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aversive motivation and the maintenance of monogamous pair bonding.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 correlate ...201323314526
circulating plasma testosterone during early neonatal life in the socially monogamous and biparental prairie vole (microtus ochrogaster).adult male prairie voles (microtus ochrogaster) are highly gregarious and socially monogamous, which is dissimilar to most other male rodents but reminiscent of many primates, including humans. this has resulted in prairie voles becoming a premier model in which to study the neural and hormonal basis of complex social behaviors, as well as the atypical development of these behaviors. this research is impeded by the complete lack of knowledge about the gonadal steroid environment during early dev ...201322770983
the role of early life experience and species differences in alcohol intake in microtine rodents.social relationships have important effects on alcohol drinking. there are conflicting reports, however, about whether early-life family structure plays an important role in moderating alcohol use in humans. we have previously modeled social facilitation of alcohol drinking in peers in socially monogamous prairie voles. we have also modeled the effects of family structure on the development of adult social and emotional behaviors. here we assessed whether alcohol intake would differ in prairie v ...201222745824
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
generation of induced pluripotent stem cells from the prairie vole.the vast majority of animals mate more or less promiscuously. a few mammals, including humans, utilize more restrained mating strategies that entail a longer term affiliation with a single mating partner. such pair bonding mating strategies have been resistant to genetic analysis because of a lack of suitable model organisms. prairie voles are small mouse-like rodents that form enduring pair bonds in the wild as well as in the laboratory, and consequently they have been used widely to study soci ...201222675440
volume transmission and its different forms in the central nervous system.volume transmission (vt) is a widespread mode of intercellular communication that occurs in the extracellular fluid (ecf) and in the cerebrospinal fluid (csf) of the brain with vt signals moving from source to target cells via energy gradients leading to diffusion and convection (flow). the vt channels are diffuse forming a plexus in the extracellular space, while in wiring transmission (wt) the channels (axons, terminals) are private. the speed is slow (seconds-minutes) in vt while rapid in the ...201323674109
κ-opioid receptors within the nucleus accumbens shell mediate pair bond maintenance.the prairie vole is a socially monogamous species in which breeder pairs typically show strong and selective pair bonds. the establishment of a pair bond is associated with a behavioral transition from general affiliation to aggressive rejection of novel conspecifics. this "selective aggression" is indicative of mate guarding that is necessary to maintain the initial pair bond. in the laboratory, the neurobiology of this behavior is studied using resident-intruder testing. although it is well es ...201222593047
chronic social isolation in the prairie vole induces endothelial dysfunction: implications for depression and cardiovascular disease.humans with depression show impaired endothelium-dependent vasodilation; one recent demonstration of which was in the form of a reduced acetylcholine (ach)-induced relaxation of adrenergically-precontracted small arteries biopsied from older depressed patients. results from such uses of ach in general have been validated as the most predictive marker of endothelium-related cardiovascular diseases. accordingly, we examined vascular reactivity to ach in the socially isolated prairie vole, a new an ...201222469565
social isolation impairs adult neurogenesis in the limbic system and alters behaviors in female prairie voles.disruptions in the social environment, such as social isolation, are distressing and can induce various behavioral and neural changes in the distressed animal. we conducted a series of experiments to test the hypothesis that long-term social isolation affects brain plasticity and alters behavior in the highly social prairie vole (microtus ochrogaster). in experiment 1, adult female prairie voles were injected with a cell division marker, 5-bromo-2'-deoxyuridine (brdu), and then same-sex pair-hou ...201222465453
neuroanatomical distribution of μ-opioid receptor mrna and binding in monogamous prairie voles (microtus ochrogaster) and non-monogamous meadow voles (microtus pennsylvanicus).the opiate system has long been implicated in the rewarding properties of social interactions. in particular, the μ-opioid receptor (mor) mediates multiple forms of social attachment, including the attachment of offspring to the mother and social bonding between mates. we have previously shown that mor in the caudate-putamen is involved in partner preference formation in monogamous prairie voles. here, using in situ hybridization and receptor autoradiography, we mapped in detail the distribution ...201323537838
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
chronic intranasal oxytocin causes long-term impairments in partner preference formation in male prairie voles.oxytocin (ot) is a hormone shown to be involved in social bonding in animal models. intranasal ot is currently in clinical trials for use in disorders such as autism and schizophrenia. we examined long-term effects of intranasal ot given developmentally in the prairie vole (microtus ochrogaster), a socially monogamous rodent, often used as an animal model to screen drugs that have therapeutic potential for social disorders.201323079235
dendritic arbor of neurons in the hypothalamic ventromedial nucleus in female prairie voles (microtus ochrogaster).female mating behavior in rats is associated with hormone-induced changes in the dendritic arbor of neurons in the ventromedial nucleus of the hypothalamus (vmh), particularly the ventrolateral portion. regulation of mating behavior in female prairie voles differs substantially from that in rats; therefore, we examined the dendritic morphology of vmh neurons in this species. sexually naïve adult female prairie voles were housed with a male to activate the females' reproductive endocrine system. ...201323058474
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
exposure to chronic isolation modulates receptors mrnas for oxytocin and vasopressin in the hypothalamus and heart.the goal of our study was to explore the effect of social isolation stress of varying durations on the plasma oxytocin (ot), messenger ribonucleic acid (mrna) for oxytocin receptor (otr), plasma arginine vasopressin (avp) and mrna for v1a receptor of avp (v1ar) expression in the hypothalamus and heart of socially monogamous female and male prairie voles (microtus ochrogaster). continuous isolation for 4 weeks (chronic isolation) increased plasma ot level in females, but not in males. one hour of ...201323439320
correlated basal expression of immediate early gene egr1 and tyrosine hydroxylase in zebrafish brain and downregulation in olfactory bulb after transitory olfactory deprivation.imprinting on kin occurs during the sixth day of larval development in zebrafish and depends on olfactory signals. in rodents, the immediate early gene egr1 is involved in maintaining the dopaminergic phenotype of periglomerular olfactory bulb cells in an activity dependent way. furthermore, egr1 is upregulated in medial amygdalar dopamine cells in some rodents (prairie voles) dependent on social pheromone interactions. thus, we aimed to investigate whether egr1 is involved in imprinting process ...201223022747
exploring the role of intra-nasal oxytocin on the partner preference effect in humans.previous studies with prairie voles suggest that the hormone oxytocin is crucial for bond formation - indicated when a partner preference is formed towards the target vole. in this study, we conduct the first empirical test of whether oxytocin likewise promotes partner preferences in humans. seventy-six undergraduate students received either oxytocin or placebo before being introduced to a male and female persona (via pre-recorded videoclips). one day later, participants were assessed for a part ...201322920910
social housing and alcohol drinking in male-female pairs of prairie voles (microtus ochrogaster).social environment influences alcohol consumption in humans; however, animal models have only begun to address biological underpinnings of these effects.201222903359
is it all in the family? the effects of early social structure on neural-behavioral systems of prairie voles (microtus ochrogaster).the transition to parenthood is generally associated with a reduction in anxiety or anxiety-like behavior across a wide range of species. in some species, juveniles provide supplementary parental care for younger siblings, a behavior known as alloparenting. although the fitness consequences of alloparenting behavior have been a focus of evolutionary research, less is known about how alloparenting behavior impacts affective states. in the socially monogamous prairie vole (microtus ochrogaster), m ...201222561732
associations between innate immune function and ectoparasites in wild rodent hosts.immune function is an important component of host fitness, and high investment in immunity should occur when the benefits outweigh the costs, such as when risk of parasitism is high. we sampled two rodent hosts, white-footed mice (peromyscus leucopus), and prairie voles (microtus ochrogaster), and their tick, flea, and mite ectoparasites. a bacterial killing assay was used to measure the host's innate immune function. we hypothesized that classes of hosts (species, sexes, or age classes) with ov ...201323417097
deltafosb is increased in the nucleus accumbens by amphetamine but not social housing or isolation in the prairie vole.the nucleus accumbens is a key region that mediates aspects of immediate and long-term adaptations to various stimuli. for example, both repeated amphetamine and pair-bonding increase dopamine d1 receptor binding in the nucleus accumbens of the monogamous prairie vole (microtus ochrogaster). this upregulation has significant and stimulus-dependent behavioral consequences. a promising candidate for these and other adaptations is the transcription factor δfosb. δfosb is a highly stable protein tha ...201222450232
buffering and plasticity in vital rates of oldfield rodents.1. under the hypothesis of environmental buffering, populations are expected to minimize the variance of the most influential vital rates; however, this may not be a universal principle. species with a life span <1 year may be less likely to exhibit buffering because of temporal or seasonal variability in vital rate sensitivities. further, plasticity in vital rates may be adaptive for species in a variable environment with reliable cues. 2. we tested for environmental buffering and plasticity in ...201222375923
neuroendocrine and behavioural responses to exposure to an infant in male prairie voles.paternal behaviour and pair-bond formation are defining characteristics of social monogamy. however, in comparison to pair-bonding, the endocrine factors associated with the male care of young are not well studied. in the present study, plasma concentrations of oxytocin, vasopressin and corticosterone (cort) were measured in reproductively naïve male prairie voles as a function of exposure to an infant or control manipulations (i.e. handling or exposure to a wooden dowel). plasma oxytocin concen ...201222356098
oxytocin receptor density is associated with male mating tactics and social monogamy.despite its well-described role in female affiliation, the influence of oxytocin on male pairbonding is largely unknown. however, recent human studies indicate that this nonapeptide has a potent influence on male behaviors commonly associated with monogamy. here we investigated the distribution of oxytocin receptors (otr) throughout the forebrain of the socially monogamous male prairie vole (microtus ochrogaster). because males vary in both sexual and spatial fidelity, we explored the extent to ...201222285648
monogamous and promiscuous rodent species exhibit discrete variation in the size of the medial prefrontal cortex.limbic-associated cortical areas, such as the medial prefrontal and retrosplenial cortex (mpfc and rs, respectively), are involved in the processing of emotion, motivation, and various aspects of working memory and have been implicated in mating behavior. to determine whether the independent evolution of mating systems is associated with a convergence in cortical mechanisms, we compared the size of mpfc and rs between the monogamous prairie vole (microtus ochrogaster) and the promiscuous meadow ...201222759599
the integration of depressive behaviors and cardiac dysfunction during an operational measure of depression: investigating the role of negative social experiences in an animal model.there is a bidirectional association between depression and cardiovascular disease. the neurobiological mechanisms underlying this association may involve an inability to cope with disrupted social bonds. this study investigated in an animal model the integration of depressive behaviors and cardiac dysfunction after a disrupted social bond and during an operational measure of depression, relative to the protective effects of intact social bonds.201722753634
bac-based sequencing of behaviorally-relevant genes in the prairie vole.the prairie vole (microtus ochrogaster) is an important model organism for the study of social behavior, yet our ability to correlate genes and behavior in this species has been limited due to a lack of genetic and genomic resources. here we report the bac-based targeted sequencing of behaviorally-relevant genes and flanking regions in the prairie vole. a total of 6.4 mb of non-redundant or haplotype-specific sequence assemblies were generated that span the partial or complete sequence of 21 beh ...201222238603
developmental exposure to a serotonin agonist produces subsequent behavioral and neurochemical changes in the adult male prairie vole.autistic spectrum disorders (asds) are classified as pervasive developmental disorders characterized by abnormalities in various cognitive and behavioral functions. although exact underlying causes are still unknown, nearly 30% of autistic patients show elevated blood levels of serotonin (5-ht) and, therefore, various genetic and environmental factors that are known to elevate 5-ht levels may play a role in the development of asds. in the present study, we used the socially monogamous male prair ...201221958679
neonatal exposure to the d1 agonist skf38393 inhibits pair bonding in the adult prairie vole.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 trea ...201121918384
chronic inorganic mercury exposure induces sex-specific changes in central tnfα expression: importance in autism?mercury is neurotoxic and increasing evidence suggests that environmental exposure to mercury may contribute to neuropathologies including alzheimer's disease and autism spectrum disorders. mercury is known to disrupt immunocompetence in the periphery, however, little is known about the effects of mercury on neuroimmune signaling. mercury-induced effects on central immune function are potentially very important given that mercury exposure and neuroinflammation both are implicated in certain neur ...201121906657
synergistic influences of phase, density, and climatic variation on the dynamics of fluctuating populations.although ecologists have long recognized that certain mammalian species exhibit high-amplitude, often multiannual, fluctuations in abundance, their causes have remained poorly understood and the subject of intense debate. a key contention has been the relative role of density-dependent and density-independent processes in governing population dynamics. we applied capture-mark-recapture analysis to 25 years of monthly trapping data from a fluctuating prairie vole microtus ochrogaster population i ...201121905434
mating increases male's interest in other females: a cognitive study in socially monogamous prairie voles (microtus ochrogaster).to determine whether socio-sexual interactions with females influence the male prairie vole's cognitive processing, three groups of males were simultaneously exposed to sensory stimuli of a control and a focal female then tested for their behavioral and neuronal responsiveness to the female cues. from the control female, all males received distal cues. from the focal female, the unmated males received distal cues, the unmated-contact males received all cues but did not mate with her, and the mat ...201121888956
cart peptide following social novelty in the prairie vole (microtus ochrogaster).prairie voles (microtus ochrogaster) are monogamous rodents that display high levels of affiliative behaviors, including pair-bonding, biparental care, and cooperative breeding. species differences in basal cocaine- and amphetamine-regulated transcript (cart) mrna and peptide expression have been found between prairie voles and polygamous meadow voles. therefore, we hypothesized that the cart system may play a role in the regulation of social behavior in this species. male and female adult prair ...201121871610
central vasopressin v1a receptor activation is independently necessary for both partner preference formation and expression in socially monogamous male prairie voles.the neuropeptide arginine vasopressin (avp) modulates a variety of species-specific social behaviors. in socially monogamous male prairie voles, avp acts centrally via vasopressin v1a receptor (v1ar) to facilitate mating induced partner preferences. the display of a partner preference requires at least 2 temporally distinct processes: social bond formation as well as its recall, or expression. studies to date have not determined in which of these processes v1ar acts to promote partner preference ...201020141291
peripheral oxytocin administration buffers autonomic but not behavioral responses to environmental stressors in isolated prairie voles.negative social experiences such as social stressors and isolation influence mental and physical illnesses, including affective disorders and heart disease. studies focused on socially monogamous prairie voles can provide insight into neurobiological systems that underlie the consequences of negative social interactions. female prairie voles were exposed to 28 days of social isolation or pairing with a female sibling (control). voles were administered daily oxytocin [20 μg/50 μl, subcutaneous (s ...201221854168
increasing oxytocin receptor expression in the nucleus accumbens of pre-pubertal female prairie voles enhances alloparental responsiveness and partner preference formation as adults.oxytocin receptors (oxtr) in the nucleus accumbens (nacc) promote alloparental behavior and partner preference formation in female prairie voles. within the nacc there is significant individual variation in oxtr binding and virgin juvenile and adult females with a high density of oxtr in the nacc display an elevated propensity to engage in alloparental behavior toward novel pups. over-expression of oxtr in the nacc of adult female prairie voles using viral vector gene transfer facilitates partne ...201121851821
activation of μ-opioid receptors in the dorsal striatum is necessary for adult social attachment in monogamous prairie voles.despite significant evidence that opioids are involved in attachment by mediating social reward and motivation, the role of opioids in the formation of adult social attachments has not been explored. we used the socially monogamous prairie vole (microtus ochrogaster) to explore the role of endogenous opioids in social bonding by examining partner preference formation in female prairie voles. we hypothesized that μ-opioid receptors (mors) in the striatum have a critical role in partner preference ...201121734650
the value of unusual animal models for alcohol research: a commentary on: anacker, loftis, and ryabinin, "alcohol intake in prairie voles is influenced by the drinking level of a peer".the recent study by anacker, loftis, and ryabinin used a novel animal model, the prairie vole, to investigate social effects on drinking. their finding that same-sex peers modulate their drinking to match each other has intriguing implications for the fields of alcohol research as well as research on social relationships.201121651584
social bonding decreases the rewarding properties of amphetamine through a dopamine d1 receptor-mediated mechanism.although the protective effects of social bonds on drug use/abuse have been well documented, we know little about the underlying neural mechanisms. using the prairie vole (microtus ochrogaster)--a socially monogamous rodent that forms long-term pair bonds after mating--we demonstrate that amphetamine (amph) conditioning induced a conditioned place preference (cpp) in sexually naive (sn), but not pair-bonded (pb), males. although amph treatment induced a similar magnitude of dopamine release in t ...201121632917
effects of social isolation on mrna expression for corticotrophin-releasing hormone receptors in prairie voles.previous studies have demonstrated that various type of stressors modulate messenger ribonucleic acid (mrna) for type 1 corticotropin-releasing hormone (crh) receptor (crh-r1 mrna) and type 2 crh receptor (crh-r2 mrna). the purpose of this study was to explore the effect of social isolation stress of varying durations on the crh, crh-r1 and crh-r2 mrnas expression in the hypothalamus, hippocampus and pituitary of socially monogamous female and male prairie voles (microtus ochrogaster). isolation ...201121095063
amphetamine alters behavior and mesocorticolimbic dopamine receptor expression in the monogamous female prairie vole.we have recently established the socially monogamous prairie vole (microtus ochrogaster) as an animal model with which to investigate the involvement of mesocorticolimbic dopamine (da) in the amphetamine (amph)-induced impairment of social behavior. as the majority of our work, to date, has focused on males, and sex differences are commonly reported in the behavioral and neurobiological responses to amph, the current study was designed to examine the behavioral and neurobiological effects of amp ...201120933511
does fertility trump monogamy?monogamous animals face an interesting dilemma: if and when to terminate a nonproductive relationship. to address this issue, we asked whether reproductive compatibility is a criterion for maintaining a monogamous pair-bond between mates. prairie voles (microtus ochrogaster), are small rodents that form long-term, monogamous pair-bonds evidenced by a strong preference for their familiar partners, and thus are an excellent model animal in which to study mate-fidelity. accordingly, we examined par ...201020823948
stability and potential inheritance of infanticidal behavior in prairie voles.naïve female prairie voles show significant variability in their behavioral response to newborns. we investigated whether that behavioral response (a) was related to the quality of postpartum maternal behavior; (b) was affected by postpartum maternal experience; and (c) could be selectively bred. the behavior of females was recorded in three conditions: as naïve in a nonreproductive context, as single lactating (no male present), and as experienced mother in a nonreproductive context. finally, f ...201020607791
oxytocin and same-sex social behavior in female meadow voles.the neuropeptide oxytocin (ot) has been implicated in a range of mammalian reproductive and social behaviors including parent-offspring bonding and partner preference formation between socially monogamous mates. its role in mediating non-reproductive social relationships in rodents, however, remains largely unexplored. we examined whether ot facilitates same-sex social preferences between female meadow voles-a species that forms social nesting groups in short, winter-like day lengths. in contras ...201020580660
prairie voles as a novel model of socially facilitated excessive drinking.social relationships strongly affect alcohol drinking in humans. traditional laboratory rodents do not exhibit social affiliations with specific peers, and cannot adequately model how such relationships impact drinking. the prairie vole is a socially monogamous rodent used to study social bonds. the present study tested the prairie vole as a potential model for the effects of social affiliations on alcohol drinking. same-sex adult sibling prairie voles were paired for five days, and then either ...201120579002
intergenerational transmission of the behavioral consequences of early experience in prairie voles.we examined intergenerational and epigenetic effects of early handling manipulations on the social behavior of the prairie vole (microtus ochrogaster), a monogamous rodent. laboratory-born parents and their newborn pups were assigned to either a man0 "zero handling" manipulation (transfer with a cup during weekly cage changes) or a man1 "gloved handling" manipulation (transfer with a gloved hand). previous studies from our laboratory (bales et al., 2007) showed that man0 juvenile males that rece ...201020457234
autonomic predictors of recovery following surgery: a comparative study.although heart rate and temperature are continuously monitored in patients during recovery following surgery, measures that extract direct manifestations of neural regulation of autonomic circuits from the beat-to-beat heart rate may be more sensitive to outcome. we explore the relationship between features of autonomic regulation and survival in the prairie vole, a small mammal, with features of vagal regulation of the heart similar to humans. cardiac vagal regulation is manifested in the beat- ...201020451468
female prairie vole mate-choice is affected by the males' birth litter composition.experimental testing and retrospective examination of breeding records were used to examine the influence of sex composition and/or size of males' birth litters on female mate-choice. sexually naïve female prairie voles (microtus ochrogaster) avoided males derived from all-male litters, but showed no preference for, or aversion to, males from single-male litters or from more typical mixed-sex litters. examination of the pregnancy status of females after two weeks of pairing with a male allowed u ...201020434472
chronic metals ingestion by prairie voles produces sex-specific deficits in social behavior: an animal model of autism.we examined the effects of chronic metals ingestion on social behavior in the normally highly social prairie vole to test the hypothesis that metals may interact with central dopamine systems to produce the social withdrawal characteristic of autism. relative to water-treated controls, 10 weeks of chronic ingestion of either hg(++) or cd(++) via drinking water significantly reduced social contact by male voles when they were given a choice between isolation or contact with an unfamiliar same-sex ...201020433873
social novelty increases tyrosine hydroxylase immunoreactivity in the extended olfactory amygdala of female prairie voles.the monogamous social behaviors of prairie voles (microtus ochrogaster) require olfactory inputs, which are processed by the posterodorsal medial amygdala (meapd) and principal bed nucleus of the stria terminalis (pbst). the male prairie vole meapd and pbst contain hundreds of cells densely immunoreactive for tyrosine hydroxylase (th-ir). female prairie voles have relatively few of these cells, but we previously found that the number of these th-ir cells is greatly increased in females by exogen ...201020381508
d2 antagonist during development decreases anxiety and infanticidal behavior in adult female prairie voles (microtus ochrogaster).on postnatal day 8, prairie vole pups were randomly assigned a treatment of 1mg/kg skf38393 (d1 agonist), quinpirole (d2 agonist), sch23390 (d1 antagonist), eticlopride (d2 antagonist), or saline vehicle. as adults, females treated with eticlopride exhibited reduced anxiety-like behavior in an elevated plus maze and a reduction in infanticidal behavior. these behavioral effects were not seen in males. these data demonstrate that a single exposure to a d2 antagonist during development can have pe ...201020152865
nucleus accumbens dopamine mediates amphetamine-induced impairment of social bonding in a monogamous rodent species.the prairie vole (microtus ochrogaster) is a socially monogamous rodent species that forms pair bonds after mating, a behavior in which central dopamine (da) has been implicated. here, we used male prairie voles to examine the effects of drug exposure on pair bonding and related neural circuitry. in our first experiment, amphetamine (amph) motivated behavior was examined using a conditioned place preference (cpp) paradigm and was shown to be mediated by activation of d1-like da receptors. next, ...201020080553
the prairie vole: an emerging model organism for understanding the social brain.unlike most mammalian species, the prairie vole is highly affiliative, forms enduring social bonds between mates and displays biparental behavior. over two decades of research on this species has enhanced our understanding of the neurobiological basis not only of monogamy, social attachment and nurturing behaviors but also other aspects of social cognition. because social cognitive deficits are hallmarks of many psychiatric disorders, discoveries made in prairie voles can direct novel treatment ...201020005580
anterior hypothalamic vasopressin regulates pair-bonding and drug-induced aggression in a monogamous rodent.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 ma ...200919858480
organizational effects of oxytocin on serotonin innervation.oxytocin (ot) has an organizational effect within the central nervous system and can have long-lasting effects on the expression of social behavior. ot has recently been implicated in modulating the release of serotonin through activation of receptors in the raphe nuclei. here we test the hypothesis that ot can have an organizational effect on the serotonergic system. male prairie voles received an intraperitoneal injection on postnatal day 1 with 3.0 or .3 µg ot, an ot antagonist, or a saline c ...201221594870
alcohol intake in prairie voles is influenced by the drinking level of a peer.peer interactions can have important effects on alcohol-drinking levels, in some cases increasing use, and in other cases preventing it. in a previous study, we have established the prairie vole as a model animal for the effects of social relationships on alcohol intake and have observed a correlation of alcohol intake between individual voles housed together as pairs. here, we investigated this correlated drinking behavior, hypothesizing that 1 animal alters its alcohol intake to match the drin ...201121575019
inorganic mercury exposure in prairie voles (microtus ochrogaster) alters the expression of toll-like receptor 4 and activates inflammatory pathways in the liver in a sex-specific manner.environmental exposure to mercury can cause a number of adverse effects in humans including the disruption of endocrine function that may result in sex-specific effects. the present study was designed to characterize sex-specific effects of chronic inorganic mercury exposure on toll-like receptor (tlr) 2 and tlr4 and inflammatory signaling in the liver of prairie voles (microtus ochrogaster). following 10 weeks of exposure to mercury via drinking water, effects on protein expression levels of tl ...201221558144
neuroanatomical projections of the species-specific tyrosine hydroxylase-immunoreactive cells of the male prairie vole bed nucleus of the stria terminalis and medial amygdala.the principal nucleus of the bed nucleus of the stria terminalis (bstpr) and posterodorsal part of the medial amygdalar nucleus (meapd) are densely interconnected sites transmitting olfactory information to brain areas mediating sociosexual behaviors. in male prairie voles (microtus ochrogaster), the bstpr and meapd contain hundreds of cells densely immunoreactive for tyrosine hydroxylase (th). such tremendous numbers of th-immunoreactive (th-ir) cells do not exist in other rodents examined, and ...201121546771
d-cycloserine facilitates socially reinforced learning in an animal model relevant to autism spectrum disorders.there are no drugs that specifically target the social deficits of autism spectrum disorders (asd). this may be due to a lack of behavioral paradigms in animal models relevant to asd. partner preference formation in the prairie vole represents a social cognitive process involving socially reinforced learning. d-cycloserine (dcs) is a cognitive enhancer that acts at the n-methyl-d-aspartate receptor to promote learning. if dcs enhances socially reinforced learning in the partner preference paradi ...201121481844
avpr1a length polymorphism is not associated with either social or genetic monogamy in free-living prairie voles.recent discoveries of single-gene influences on social behaviour have generated a great deal of interest in the proximate mechanisms underlying the expression of complex behaviours. length polymorphism in a microsatellite in the regulatory region of the gene encoding the vasopressin 1a receptor (avpr1a) has been associated with both inter- and intra-specific variation in socially monogamous behaviour in voles (genus microtus) under laboratory conditions. here, we evaluate the relationship betwee ...201121442019
24-hour autonomic dysfunction and depressive behaviors in an animal model of social isolation: implications for the study of depression and cardiovascular disease.to investigate the hypothesis that long-term social isolation in an animal model would produce depression-relevant behaviors and disruptions in the 24-hour autonomic and activity parameters, and to further demonstrate the utility and validity of an animal model for the study of social environment, behavior, and autonomic function. converging evidence from both experimental and epidemiological studies indicates that there is a bidirectional association between depression and cardiovascular diseas ...201121097661
sex steroids are necessary in the second postnatal week for the expression of male alloparental behavior in prairie voles (microtus ochragaster).sex steroids play a significant role in organizing male social behavior, which is associated with low levels of pro-social behavior and high levels of aggression. however, the role of steroids in organizing behavior in highly social males is unclear. the authors tested the hypothesis that low levels of sex steroids facilitate the expression of pro-social behavior in male prairie voles (microtus ochragaster), predicting that inhibition of testosterone and estradiol would reduce spontaneous-allopa ...200919824762
polymorphism at the avpr1a locus in male prairie voles correlated with genetic but not social monogamy in field populations.integrative studies of genetics, neurobiology and behaviour indicate that polymorphism in specific genes contributes to variation observed in some complex social behaviours. the neuropeptide arginine vasopressin plays an important role in the regulation of a variety of social behaviours, including social attachment of males to females, through its action on the vasopressin 1a receptor (v1ar). in socially monogamous prairie voles (microtus ochrogaster), polymorphism in the length of microsatellit ...200919821904
the impact of early life family structure on adult social attachment, alloparental behavior, and the neuropeptide systems regulating affiliative behaviors in the monogamous prairie vole (microtus ochrogaster).early social attachments lie at the heart of emotional and social development in many mammals, including humans. in nature, monogamous prairie voles (microtus ochrogaster) experience considerable natural variation in early social attachment opportunities due to differences in family structure [e.g., single-mothers (sm), solitary breeding pairs, and communal groups]. we exploited some of this natural variation in family structure to examine the influence of early social environment on the develop ...200919753327
alloparenting experience affects future parental behavior and reproductive success in prairie voles (microtus ochrogaster).various hypotheses have been proposed to explain the function of alloparental behavior in cooperatively breeding species. we examined whether alloparental experience as juveniles enhanced later parental care and reproductive success in the prairie vole (microtus ochrogaster), a cooperatively breeding rodent. juveniles cared for one litter of siblings (1ex), two litters of siblings (2ex) or no siblings (0ex). as adults, these individuals were mated to other 0ex, 1ex or 2ex voles, yielding seven d ...201019732810
dopamine regulation of social choice in a monogamous rodent species.there is growing appreciation that social decision making in humans is strongly influenced by hedonic and emotional processing. the field of social neuroeconomics has shown that neural systems important for reward are associated with social choice and social preferences in humans. here, we show that the neurobiology of social preferences in a monogamous rodent species, the prairie vole, is also regulated by neural systems involved in reward and emotional processing. specifically, we describe how ...200919707518
costs of pair-bonding and paternal care in male prairie voles (microtus ochrogaster).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 prairi ...200919576236
sexual dimorphism and hormone responsiveness in the spinal cord of the socially monogamous prairie vole (microtus ochrogaster).prairie voles (microtus ochrogaster) are exceptional among rodents in that many aspects of their brain and behavior are not masculinized by exogenous aromatizable androgens. however, the sexually differentiated endpoints studied to date rely on estrogenic mechanisms in other mammals. we examined whether sexual differentiation of an androgen receptor-dependent sex difference would be similarly distinct in prairie voles. male mammals have more and larger motoneurons projecting to perineal muscles ...200919575447
oxytocin protects against negative behavioral and autonomic consequences of long-term social isolation.positive social interactions and social support may protect against various forms of mental and physical illness, although the mechanisms for these effects are not well identified. the socially monogamous prairie vole, which--like humans--forms social bonds and displays high levels of parasympathetic activity, has provided a useful model for investigating neurobiological systems that mediate the consequences of sociality. in the present study, adult female prairie voles were exposed to social is ...200919553027
consequences of early experiences and exposure to oxytocin and vasopressin are sexually dimorphic.in the socially monogamous prairie vole, we have observed that small changes in early handling, as well as early hormonal manipulations can have long-lasting and sexually dimorphic effects on behavior. these changes may be mediated in part by changes in parental interactions with their young, acting on systems that rely on oxytocin (ot) and arginine vasopressin (avp). knowledge of both endogenous and exogenous influences on systems that rely on ot and avp may be helpful in understanding sexually ...200919546570
social environment alters central distribution of estrogen receptor alpha in juvenile prairie voles.it is well established that social environment, particularly isolation, has a significant impact on social behaviors and neuroendocrine responses. estrogen receptor alpha (eralpha) expression in limbic structures and associated nuclei is related to the display of social behaviors. we hypothesized that the stress of isolation would cause changes in the pattern of eralpha expression in the brain. using a highly social (typically monogamous and biparental) rodent species, the prairie vole (microtus ...200919539635
social contact elicits immediate-early gene expression in dopaminergic cells of the male prairie vole extended olfactory amygdala.male prairie voles (microtus ochrogaster) are a valuable model in which to study the neurobiology of sociality because, unlike most mammals, they pair bond after mating and display paternal behaviors. research on the regulation of these social behaviors has highlighted dopamine (da) neurotransmission in both pair bonding and parenting. we recently described large numbers of dopaminergic cells in the male prairie vole principal nucleus of the bed nucleus of the stria terminalis (pbst) and postero ...200919524021
amphetamine effects in microtine rodents: a comparative study using monogamous and promiscuous vole species.we compared amphetamine-induced dopamine release in the nucleus accumbens of vole species that exhibit differing mating systems to examine potential interactions between social organization and substance abuse. we found no species or regional differences in basal extracellular dopamine, however, monogamous voles had greater and longer-lasting increases in extracellular dopamine after amphetamine treatment than did promiscuous voles. we then examined whether amphetamine-induced increase in extrac ...200717706877
social isolation modulates corticotropin-releasing factor type 2 receptor, urocortin 1 and urocortin 2 mrnas expression in the cardiovascular system of prairie voles.the purpose of the present study was to examine the effect of social isolation stress on the expression of messengers ribonucleic acid (mrnas) for corticotropin-releasing factor receptor type 2 (crf2 receptor), urocortin 1 (ucn 1) and urocortin 2 (ucn 2) in the cardiovascular system of female and male prairie voles (microtus ochrogaster). isolation for 1 h (single isolation) or 1 h of isolation every day for 4 weeks (repeated isolation) was followed by a marked increase in plasma corticosterone ...200919452635
androgenic and oestrogenic influences on tyrosine hydroxylase-immunoreactive cells of the prairie vole medial amygdala and bed nucleus of the stria terminalis.the posterodorsal medial amygdala (meapd) and principal nucleus of the bed nucleus of the stria terminalis (pbst) are densely interconnected sites integrating steroid hormone and olfactory information necessary for sociosexual behaviours in many rodents. our laboratory recently reported sexually dimorphic populations of cells containing tyrosine hydroxylase (th) located in the meapd and pbst of prairie voles (microtus ochrogaster), with males having many more th-immunoreactive (-ir) cells in the ...201020136687
estrogen receptor-alpha in the bed nucleus of the stria terminalis regulates social affiliation in male prairie voles (microtus ochrogaster).estrogen receptor alpha (eralpha) typically masculinizes male behavior, while low levels of eralpha in the medial amygdala (mea) and the bed nucleus of the stria terminalis (bst) are associated with high levels of male prosocial behavior. in the males of the highly social prairie vole (microtus ochrogaster), increasing eralpha in the mea inhibited the expression of spontaneous alloparental behavior and produced a preference for novel females. to test for the effects of increased eralpha in the b ...201020111713
post-weaning social isolation alters anxiety-related behavior and neurochemical gene expression in the brain of male prairie voles.stressful social experiences early in life, such as maternal separation and social isolation, have enduring effects on the development of the brain and behavior. in the present study in socially monogamous male prairie voles (microtus ochrogaster), we found that following 6 weeks of social isolation after weaning males spent more time in the closed arms and less time in the open arms during an elevated plus maze (epm) test, moved more frequently from central to peripheral squares in an open fiel ...200919429056
connections of auditory and visual cortex in the prairie vole (microtus ochrogaster): evidence for multisensory processing in primary sensory areas.in prairie voles, primary sensory areas are dominated by neurons that respond to one sensory modality, but some neurons also respond to stimulation of other modalities. to reveal the anatomical substrate for these multimodal responses, we examined the connections of the primary auditory area + the anterior auditory field (a1 + aaf), the temporal anterior area (ta), and the primary visual area (v1). a1 + aaf had intrinsic connections and connections with ta, multimodal cortex (mm), v1, and primar ...201019395525
variation in oxytocin receptor density in the nucleus accumbens has differential effects on affiliative behaviors in monogamous and polygamous voles.oxytocin receptors in the nucleus accumbens have been implicated in the regulation of alloparental behavior and pair bond formation in the socially monogamous prairie vole. oxytocin receptor density in the nucleus accumbens is positively correlated with alloparenting in juvenile and adult female prairie voles, and oxytocin receptor antagonist infused into the nucleus accumbens blocks this behavior. furthermore, prairie voles have higher densities of oxytocin receptors in the accumbens than nonmo ...200919193878
social investigation in a memory task relates to natural variation in septal expression of oxytocin receptor and vasopressin receptor 1a in prairie voles (microtus ochrogaster).arginine vasopressin (avp) and oxytocin (ot) influence social behavior and cognitive processes and may explain some of the variance associated with individual differences in behavior. although great focus has been placed on the roles of these peptides in learning and memory, less attention has been given to the receptors to which they bind. the authors exposed male prairie voles (microtus ochrogaster) to novel females in a multitrial social recognition test to investigate whether individual diff ...200919824764
stress differentially modulates mrna expression for corticotrophin-releasing hormone receptors in hypothalamus, hippocampus and pituitary of prairie voles.this study compares the effect of an acute stressor (restraint for 1h) versus a chronic stressor (social isolation for 4 weeks) on the expression of mrnas for corticotropin-releasing hormone (crh), crh receptor type 1 (crh-r1) and type 2 (crh-r2) in the hypothalamus, hippocampus and pituitary of socially monogamous female prairie voles (microtus ochrogaster). animals were studied immediately following a stressor or as a function of repairing with a familiar sibling. despite elevated expression o ...200919185916
neuroendocrinology of social behavior.discovering the hormonal and neural mechanisms that promote affiliative social behavior is a high priority in behavioral neuroscience. although studies with standard laboratory rodents have afforded many important insights, exciting advances are also occurring through comparative research with nonstandard species that vary in sociality or form socially monogamous pair bonds, work that is often informed by an explicitly evolutionary perspective. research with prairie voles has examined the roles ...200919106448
mercury and methylmercury accumulation and excretion in prairie voles (microtus ochrogaster) receiving chronic doses of methylmercury.methylmercury cation (mehg) and divalent mercury (hg++) accumulation in liver, kidney, and brain were quantified in prairie voles (microtus ochrogaster) at 0, 3, 6, and 12 weeks during chronic exposure to aqueous mehg. dose groups received deionized water or aqueous solutions containing 9, 103, or 920 ng mehg/ml. our study presents temporal patterns of hg++ and mehg concentrations in organ tissues and makes inter-tissue comparisons at each time point to illustrate the accumulation and distributi ...200717364240
in three brain regions central to maternal behaviour, neither male nor female phodopus dwarf hamsters show changes in oestrogen receptor alpha distribution with mating or parenthood.oestrogen receptor (er)alpha immunoreactivity in three brain regions relevant to maternal behaviour (medial preoptic area, bed nucleus of the stria terminalis and medial amygdala) was measured in two species of dwarf hamster that both mate during a postpartum oestrous but differ in expression of paternal behaviour. male and female phodopus campbelli and phodopus sungorus were sampled as sexually naive adults, following mating to satiety, and as new parents. in all brain regions, females expresse ...200819094078
the crf system mediates increased passive stress-coping behavior following the loss of a bonded partner in a monogamous rodent.social relationships significantly influence physiology and behavior, including the hypothalamo-pituitary-adrenal axis, anxiety, and mental health. disruption of social bonds through separation or death often results in profound grieving, depression, and physical illness. as the monogamous prairie vole forms enduring, selective pair bonds with the mating partner, they provide an animal model to study the physiological consequences of pair bonding and, thus, the loss of the bonded partner. male p ...200918923404
variation in neural v1ar predicts sexual fidelity and space use among male prairie voles in semi-natural settings.although prairie voles (microtus ochrogaster) are socially monogamous, males vary in both sexual and spatial fidelity. most males form pairbonds, cohabit with one female, and defend territories. wandering males, in contrast, have expansive home ranges that overlap many males and females. in the laboratory, pairing is regulated by arginine vasopressin and its predominant cns receptor, vasopressin 1a receptor (v1ar). we investigated individual differences in forebrain v1ar expression of male prair ...200818212120
field tests of cis-regulatory variation at the prairie vole avpr1a locus: association with v1ar abundance but not sexual or social fidelity.the neuropeptide vasopressin and its receptor v1ar are broadly implicated in social behavior and play a central role in several key aspects of male mating tactics in voles. in the prairie vole, a microsatellite in the cis-regulatory region of the gene encoding v1ar (avpr1a) provides a potential genetic basis for individual variation in neural phenotype and behavior; recent studies found that allele length predicts v1ar expression and male social attachment in the laboratory. here, we explore the ...200818722379
oxytocin, vasopressin and sociality.the neurobiology of social behaviour is interwoven with autonomic, endocrine and other homoeostatic processes responsible for the adaptive functions of reproduction and survival. young mammals are dependent on their mothers for nourishment, and the interaction between the mother and infant may be a physiological and neuroendocrine prototype for mammalian sociality. although these adaptive functions of the mother-infant social behavioural dyad are obvious, adult social interactions, including soc ...200818655893
sex differences and effects of neonatal aromatase inhibition on masculine and feminine copulatory potentials in prairie voles.copulatory behaviors in most rodents are highly sexually dimorphic, even when circulating hormones are equated between the sexes. prairie voles (microtus ochrogaster) are monomorphic in their display of some social behaviors, including partner preferences and parenting, but differences between the sexes in their masculine and feminine copulatory behavior potentials have not been studied in detail. furthermore, the role of neonatal aromatization of testosterone to estradiol on the development of ...200818378236
opposing regulation of pair bond formation by camp signaling within the nucleus accumbens shell.the formation of monogamous pair bonds, by prairie voles, is facilitated by activation of dopamine (da) d2-like, but not d1-like, receptors within the nucleus accumbens (nacc) shell. because da exerts opposing regulation of camp production depending on the subtype of receptor activated, we tested the hypothesis that da regulation of pair bond formation is mediated via the camp signaling cascade. consistent with activation of d2-like receptors, decreasing camp signaling, by blocking camp binding ...200718045929
social isolation in prairie voles induces behaviors relevant to negative affect: toward the development of a rodent model focused on co-occurring depression and anxiety.recent evidence suggests substantial overlap between mood and anxiety disorders, both in clinical presentation and associated features. a theoretical framework to account for this overlap focuses on negative affectivity, defined as the disposition to experience negative emotional states, including fear, sadness, and guilt. this model has been successful in explaining the co-occurrence of depressive and anxiety disorders in humans. as a next step, development of an animal model focused on both de ...200817935206
pup exposure elicits hippocampal cell proliferation in the prairie vole.the onset of parental behavior has profound and enduring effects on behavior and neurobiology across a variety of species. in some cases, mere exposure to a foster neonate (and a subsequent parental response) can have similar effects. in the present experiment, we exposed adult male and female prairie voles (microtus ochrogaster) to two foster pups for 20 min and quantified cell proliferation in the dentate gyrus of the hippocampus (dg), medial amygdala (mea) and cortical amygdala (cora). prairi ...200817913255
gene regulation as a modulator of social preference in voles.most mammalian species are nonmonogamous: the female alone cares for the young and males and females do not share nest sites. within the genus microtus, there exists ample diversity in social structure for neuroethological and neurobiological investigation. prairie voles (microtus ochrogaster) are socially monogamous: both the males and females contribute to care of the young within a shared nest site as a breeding pair through multiple breeding seasons. closely related species such as the monta ...200717888796
urocortin ii increases spontaneous parental behavior in prairie voles (microtus ochrogaster).stress and anxiety play a role in many psychological processes including social behavior. the present study examines the effects of urocortin ii (ucn ii) on spontaneous parental behavior in adult prairie voles (microtus ochrogaster). ucn ii was found to increase passive parental behavior in voles while not affecting any stress-related measures. delineating the mechanism of this change will aid in our understanding of the regulation of parenting.200817888526
female-directed aggression predicts paternal behavior, but female prairie voles prefer affiliative males to paternal males.in the socially monogamous prairie vole, microtus ochrogaster, male affiliation and parental care are influenced by the neuropeptide arginine vasopressin and expression of its receptor v1ar. if parental care and adult affiliation can be considered a behavioral syndrome, females might use male affiliative behavior as a cue to choose a good father. we investigated three questions: (1) do females prefer affiliative males; (2) do males that are affiliative with females demonstrate paternal behavior ...200817878716
modulation of cardiac oxytocin receptor and estrogen receptor alpha mrnas expression following neonatal oxytocin treatment.oxytocin (ot) is known for its role in reproduction. however, evidence has emerged suggesting its involvement in the regulation of the cardiovascular system. here we examine the hypothesis that neonatal exposure to ot can have both short-term and long-lasting consequences on gene expression in heart tissue. on the first day of postnatal life, female and male prairie voles (microtus ochrogaster) were randomly assigned to receive one of following treatments: 50 microl i.p. injection of (a) 3 micro ...200717873327
social isolation induces behavioral and neuroendocrine disturbances relevant to depression in female and male prairie voles.supportive social interactions may be protective against stressors and certain mental and physical illness, while social isolation may be a powerful stressor. prairie voles are socially monogamous rodents that model some of the behavioral and physiological traits displayed by humans, including sensitivity to social isolation. neuroendocrine and behavioral parameters, selected for their relevance to stress and depression, were measured in adult female and male prairie voles following 4 weeks of s ...201617825994
the organizational effects of oxytocin on the central expression of estrogen receptor alpha and oxytocin in adulthood.previous studies have demonstrated that neonatal manipulation of oxytocin (ot) has effects on the expression of estrogen receptor alpha (er alpha) and the central production of oxytocin observed in juveniles (at weaning, 21 days of age). the goal of this study was to determine whether the effects of neonatal manipulation of ot last into adulthood, and if the effects differ from those observed during the early postnatal period. on the first day of life, prairie voles (microtus ochrogaster) receiv ...200717825097
social isolation disrupts autonomic regulation of the heart and influences negative affective behaviors.there is a documented association between affective disorders (e.g., depression and anxiety) and cardiovascular disease in humans. chronic social stressors may play a mechanistic role in the development of behavioral and cardiac dysregulation. the current study investigated behavioral, cardiac, and autonomic responses to a chronic social stressor in prairie voles, a rodent species that displays social behaviors similar to humans.200717658486
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