this behavior is limited by its apparent absence in laboratory animals. here, we provide empirical evidence that a rodent species, the highly social and monogamous prairie vole (microtus ochrogaster), greatly increases partner-directed grooming toward familiar conspecifics (but not strangers) that have experienced an unobserved stressor, providing soci ...201626798013
male prairie voles display cardiovascular dipping associated with an ultradian activity cycle.mammals typically display alternating active and resting phases and, in most species, these rhythms follow a circadian pattern. the active and resting phases often are accompanied by corresponding physiological changes. in humans, blood pressure decreases during the resting phase of the activity cycle, and the magnitude of that "nocturnal dipping" has been used to stratify patients according to the risk for cardiovascular disease. however, in contrast to most mammals, prairie voles (microtus och ...201626780151
induced pluripotent stem cells with six reprogramming factors from prairie vole, which is an animal model for social behaviors.prairie voles show strong pair bonding with their mating partners, and they demonstrate parental behavior toward their infants, indicating that the prairie vole is a unique animal model for analysis of molecular mechanisms of social behavior. until a recent study, the signaling pathway of oxytocin was thought to be critical for the social behavior of prairie voles, but neuron-specific functional research may be necessary to identify the molecular mechanisms of social behavior. prairie vole pluri ...201626777120
sex differences in microglial colonization and vulnerabilities to endocrine disruption in the social brain.during development, microglia, the resident immune cells of the brain, play an important role in synaptic organization. microglial colonization of the developing brain is sexually dimorphic in some regions, including nuclei critical for the coordination of social behavior, suggesting steroid hormones have an influencing role, particularly estrogen. by extension, microglial colonization may be vulnerable to endocrine disruption. concerns have been raised regarding the potential for endocrine disr ...201627102938
male prairie voles with different avpr1a microsatellite lengths do not differ in courtship behaviour.females are generally expected to be selective when choosing their social and sexual partners. in a previous laboratory study, female prairie voles (microtus ochrogaster) showed significant social and sexual preferences for males with longer microsatellite dna within the avpr1a gene encoding the vasopressin 1a receptor, as predicted if females select mates whose parental behaviour should increase female reproductive success. we tested the hypothesis that males with short versus long avpr1a micro ...201627083501
ghrelin receptor (ghs-r1a) antagonism alters preference for ethanol and sucrose in a concentration-dependent manner in prairie voles.ghrelin receptor (ghs-r1a) activity has been implicated in reward for preferred foods and drugs; however, a recent study in our laboratory indicated that ghs-r1a antagonism reduces early (after only four exposures) preference for 20% ethanol, but not 10% sucrose in prairie voles, a genetically diverse high alcohol-consuming species. the purpose of the present study was to determine if these effects of ghs-r1a antagonism depend on the concentration of the rewarding solution being consumed. we fir ...201626723269
the ties that bond: neurochemistry of attachment in voles.in socially monogamous prairie voles (microtus ochrogaster), mating induces three primary types of behavior; namely, partner preference, selective aggression toward conspecific strangers, and bi-parental care, making this rodent an ideal model system to study sociality and underlying neurochemical mechanisms associated with monogamous mating strategies. here, we highlight species differences in neurochemical receptor distributions associated with mating experience leading to the establishment of ...201627131991
trichostatin a (tsa) facilitates formation of partner preference in male prairie voles (microtus ochrogaster).in the socially monogamous prairie voles (microtus ochrogaster), the development of a social bonding is indicated by the formation of partner preference, which involves a variety of environmental and neurochemical factors and brain structures. in a most recent study in female prairie voles, we found that treatment with the histone deacetylase inhibitor trichostatin a (tsa) facilitates the formation of partner preference through up-regulation of oxytocin receptor (otr) and vasopressin v1a recepto ...201627074037
prairie voles as a model to screen medications for the treatment of alcoholism and addictions.most preclinical studies of medications to treat addictions are performed in mice and rats. these two rodent species belong to one phylogenetic subfamily, which narrows the likelihood of identifying potential mechanisms regulating addictions in other species, ie, humans. expanding the genetic diversity of organisms modeling alcohol and drug abuse enhances our ability to screen for medications to treat addiction. recently, research laboratories adapted the prairie vole model to study mechanisms o ...201627055620
prairie vole pups show potentiated isolation-induced vocalizations following isolation from their mother, but not their father.vocalizations can be markers of emotional social communication. maternal potentiation was originally described as an increased rate of vocalization by isolated rat pups following an interaction with their mothers, but not with other social companions. here we asked if potentiation in prairie voles, a species with pair-bonding and bi-parental rearing, is parent-specific. we found that isolated, 8-11-day-old voles exhibited potentiation following reunions with the dam, but not the sire. these resp ...201626990108
fine-scale spatial patterns of genetic relatedness among resident adult prairie voles.characterizing the spatial arrangement of related individuals within populations can convey information about opportunities for the evolution of kin-selected social behaviors, the potential for inbreeding, and the geographic distribution of genetic variation. prairie voles (microtus ochrogaster) are socially monogamous rodents that sometimes breed cooperatively. individuals of both sexes are highly philopatric, and among natal dispersers, the average dispersal distance is about 30 m. such limite ...201526989264
species differences in behavior and cell proliferation/survival in the adult brains of female meadow and prairie voles.microtine rodents display diverse patterns of social organization and behaviors, and thus provide a useful model for studying the effects of the social environment on physiology and behavior. the current study compared the species differences and the effects of oxytocin (ot) on anxiety-like, social affiliation, and social recognition behaviors in female meadow voles (microtus pennsylvanicus) and prairie voles (microtus ochrogaster). furthermore, cell proliferation and survival in the brains of a ...201626708743
exploration in a dispersal task: effects of early experience and correlation with other behaviors in prairie voles (microtus ochrogaster).socially monogamous prairie voles (microtus ochrogaster) display remarkable individual variation in social behaviors, which has been associated with differences in early life experience and neuropeptide receptor densities. these differences are also seen in the wild, where approximately 70% of young voles remain in their natal group as non-breeding alloparents, while the other 30% disperse. we investigated whether natural variation in early parental care could contribute to offspring's willingne ...201627720755
a single prolonged stress paradigm produces enduring impairments in social bonding in monogamous prairie voles.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 traumati ...201627522019
sexual fidelity trade-offs promote regulatory variation in the prairie vole brain.individual variation in social behavior seems ubiquitous, but we know little about how it relates to brain diversity. among monogamous prairie voles, levels of vasopressin receptor (encoded by the gene avpr1a) in brain regions related to spatial memory predict male space use and sexual fidelity in the field. we find that trade-offs between the benefits of male fidelity and infidelity are reflected in patterns of territorial intrusion, offspring paternity, avpr1a expression, and the evolutionary ...201526659055
central oxytocin receptors mediate mating-induced partner preferences and enhance correlated activation across forebrain nuclei in male prairie voles.oxytocin (ot) is a deeply conserved nonapeptide that acts both peripherally and centrally to modulate reproductive physiology and sociosexual behavior across divergent taxa, including humans. in vertebrates, the distribution of the oxytocin receptor (otr) in the brain is variable within and across species, and otr signaling is critical for a variety of species-typical social and reproductive behaviors, including affiliative and pair bonding behaviors in multiple socially monogamous lineages of f ...201626643557
oxytocin promotes functional coupling between paraventricular nucleus and both sympathetic and parasympathetic cardioregulatory nuclei.the neuropeptide oxytocin (oxt) facilitates prosocial behavior and selective sociality. in the context of stress, oxt also can down-regulate hypothalamic-pituitary-adrenal (hpa) axis activity, leading to consideration of oxt as a potential treatment for many socioaffective disorders. however, the mechanisms through which administration of exogenous oxt modulates social behavior in stressful environmental contexts are not fully understood. here, we investigate the hypothesis that autonomic pathwa ...201626836772
local oxytocin tempers anxiety by activating gabaa receptors in the hypothalamic paraventricular nucleus.oxytocin (oxt) is released in various hypothalamic and extrahypothalamic brain areas in response to anxiogenic stimuli to regulate aspects of emotionality and stress coping. we examined the anxiolytic action of oxt in the hypothalamic paraventricular nucleus (pvn) while appraising if oxt recruits gaba neurons to inhibit the behavioral, hormonal, and neuronal response to stress in female prairie voles (microtus ochrogaster). voles received an injection of oxt in the pvn either before or after an ...201626415118
dimercaptopropane sulfonate chelation affects in vivo hg and mehg distribution in tissues and urine of prairie voles (microtus ochrogaster).methyl mercury cation (mehg(+)) and divalent mercury (hg(2+)) were quantified in urine, liver, kidney, and brain of prairie voles (microtus ochrogaster) during a 12 week exposure to aqueous mehg(+) at concentrations of 10, 100, and 1000 ng mehg(+)/ml. aqueous mehg(+) exposures increased mercury accumulation in tissues of voles from each exposure group. accumulation was greater within the higher two exposure groups. similar [hg(2+)] and [mehg(+)] were determined within a given organ type before a ...201526412077
voluntary exercise facilitates pair-bonding in male prairie voles.the neuropeptides oxytocin and vasopressin have been implicated in exercise, as well as monogamy and parental behavior. in this study, we compared behavioral and neuroendocrine effects of access to an exercise wheel vs. the sedentary state typical in lab animal housing. male prairie voles (microtus ochrogaster) were studied because of their extensive repertoire of social behaviors including pair bond formation and biparental care, which are influenced by oxytocin and vasopressin. subjects in one ...201626409174
social recognition in paired but not single male prairie voles.social recognition is an integral component of behavior that underlies many much larger behavioral suites. for example, monogamous pair bonding is relatively meaningless if an individual cannot recall with whom the bond was with. prairie voles (microtus ochrogaster) are a socially monogamous rodent, well known for their long-term pair bonds between males and females. although previous work has shown that bonded males reliably spend more time with their pair-mate over an unfamiliar female, recent ...201526365995
effects of population density on corticosterone levels of prairie voles in the field.high population density is often associated with increased levels of stress-related hormones, such as corticosterone (cort). prairie voles (microtus ochrogaster) are a socially monogamous species known for their large population density fluctuations in the wild. although cort influences the social behavior of prairie voles in the lab, the effect of population density on cort has not previously been quantified in this species in the field. we validated a non-invasive hormone assay for measuring c ...201626342968
neuropeptidergic regulation of pair-bonding and stress buffering: lessons from voles.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 un ...201526335886
neonatal exposure to amphetamine alters social affiliation and central dopamine activity in adult male prairie voles.the prairie vole (microtus ochrogaster) is a socially monogamous rodent species that forms pair bonds after mating. recent data have shown that amphetamine (amph) is rewarding to prairie voles as it induces conditioned place preferences. further, repeated treatment with amph impairs social bonding in adult prairie voles through a central dopamine (da)-dependent mechanism. the present study examined the effects of neonatal exposure to amph on behavior and central da activity in adult male prairie ...201526321240
intergenerational transmission of alloparental behavior and oxytocin and vasopressin receptor distribution in the prairie vole.variation in the early environment has the potential to permanently alter offspring behavior and development. we have previously shown that naturally occurring variation in biparental care of offspring in the prairie vole is related to differences in social behavior of the offspring. it was not, however, clear whether the behavioral differences seen between offspring receiving high compared to low amounts of parental care were the result of different care experiences or were due to shared geneti ...201526257619
effects of postnatal estrogen manipulations on juvenile alloparental behavior.sex- and species-specific patterns of estrogen receptor (er)-α expression are established early in development, which may contribute to sexual differentiation of behavior and determine male social organization. the current study investigated the effects of erα and erβ activation during the second postnatal week on subsequent alloparental behavior and erα expression in juvenile prairie voles. male and female pups were treated daily with 17β-estradiol (e2, erα/erβ agonist), ppt (selective erα agon ...201526222494
the oxytocin system promotes resilience to the effects of neonatal isolation on adult social attachment in female prairie voles.genes and social experiences interact to create variation in social behavior and vulnerability to develop disorders of the social domain. socially monogamous prairie voles display remarkable diversity in neuropeptide receptor systems and social behavior. here, we examine the interaction of early-life adversity and brain oxytocin receptor (otr) density on adult social attachment in female prairie voles. first, pups were isolated for 3 h per day, or unmanipulated, from postnatal day 1-14. adult su ...201526196439
voluntary locomotor activity mitigates oxidative damage associated with isolation stress in the prairie vole (microtus ochrogaster).organismal performance directly depends on an individual's ability to cope with a wide array of physiological challenges. for social animals, social isolation is a stressor that has been shown to increase oxidative stress. another physiological challenge, routine locomotor activity, has been found to decrease oxidative stress levels. because we currently do not have a good understanding of how diverse physiological systems like stress and locomotion interact to affect oxidative balance, we studi ...201526179798
individual differences in cortical connections of somatosensory cortex are associated with parental rearing style in prairie voles (microtus ochrogaster).early-life sensory experiences have a profound effect on brain organization, connectivity, and subsequent behavior. in most mammals, the earliest sensory inputs are delivered to the developing brain through tactile contact with the parents, especially the mother. prairie voles (microtus ochrogaster) are monogamous and, like humans, are biparental. within the normal prairie vole population, both the type and the amount of interactions, particularly tactile contact, that parents have with their of ...201626101098
immunoglobulin genomics in the prairie vole (microtus ochrogaster).in science, the prairie voles are ideal models for studying the regulatory mechanisms of social behavior in humans. the utility of the prairie vole as a biology model can be further enhanced by characterization of the genes encoding components of the immune system. here, we report the genomic organization of the prairie vole immunoglobulin heavy and light chain genes. the prairie vole igh locus on chromosome 1 spans over 1600kb, and consists of at least 79 vh segments (28 potentially functional ...201526073565
in vitro culture and in vitro fertilization techniques for prairie voles (microtus ochrogaster).prairie vole (microtus ochrogaster) is a highly social animal and is a commonly used animal model for neuropsychopharmacological and psychiatric studies. to date, only a few reports on the development of transgenic prairie voles which was primarily due to the suboptimal development of assisted reproductive technology (art) in prairie voles. limitations in art further hinder the development of genetically modified prairie voles such as the application of conventional gene targeting technologies u ...201526071353
neural mechanisms of mother-infant bonding and pair bonding: similarities, differences, and broader implications.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 ...201626062432
escalated aggression in animal models: shedding new light on mesocorticolimbic circuits.recent developments promise to significantly advance the understudied behavioral and neurobiology of aggression: (1) animal models that capture essential features of human violence and callousness have been developed. these models range from mice that have been selectively bred for short attack latencies, monogamous prairie voles, and glucocorticoid-compromised rats to rodents and non-human primates that escalate their aggression after consuming or when withdrawing from alcohol. (2) optogenetic ...201525938130
early rearing experience is associated with vasopressin immunoreactivity but not reactivity to an acute non-social stressor in the prairie vole.the early life experiences of an organism have the potential to alter its developmental trajectories. perhaps one of the most powerful influences during this period is the parent-offspring relationship. previous work in several mammalian species has demonstrated that parental care in early life and specifically maternal behavior can influence several adult outcomes in offspring, including affiliative and aggressive behavior, parental behavior, hypothalamic-pituitary-adrenal (hpa) functioning and ...201525890274
oxytocin in the nucleus accumbens shell reverses crfr2-evoked passive stress-coping after partner loss in monogamous male prairie voles.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 ...201626615473
perinatal and juvenile social environments interact to shape cognitive behaviour and neural phenotype in prairie voles.social environments experienced at different developmental stages profoundly shape adult behavioural and neural phenotypes, and may have important interactive effects. we asked if social experience before and after weaning influenced adult social cognition in male prairie voles. animals were raised either with or without fathers and then either housed singly or in sibling pairs. males that were socially deprived before (fatherless) and after (singly housed) weaning did not demonstrate social rec ...201526609086
female-paced mating does not affect pair-bond expression by male prairie voles (microtus ochrogaster).prairie vole males typically display robust preferences for affiliation with their respective mates that indicate the expression of a pair-bond. however, it recently has been shown that the strength of a male vole's pair-bond can differ depending on the reproductive status of his mate. in the present study, we examined the possibility that female-controlled pacing of the mating sequence could alter males' affiliative behaviors in a partner-preference test by affecting reproductive success. we ex ...201526594105
regional differences in mu and kappa opioid receptor g-protein activation in brain in male and female prairie voles.prairie voles are unusual mammals in that, like humans, they are capable of forming socially monogamous pair bonds, display biparental care, and engage in alloparental behaviors. both mu and kappa opioid receptors are involved in behaviors that either establish and maintain, or result from pair bond formation in these animals. mu and kappa opioid receptors both utilize inhibitory g-proteins in signal transduction mechanisms, however the efficacy by which these receptor subtypes stimulate g-prote ...201526523979
developmental expression of estrogen receptor beta in the brain of prairie voles (microtus ochrogaster).here, for the first time, the expression of estrogen receptor beta (erβ) is characterized in the brains of the highly prosocial prairie vole (microtus ochrogaster). erβ immunoreactivity was compared in weanlings (postnatal day 21) and adult males and females. the results indicate several major findings. first, unlike erα, erβ expression is not sexually dimorphic. second, the adult pattern of erβ-ir is established at the time of weaning, as there were no age-dependent effects on distribution. fin ...201626419697
melanocortin receptor agonists facilitate oxytocin-dependent partner preference formation in the prairie vole.the central melanocortin (mc) system has been widely studied for its effects on food intake and sexual behavior. however, the mc system, and more specifically the mc4 receptor (mc4r), also interacts with neurochemical systems that regulate socioemotional behaviors, including oxytocin (ot) and dopamine. in monogamous prairie voles, ot and dopamine interact to promote partner preference formation, a laboratory measure of an enduring social bond between mates. here we investigated the effects of mc ...201525652247
social isolation disrupts innate immune responses in both male and female prairie voles and enhances agonistic behavior in female prairie voles (microtus ochrogaster).psychosocial stress, specifically social isolation, is an important risk factor for the development of a variety of psychological and physiological disorders. changes in immune function have been hypothesized to mediate this relationship. the current study used the prairie vole (microtus ochrogaster) model of isolation-induced depressive-like behavior to test whether social isolation led to changes in innate immune function. specifically, we used hemolytic complement (ch50) and bacteria killing ...201525639952
spontaneous emergence of overgrown molar teeth in a colony of prairie voles (microtus ochrogaster).continuously growing incisors are common to all rodents, which include the microtus genus of voles. however, unlike many rodents, voles also possess continuously growing molars. here, we report spontaneous molar defects in a population of prairie voles (microtus ochrogaster). we identified bilateral protuberances on the ventral surface of the mandible in several voles in our colony. in some cases, the protuberances broke through the cortical bone. the mandibular molars became exposed and infecte ...201525634121
behavioral comparisons of male and female pups of prairie voles (microtus ochrogaster) and meadow voles (m. pennsylvanicus).sexual dimorphism in mammals typically is reduced in monogamous species relative to polygynous species, with promiscuous species being intermediate. this pattern of dimorphism characterizes adult behavior and body mass of prairie voles, a monogamous species, when compared with meadow voles, a closely related polygynous or promiscuous species. we examined whether the pattern also applies to young of the two species by observing individual pups living in family groups in seminatural environments. ...201525631873
early rearing experience is related to altered aggression and vasopressin production following chronic social isolation in the prairie vole.parent-offspring interactions early in life can permanently shape the developmental path of those offspring. manipulation of maternal care has long been used to alter the early-life environment of infants and impacts their later social behavior, aggression, and physiology. more recently, naturally occurring variation in maternal licking and grooming behavior has been shown to result in differences in social behavior and stress physiology in adult offspring. we have developed a model of natural v ...201525623420
acoustic features of prairie vole (microtus ochrogaster) ultrasonic vocalizations covary with heart rate.vocalizations serve as a conspecific social communication system among mammals. modulation of acoustic features embedded within vocalizations is used by several mammalian species to signal whether it is safe or dangerous to approach conspecific and heterospecific mammals. as described by the polyvagal theory, the phylogenetic shift in the evolution of mammals involved an adaptive neuroanatomical link between the neural circuits regulating heart rate and the muscles involved in modulating the aco ...201525447483
long-term exposure to intranasal oxytocin in a mouse autism model.oxytocin (ot) is a neuropeptide involved in mammalian social behavior. it is currently in clinical trials for the treatment of autism spectrum disorder (asd). previous studies in healthy rodents (prairie voles and c57bl/6j mice) have shown that there may be detrimental effects of long-term intranasal administration, raising the questions about safety and efficacy. to investigate the effects of ot on the aspects of asd phenotype, we conducted the first study of chronic intranasal ot in a well-val ...201425386957
altered connexin 43 and connexin 45 protein expression in the heart as a function of social and environmental stress in the prairie vole.exposure to social and environmental stressors may influence behavior as well as autonomic and cardiovascular regulation, potentially leading to depressive disorders and cardiac dysfunction including elevated sympathetic drive, reduced parasympathetic function, and ventricular arrhythmias. the cellular mechanisms that underlie these interactions are not well understood. one mechanism may involve alterations in the expression of connexin43 (cx43) and connexin45 (cx45), gap junction proteins in th ...201525338193
oxytocin and object preferences in the male prairie vole.the neuropeptide oxytocin has been previously associated with social attachment behaviors in various species. studies in socially monogamous prairie voles (microtus ochrogaster) and other species have implicated oxytocin in partner preferences and other social behaviors. in the present study male prairie voles were injected intraperitoneally with either oxytocin or the selective oxytocin antagonist, l-368,899, and were assessed for object preference (for small inanimate toys) 30-min after inject ...201425219944
centrally-administered oxytocin promotes preference for familiar objects at a short delay in ovariectomized female rats.oxytocin has been previously associated with social attachment behaviors in various species, however, most studies focused on partner preference in the socially-monogamous prairie vole. in these, oxytocin treatment was shown to promote partner preference, such that females receiving either central or pulsatile peripheral administration would spend more time with a familiar male. this behavioral outcome was blocked by oxytocin receptor antagonist treatment. the aim of the current study was to fur ...201425127685
translational implications of oxytocin-mediated social buffering following immobilization stress in female prairie voles. 201425060784
a novel model for neuroendocrine toxicology: neurobehavioral effects of bpa exposure in a prosocial species, the prairie vole (microtus ochrogaster).impacts on brain and behavior have been reported in laboratory rodents after developmental exposure to bisphenol a (bpa), raising concerns about possible human effects. epidemiological data suggest links between prenatal bpa exposure and altered affective behaviors in children, but potential mechanisms are unclear. disruption of mesolimbic oxytocin (ot)/vasopressin (avp) pathways have been proposed, but supporting evidence is minimal. to address these data gaps, we employed a novel animal model ...201425051448
establishment of stable dominance interactions in prairie vole peers: relationships with alcohol drinking and activation of the paraventricular nucleus of the hypothalamus.dominance hierarchies are an important aspect of group-living as they determine individual access to resources. the existence of dominance ranks in access to space has not been described in socially monogamous, communally nesting prairie voles (microtus ochrogaster). here, we tested whether dominance could be assessed using the tube test. we also tested whether dominance related to alcohol intake, similar to what has been demonstrated in nonmonogamous species. same-sex pairs of unfamiliar peers ...201424963825
sex differences in the influence of social context, salient social stimulation and amphetamine on ultrasonic vocalizations in prairie voles.prairie voles (microtus ochrogaster) are a socially monogamous rodent species and their cooperative behaviors require extensive communication between conspecifics. rodents use ultrasonic vocalizations (usvs) to communicate and because a prairie vole breeder pair must engage in extensive cooperation for successful reproduction, auditory communication may be critical for this species. therefore, we sought to characterize usvs in adult male and female prairie voles, and to determine how these calls ...201424952968
oxytocin reverses amphetamine-induced deficits in social bonding: evidence for an interaction with nucleus accumbens dopamine.drug addiction has devastating consequences on social behaviors and can lead to the impairment of social bonding. accumulating evidence indicates that alterations in oxytocin (ot) and dopamine (da) neurotransmission within brain reward circuitry may be involved. we investigated this possibility, as well as the therapeutic potential of ot for drug-induced social deficits, using the prairie vole (microtus ochrogaster)-a socially monogamous rodent that forms enduring pair bonds between adult mates. ...201424948805
the crf system and social behavior: a review.the corticotropin-releasing factor (crf) system plays a key role in a diversity of behaviors accompanying stress, anxiety and depression. there is also substantial research on relationships between social behaviors and the crf system in a variety of taxa including fish, birds, rodents, and primates. some of these relationships are due to the broad role of crf and urocortins in stress and anxiety, but these peptides also modulate social behavior specifically. for example, the social interaction ( ...201323754975
neonatal melanocortin receptor agonist treatment reduces play fighting and promotes adult attachment in prairie voles in a sex-dependent manner.the melanocortin receptor (mcr) system has been studied extensively for its role in feeding and sexual behavior, but effects on social behavior have received little attention. α-msh interacts with neural systems involved in sociality, including oxytocin, dopamine, and opioid systems. acute melanotan-ii (mtii), an mc3/4r agonist, potentiates brain oxytocin (ot) release and facilitates ot-dependent partner preference formation in socially monogamous prairie voles. here we examined the long-term im ...201424923239
effects of sex and reproductive experience on the number of orexin a-immunoreactive cells in the prairie vole brain.large populations of cells synthesizing the neuropeptide orexin (ox) exist in the caudal hypothalamus of all species examined and are implicated in physiological and behavioral processes including arousal, stress, anxiety and depression, reproduction, and goal-directed behaviors. hypothalamic ox expression is sexually dimorphic in different directions in laboratory rats (f>m) and mice (m>f), suggesting different roles in male and female physiology and behavior that are species-specific. we here ...201424874707
rnai knockdown of oxytocin receptor in the nucleus accumbens inhibits social attachment and parental care in monogamous female prairie voles.oxytocin modulates many aspects of social cognition and behaviors, including maternal nurturing, social recognition and bonding. natural variation in oxytocin receptor (oxtr) density in the nucleus accumbens (nacc) is associated with variation in alloparental behavior, and artificially enhancing oxtr expression in the nacc enhances alloparental behavior and pair bonding in socially monogamous prairie voles. furthermore, infusion of an oxtr antagonist into the nacc inhibits alloparental behavior ...201525874849
ghs-r1a antagonism reduces alcohol but not sucrose preference in prairie voles.ghrelin has been shown to mediate food and drug reward in rats and mice, and the rewarding properties of sweet foods and alcohol are known to contribute to overconsumption of these substances.201525843741
cardioacceleration in alloparents in response to stimuli from prairie vole pups: the significance of thermoregulation.autonomic responses, including changes in heart rate and respiratory sinus arrhythmia (rsa) can provide indications of emotional reactivity to social stimuli in mammals. we have previously reported that male prairie voles (microtus ochrogaster) spontaneously care for unfamiliar infants, showing a robust and sustained increase in heart rate in the presence of a pup, thus providing an opportunity to examine the physiology of care-giving in reproductively naïve animals. however, the purpose of such ...201525721742
breaking bonds in male prairie vole: long-term effects on emotional and social behavior, physiology, and neurochemistry.social relationships are essential for many fundamental aspects of life while bond disruption can be detrimental to mental and physical health. male prairie voles form enduring social bonds with their female partners, allowing the evaluation of partner loss on behavior, physiology, and neurochemistry. males were evaluated for partner preference formation induced by 24h of mating, and half were separated from their partner for 4 wk. in experiment 1, partner loss significantly increased anxiety-li ...201424561258
autonomic, behavioral and neuroendocrine correlates of paternal behavior in male prairie voles.socially monogamous prairie voles (microtus ochrogaster) are biparental and alloparental. in the present study, we compared behavioral, cardiovascular and neuroendocrine parameters in male prairie voles with experience caring for pups (fathers), versus reproductively inexperienced virgin males. father and virgins showed generally similar responses to unrelated pups. however, in the fathers studied prior to and during pup exposure, heart rate was lower and respiratory sinus arrhythmia tended to b ...201424534169
does paedomorphosis contribute to prairie vole monogamy?we examined skull morphology in prairie voles (microtus ochrogaster) and meadow voles (m. pennsylvanicus), two closely related species with fundamentally different mating systems, to test the hypothesis that paedomorphosis contributes to the evolution of monogamous mating systems. using several skull measurements, we found that the overall length:width ratio of meadow vole skulls was greater than that of prairie voles suggesting that meadow vole have longer narrower skulls. we then examined whic ...201726594100
sex, drugs, and violence: neuromodulation of attachment and conflict in voles.prairie voles (microtus ochrogaster) are a rodent species that display socially monogamous pair-bonds, a behavior illustrated by several types of social interactions such as mating-induced partner preference, selective aggression toward conspecific strangers, and bi-parental care. therefore, this species has provided an excellent opportunity for the study of pair-bonding and its underlying neurochemical mechanisms. this chapter discusses the utility of this unique rodent in the study of attachme ...201424301199
social partners prevent alcohol relapse behavior in prairie voles.there is robust evidence for a protective role of interpersonal factors such as social support on alcohol relapse, but research on the mechanisms that social factors may be acting on to effectively protect individuals against relapse is lacking. prairie voles are highly social, monogamous rodents that freely self-administer ethanol in high amounts, and are a useful model for understanding social influences on alcohol drinking. here we investigated whether prairie voles can be used to model socia ...201424275014
social recognition is context dependent in single male prairie voles.single males might benefit from knowing the identity of neighbouring males when establishing and defending boundaries. similarly, males should discriminate between individual females if this leads to more reproductive opportunities. contextual social cues may alter the value of learning identity. knowing the identity of competitors that intrude into an animal's territory may be more salient than knowing the identity of individuals on whose territory an animal is trespassing. hence, social and en ...201324273328
hypothalamic oxytocin mediates social buffering of the stress response.while stressful life events can enhance the risk of mental disorders, positive social interactions can propagate good mental health and normal behavioral routines. still, the neural systems that promote these benefits are undetermined. oxytocin is a hormone involved in social behavior and stress; thus, we focus on the impact that social buffering has on the stress response and the governing effects of oxytocin.201424183103
disruption of social bonds induces behavioral and physiological dysregulation in male and female prairie voles.the social disruption of losing a partner may have particularly strong adverse effects on psychological and physiological functioning. more specifically, social stressors may play a mediating role in the association between mood disorders and cardiovascular dysfunction. this study investigated the hypothesis that the disruption of established social bonds between male and female prairie voles would produce depressive behaviors and cardiac dysregulation, coupled with endocrine and autonomic nervo ...201424161576
does mating prevent monogamous males from seeking other females? a study in prairie voles (microtus ochrogaster).male prairie voles form pair bonds under laboratory conditions, but show a variety of mating tactics in nature. we tested them in the laboratory to determine if their decision to reproduce with a single or multiple females is related to how they process sensory information from females. three groups of mated males were tested for their attentiveness toward two females and their odors. males given a choice to investigate a box holding their mate or a box holding a sexually receptive female spent ...201324140461
influence of global atmospheric change on the feeding behavior and growth performance of a mammalian herbivore, microtus ochrogaster.global atmospheric change is influencing the quality of plants as a resource for herbivores. we investigated the impacts of elevated carbon dioxide (co2) and ozone (o3) on the phytochemistry of two forbs, solidago canadensis and taraxacum officinale, and the subsequent feeding behavior and growth performance of weanling prairie voles (microtus ochrogaster) feeding on those plants. plants for the chemical analyses and feeding trials were harvested from the understory of control (ambient air), ele ...201323977345
autonomic substrates of the response to pups in male prairie voles.caregiving by nonparents (alloparenting) and fathers is a defining aspect of human social behavior, yet this phenomenon is rare among mammals. male prairie voles (microtus ochrogaster) spontaneously exhibit high levels of alloparental care, even in the absence of reproductive experience. in previous studies, exposure to a pup was selectively associated with increased activity in oxytocin and vasopressin neurons along with decreased plasma corticosterone. in the present study, physiological, phar ...201323940535
sexual dimorphism in the brain of the monogamous california mouse (peromyscus californicus).sex differences in behavior and morphology are usually assumed to be stronger in polygynous species compared to monogamous species. a few brain structures have been identified as sexually dimorphic in polygynous rodent species, but it is less clear whether these differences persist in monogamous species. california mice are among the 5% or less of mammals that are considered to be monogamous and as such provide an ideal model to examine sexual dimorphism in neuroanatomy. in the present study we ...201323881046
identification of subpopulations of prairie voles differentially susceptible to peer influence to decrease high alcohol intake.peer influences are critical in the decrease of alcohol (ethanol) abuse and maintenance of abstinence. we previously developed an animal model of inhibitory peer influences on ethanol drinking using prairie voles and here sought to understand whether this influential behavior was due to specific changes in drinking patterns and to variation in a microsatellite sequence in the regulatory region of the vasopressin receptor 1a gene (avpr1a). adult prairie voles' drinking patterns were monitored in ...201323847535
prairie voles pair up. 201323783308
histone deacetylase inhibitors facilitate partner preference formation in female prairie voles.in the socially monogamous prairie vole (microtus ochrogaster), mating induces enduring pair-bonds that are initiated by partner preference formation and regulated by a variety of neurotransmitters, including oxytocin, vasopressin and dopamine. we examined potential epigenetic mechanisms mediating pair-bond regulation and found that the histone deacetylase inhibitors sodium butyrate and trichostatin a (tsa) facilitated partner preference formation in female prairie voles in the absence of mating ...201323727821
μ-opioid receptors within subregions of the striatum mediate pair bond formation through parallel yet distinct reward mechanisms.the prairie vole is a socially monogamous rodent that is an excellent animal model for studies of the neurobiology of social attachment. such studies have demonstrated that activation of reward circuitry during social interactions facilitates pair bond formation. within this circuitry, μ-opioid receptors (mors) modulate naturally rewarding behavior in an anatomically segregated manner; mors located throughout the striatum (dorsal striatum, nac core, and the entire nac shell) are implicated in ge ...201323699524
the effects of environmental enrichment on depressive and anxiety-relevant behaviors in socially isolated prairie voles.social isolation is associated with depression, anxiety, and negative health outcomes. environmental enrichment, including environmental and cognitive stimulation with inanimate objects and opportunities for physical exercise, may be an effective strategy to include in treatment paradigms for affective disorders as a function of social isolation. in a rodent model-the socially monogamous prairie vole-we investigated the hypothesis that depression- and anxiety-related behaviors after social isola ...201424804886
drinking alcohol has sex-dependent effects on pair bond formation in prairie voles.alcohol use and abuse profoundly influences a variety of behaviors, including social interactions. in some cases, it erodes social relationships; in others, it facilitates sociality. here, we show that voluntary alcohol consumption can inhibit male partner preference (pp) formation (a laboratory proxy for pair bonding) in socially monogamous prairie voles (microtus ochrogaster). conversely, female pp is not inhibited, and may be facilitated by alcohol. behavior and neurochemical analysis suggest ...201424711424
hypothalamic oxytocin and vasopressin neurons exert sex-specific effects on pair bonding, gregariousness, and aggression in finches.antagonism of oxytocin (ot) receptors (otrs) impairs the formation of pair bonds in prairie voles (microtus ochrogaster) and zebra finches (taenioypygia guttata), and also reduces the preference for the larger of two groups ("gregariousness") in finches. these effects tend to be stronger in females. the contributions of specific peptide cell groups to these processes remain unknown, however. this issue is complicated by the fact that otrs in finches and voles bind not only forms of ot, but also ...201424711411
chemosensory cues affect amygdaloid neurogenesis and alter behaviors in the socially monogamous prairie vole.the current study examined the effects of pheromonal exposure on adult neurogenesis and revealed the role of the olfactory pathways on adult neurogenesis and behavior in the socially monogamous prairie vole (microtus ochrogaster). subjects were injected with a cell proliferation marker [5-bromo-2'-deoxyuridine (brdu)] and then exposed to their own soiled bedding or bedding soiled by a same- or opposite-sex conspecific. exposure to opposite-sex bedding increased brdu labeling in the amygdala (amy ...201424641515
growing up in the family or growing up alone influences behavior and hormones, but not arginine vasopressin receptor 1a expression in male african striped mice.in many species males display alternative reproductive tactics (arts). while males of different tactics differ behaviorally in the field, it is often not known whether these behavioral differences would also occur under standardized laboratory conditions, nor how arts are regulated by the brain. in the present study we kept male african striped mice (rhabdomys pumilio) in captivity either in family groups or solitary, to mimic arts observed in the field. this allowed us to study these males beha ...201424631307
natural variation in early parental care correlates with social behaviors in adolescent prairie voles (microtus ochrogaster).natural variation in early parental care may contribute to long-term changes in behavior in the offspring. here we investigate the role of variable early care in biparental prairie voles (microtus ochrogaster). total amounts of parental care were initially quantified for 24 breeder pairs and pairs were ranked in relation to one another based on total contact. consistency in key components of care suggested a trait-like quality to parental care. based on this ranking, breeder pairs from the top ( ...201323515227
female alternative mating tactics, reproductive success and nonapeptide receptor expression in the social decision-making network.the decision to mate may be one of the most important decisions that animals make. for monogamous species, this decision can carry the added weight of limiting future mating opportunities. the mechanisms that govern these decisions have presumably been shaped by evolution in ways that optimize decision-making processes. in particular, a so-called social decision-making network (sdm) has been proposed, which integrates brain structures comprising the 'social behavior network' with a neural system ...201323500897
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