RESUMEN
Mammalian infants depend on parental care for survival, with numerous consequences for their behavioral development. We investigated the epigenetic and neurodevelopmental mechanisms mediating the impact of early biparental care on development of alloparenting behavior, or caring for offspring that are not one's own. We find that receiving high parental care early in life leads to slower epigenetic aging of both sexes and widespread male-specific differential expression of genes related to synaptic transmission and autism in the nucleus accumbens. Examination of parental care composition indicates that high-care fathers promote a male-specific increase in excitatory synapses and increases in pup retrieval behavior as juveniles. Interestingly, females raised by high-care fathers have the opposite behavioral response and display fewer pup retrievals. These results support the concept that neurodevelopmental trajectories are programmed by different features of early-life parental care and reveal that male neurodevelopmental processes are uniquely sensitive to care by fathers.
Asunto(s)
Conducta Animal , Padre , Humanos , Femenino , Animales , Masculino , Conducta Animal/fisiología , Conducta Materna/fisiología , Núcleo Accumbens , Padres , Conducta Paterna , Arvicolinae/fisiologíaRESUMEN
Cesarean delivery is associated with diminished plasma levels of several 'birth-signaling' hormones, such as oxytocin and vasopressin. These same hormones have been previously shown to exert organizational effects when acting in early life. For example, our previous work found a broadly gregarious phenotype in prairie voles exposed to oxytocin at birth. Meanwhile, cesarean delivery has been previously associated with changes in social behavior and metabolic processes related to oxytocin and vasopressin. In the present study, we investigated the long-term neurodevelopmental consequences of cesarean delivery in prairie voles. After cross-fostering, vole pups delivered either via cesarean or vaginal delivery were studied throughout development. Cesarean-delivered pups responded to isolation differently in terms of their vocalizations (albeit in opposite directions in the two experiments), huddled in less cohesive groups under warmed conditions, and shed less heat. As young adults, we observed no differences in anxiety-like or alloparental behavior. However, in adulthood, cesarean-delivered voles of both sexes failed to form partner preferences with opposite sex conspecifics. In a follow-up study, we replicated this deficit in partner-preference formation among cesarean-delivered voles and were able to normalize pair-bonding behavior by treating cesarean-delivered vole pups with oxytocin (0.25 mg/kg) at delivery. Finally, we detected minor differences in regional oxytocin receptor expression within the brains of cesarean-delivered voles, as well as microbial composition of the gut. Gene expression changes in the gut epithelium indicated that cesarean-delivered male voles have altered gut development. These results speak to the possibility of unintended developmental consequences of cesarean delivery, which currently accounts for 32.9 % of deliveries in the U.S. and suggest that further research should be directed at whether hormone replacement at delivery influences behavioral outcomes in later life.
Asunto(s)
Pradera , Oxitocina , Animales , Femenino , Masculino , Oxitocina/metabolismo , Estudios de Seguimiento , Apareamiento , Vasopresinas/metabolismo , Conducta Social , Receptores de Oxitocina/genética , Receptores de Oxitocina/metabolismo , Arvicolinae/fisiologíaRESUMEN
The social behavior network (SBN) has provided a framework for understanding the neural control of social behavior. The original SBN hypothesis proposed this network modulates social behavior and should exhibit distinct patterns of neural activity across nodes, which correspond to distinct social contexts. Despite its tremendous impact on the field of social neuroscience, no study has directly tested this hypothesis. Thus, we assessed Fos responses across the SBN of male prairie voles (Microtus ochrogaster). Virgin/non-bonded and pair bonded subjects were exposed to a sibling cagemate or pair bonded partner, novel female, novel male, novel meadow vole, novel object, or no stimulus. Inconsistent with the original SBN hypothesis, we did not find profoundly different patterns of neural responses across the SBN for different contexts, but instead found that the SBN generated significantly different patterns of activity in response to social novelty in pair bonded, but not non-bonded males. These findings suggest that non-bonded male prairie voles may perceive social novelty differently from pair bonded males or that SBN functionality undergoes substantial changes after pair bonding. This study reveals novel information about bond-dependent, context-specific neural responsivity in male prairie voles and suggests that the SBN may be particularly important for processing social salience. Further, our study suggests there is a need to reconceptualize the framework of how the SBN modulates social behavior.
Asunto(s)
Pradera , Conducta Social , Masculino , Femenino , Humanos , Animales , Arvicolinae/fisiología , ApareamientoRESUMEN
Monogamous pair bonding has evolved to enhance reproductive success and ensure offspring survival. Although the behavioral and neural mechanisms regulating the formation of pair bonds have been relatively well outlined, how these relationships are regulated and maintained across the lifetime of an individual remains relatively unexplored. One way to explore this is to study the maintenance of a social bond across a major life-history transition. The transition to motherhood is among the most poignant moments in the life history of a female, and is associated with significant neural and behavioral changes and shifting priorities. The nucleus accumbens (NAc) is known to modulate social valence and is central to mammalian pair bonding. In this study, we investigated two mechanisms driving variation in bond strength in the socially monogamous prairie vole (Microtus ochrogaster). We manipulated neural activity of the NAc at two distinct stages of life-history, before and after the birth of offspring, to assess how neural activity and social contexts modulate female pair bond strength. Our results showed DREADD (Designer Receptor Exclusively Activated by Designer Drugs) inhibition of the NAc decreases affiliative behavior towards the mating partner, whereas DREADD activation of the NAc increases affiliative behavior of strangers, thereby decreasing social selectivity. We also found a robust "birth effect" on pair bond strength, such that bonds with partners were weakened after the birth of offspring, an effect not attributable to the amount of cohabitation time with a partner. Overall, our data support the hypotheses that NAc activity modulates reward/saliency within the social brain in different ways, and that motherhood comes with a cost for the bond strength between mating partners.
Asunto(s)
Núcleo Accumbens , Apareamiento , Animales , Femenino , Pradera , Conducta Social , Arvicolinae/fisiología , Proteínas de Unión al ADN/farmacologíaRESUMEN
Pair-bond formation depends vitally on neuromodulatory signaling within the nucleus accumbens, but the neuronal dynamics underlying this behavior remain unclear. Using 1-photon in vivo Ca2+ imaging in monogamous prairie voles, we found that pair bonding does not elicit differences in overall nucleus accumbens Ca2+ activity. Instead, we identified distinct ensembles of neurons in this region that are recruited during approach to either a partner or a novel vole. The partner-approach neuronal ensemble increased in size following bond formation, and differences in the size of approach ensembles for partner and novel voles predict bond strength. In contrast, neurons comprising departure ensembles do not change over time and are not correlated with bond strength, indicating that ensemble plasticity is specific to partner approach. Furthermore, the neurons comprising partner and novel-approach ensembles are nonoverlapping while departure ensembles are more overlapping than chance, which may reflect another key feature of approach ensembles. We posit that the features of the partner-approach ensemble and its expansion upon bond formation potentially make it a key neuronal substrate associated with bond formation and maturation.
Asunto(s)
Neuronas/fisiología , Núcleo Accumbens/fisiología , Apareamiento , Conducta Sexual Animal/fisiología , Animales , Arvicolinae/fisiología , Femenino , Masculino , Preferencia en el Apareamiento Animal/fisiología , Núcleo Accumbens/diagnóstico por imagen , Conducta SocialRESUMEN
Repeated formation and subsequent dissolution of romantic relationships is common in humans across a lifetime. The socially monogamous prairie vole (Microtus ochrogaster) is used to study mechanisms of these bonds. At least in the laboratory, male prairie voles form bonds with a new female partner after loss of a previous partner. Initial bond formation depends on activation of dopamine D2-like receptors in the nucleus accumbens. Blocking activity of this receptor subtype disrupts formation of an animal's first pair bond. It is not known if these same D2-like receptors facilitate pair bonding with a subsequent partner after previous partner loss. This study examined the effects of D2-like receptor blockade on repeated pair bonding in male prairie voles. Males were paired with an initial female and allowed to mate before being separated. After a 5-day separation, males were then treated with either saline or eticlopride, a selective D2-receptor antagonist, prior to being paired with a second female and being allowed to mate. After a second separation, males were tested to determine if they developed a preference for spending time with their first or second mate. Eticlopride-treated males spent more time in a cage containing one of their previous partners compared to time in an empty cage but did not form a selective preference for either partner. Saline-treated males preferred their second, more recent partner. D2 receptor antagonism, then, disrupts bond formation in a second pairing but does not help to maintain a bond with the initial partner.
Asunto(s)
Pradera , Apareamiento , Animales , Arvicolinae/fisiología , Proteínas de Unión al ADN/farmacología , Femenino , Masculino , Conducta Sexual Animal/fisiología , Conducta SocialRESUMEN
Formation of long-term pair-bonds is a complex process, involving multiple neural circuits and is context- and experience-dependent. While laboratory studies using prairie voles have identified the involvement of several neural mechanisms, efforts to translate these findings into predictable field outcomes have been inconsistent at best. Here we test the hypothesis that inhibition of oestrogen receptor alpha (ERα) in the medial amygdala of male prairie voles would significantly increase the expression of social monogamy in the field. Prairie vole populations of equal sex ratio were established in outdoor enclosures with males bred for high levels of ERα expression and low levels of prosocial behaviour associated with social monogamy. Medial amygdala ERα expression was knocked down in half the males per population. Knockdown males displayed a greater degree of social monogamy in five of the eight behavioural indices assessed. This study demonstrates the robust nature of ERα in playing a critical role in the expression of male social monogamy in a field setting.
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Receptor alfa de Estrógeno , Conducta Social , Amígdala del Cerebelo/metabolismo , Animales , Arvicolinae/genética , Arvicolinae/metabolismo , Receptor alfa de Estrógeno/genética , Receptor alfa de Estrógeno/metabolismo , Pradera , MasculinoRESUMEN
Social support from a spouse, long-term partner, or someone who provides emotional or instrumental support may protect against consequences of aging, including mediating behavioral stress reactivity and altering neurobiological process that underlie short-term stress responses. Therefore, long-term social bonding may have behavioral and neurobiological benefits. The socially monogamous prairie vole provides a valuable experimental model for investigating the benefits of long-term social bonds on short-term stress reactivity in aging animals, given their unique social structure of forming enduring opposite-sex bonds, living in family groups, and bi-parental rearing strategies. Male-female pairs of long-term, cohabitating prairie voles were investigated for short-term behavioral and neuroendocrine stress reactivity following either long-term social pairing (control), or a period of social isolation. In Experiment 1, social isolation was associated with altered behavioral reactivity to an acute swim stressor, and greater neural activation in the hypothalamic paraventricular nucleus, as well as specifically the parvocellular region, following the swim stressor (vs. control). In Experiment 2, social isolation was associated with greater corticosterone reactivity following an acute restraint stressor (vs. control). No sex differences were observed. Exploratory correlation and subgroup analyses revealed systematic relationships among various demographic variables (such as age of the subjects, amount of time the pair cohabitated together, and number of litters the pair reared together) and the behavioral and neuroendocrine outcome measures. These findings may inform our understanding of the benefits of long-term social bonding on modulating short-term behavioral and neuroendocrine responses to stress.LAY SUMMARYReceiving social support from a long-term spouse or partner, or having a strong support network from friends, may have important health benefits as people age. In aging monogamous prairie voles, social isolation from a long-term social partner disrupted behaviors and short-term stress responses, whereas living with a long-term partner protected against these disruptions. This research is important for our understanding of the benefits of social support on stress responses as we age.
Asunto(s)
Pradera , Estrés Psicológico , Envejecimiento , Animales , Arvicolinae , Femenino , Masculino , Sistemas Neurosecretores , Conducta Social , Aislamiento SocialRESUMEN
Dopamine signaling mediates the formation of some types of social relationships, including reproductive pair bonds in the socially monogamous prairie vole (Microtus ochrogaster). In addition to these pair bonds with mates, prairie voles demonstrate selective preferences for familiar same-sex peers. The dependence of peer relationships on dopamine signaling has not been tested, and the mechanisms supporting these relationships may differ from those underlying pair bonds. We examined the effects of pharmacological manipulations of dopamine signaling on peer partner preference and socially conditioned place preference in female prairie voles. Haloperidol blockade of dopamine receptors at multiple doses did not alter selective preferences for familiar same-sex partners, suggesting that dopamine neurotransmission is not necessary for the formation of prairie vole peer relationships, unlike mate relationships. Dopamine receptor agonist apomorphine facilitated peer partner preferences under conditions normally insufficient for partner preference formation; however, in the absence of effects from blockade, it is difficult to distinguish between a role for dopamine in partner preference formation and the generally rewarding properties of a dopamine agonist. Prairie voles exhibited socially conditioned place preferences for new but not long-term same-sex peers, and these preferences were not blocked by haloperidol. These results suggest that prairie vole peer relationships are less dependent on dopamine signaling than pair bonds, while still being rewarding. The data support distinct roles of dopamine and motivation in prairie vole peer relationships relative to mate relationships, suggesting that reproductive bonds are mediated differently from non-reproductive ones.
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Arvicolinae/fisiología , Dopamina/metabolismo , Conducta Social , Animales , Dopamina/fisiología , Agonistas de Dopamina/farmacología , Femenino , Masculino , Motivación/efectos de los fármacos , Apareamiento , Grupo Paritario , Receptores Dopaminérgicos/metabolismo , Receptores Dopaminérgicos/fisiología , Recompensa , Conducta Sexual Animal/efectos de los fármacos , Transducción de Señal/efectos de los fármacos , Transducción de Señal/fisiologíaRESUMEN
Uncontrollable stress precipitates negative mental and physical health outcomes. Furthermore, the vicarious experience of stress (e.g. observing another individual experience a direct stressor) can mimic the effects of directly experiencing the stressor. The current experiment examined the behavioral and physiological effects of the vicarious experience of stress using the socially monogamous prairie vole. Male prairie voles were exposed to either an empty open field chamber, or a chamber in which the animal observed a sibling undergoing a concurrent direct physical stressor (tail suspension test) for five minutes. Exploratory and anxiety-like behaviors were recorded in all observers during the test session. Cardiac indices of heart rate and heart rate variability were recorded in a subset of observers prior to, during, and following the test session. Corticosterone levels were measured in all observers and siblings following the test session. When compared to animals exposed to an empty open field chamber, animals that observed a sibling undergo a direct physical stressor exhibited increased heart rate and circulating corticosterone, and decreased heart rate variability. These physiological stress indicators were supported by behavioral changes, including increased freezing followed immediately by orienting of the head toward the center of the apparatus, and decreased locomotion, grooming, and rearing. These preliminary results suggest that prairie voles experience stress vicariously, and provide a foundation for additional studies focused on the underlying mechanisms of vicarious stress. The use of this model may inform our understanding of the social transmission of stress among social species, including humans.LAY SUMMARYThe experience of stress, including observing stress in a loved one, has negative consequences on mental and physical health. This study used a social rodent (prairie voles) to demonstrate that stress transfers among social individuals, consequently producing an increased physiological and behavioral stress response in prairie voles observing their siblings experience stress. This research informs our understanding of the interactions of social experiences and stress in humans.
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Hermanos , Aislamiento Social , Animales , Arvicolinae , Pradera , Humanos , Masculino , Estrés PsicológicoRESUMEN
Monogamous prairie voles (Microtus ochrogaster) form mating-based pair bonds. Although wild prairie voles rarely re-pair following loss of a partner, laboratory studies have shown that previous pairing and mating does not negate the ability to form a new partner preference. However, little is known about how prior bond experience may alter the trajectory and display of a new pair bond. In the present study, we disrupted an initial pair bond by separating partners and then varied the amount of time before a new partner was introduced. We assessed how separation time affected the stability of partner preference over time and influenced decision-making in male voles performing a head-to-head partner preference test in which they chose between the first and second partner. We found that the ability to consistently display a preference for the second partner, supplanting the initial pair bond, depended on how long the test animal was separated from their first partner. Prior bonding experience also shaped the subsequent effects of mating on partner preference. Partner preference strength was sensitive to latency to mate with the second partner but not the first partner, irrespective of separation time. These results suggest that the ability to form a consistent, strong preference for a new partner after an initial pair bond depends upon the amount of time that has passed since separation from the first partner. These results provide valuable insight into how social bonds are dynamically shaped by prior social experience and identify variables that contribute to recovery from partner loss and the ability to form a new pair bond. They also delineate a behavioral trajectory essential for future work examining the hormonal and genetic changes that enable recovery from partner loss.
Asunto(s)
Arvicolinae/fisiología , Apareamiento , Conducta Sexual Animal/fisiología , Animales , Conducta de Elección/fisiología , Femenino , Masculino , Conducta Social , Factores de TiempoRESUMEN
Behavioral neuroendocrinology has a rich history of using diverse model organisms to elucidate general principles and evolution of hormone-brain-behavior relationships. The oxytocin and vasopressin systems have been studied in many species, revealing their role in regulating social behaviors. Oxytocin and vasopressin receptors show remarkable species and individual differences in distribution in the brain that have been linked to diversity in social behaviors. New technologies allow for unprecedented interrogation of the genes and neural circuitry regulating behaviors, but these approaches often require transgenic models and are most often used in mice. Here we discuss seminal findings relating the oxytocin and vasopressin systems to social behavior with a focus on non-traditional animal models. We then evaluate the potential of using CRISPR/Cas9 genome editing to examine the roles of genes and enable circuit dissection, manipulation and activity monitoring of the oxytocin and vasopressin systems. We believe that it is essential to incorporate these genetic and circuit level techniques in comparative behavioral neuroendocrinology research to ensure that our field remains innovative and attractive for the next generation of investigators and funding agencies.
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Edición Génica , Oxitocina/fisiología , Conducta Social , Vasopresinas/fisiología , Animales , Animales Modificados Genéticamente , Ciencias Bioconductuales/historia , Ciencias Bioconductuales/tendencias , Encéfalo/metabolismo , Sistemas CRISPR-Cas/genética , Edición Génica/historia , Edición Génica/tendencias , Historia del Siglo XXI , Ratones , Receptores de Oxitocina/genética , Receptores de Vasopresinas/genéticaRESUMEN
Available pharmacotherapies to treat alcohol use disorder (AUD) show limited efficacy. Preclinical studies in mice and rats suggested that antagonists of the corticotropin releasing factor receptor 1 (CRFR1) could be more efficacious for such treatment. However, clinical trials with CRFR1 antagonists were not successful. While a number of potential explanations for this translational failure have been suggested, we hypothesized that the lack of success in clinical trials could be in part due to different neuroanatomical organization of the CRFR1 system in mice and rats versus humans. The CRF system in prairie voles (Microtus ochrogaster), a socially monogamous rodent species, also shows differences in organization from mice and rats. To test our hypothesis, we compared the efficacy of a potent CRFR1 antagonist, CP-376,395, to modulate alcohol drinking in male and female prairie voles versus male and female C57BL/6J mice using an almost identical 2-bottle choice drinking procedure. CP-376,375 (10 and 20 mg/kg, i.p.) significantly decreased alcohol intake (but not alcohol preference) in mice, but not prairie voles. Furthermore, administration of this antagonist (20 mg/kg, i.p.) prior to the partner preference test (PPT) decreased partner preference (PP) in male prairie voles. These findings support our hypothesis that the greater efficacy of CRFR1 antagonists to suppress alcohol consumption in mice and rats versus other mammalian species could be due to the differences in organization of the CRFR1 system between species. They further indicate that activity of the CRFR1 system is necessary for the formation of pair-bonds, but not consumption of high doses of alcohol. Overall, we suggest that testing potential pharmacotherapies should not rely only on studies in mice and rats.
Asunto(s)
Consumo de Bebidas Alcohólicas/fisiopatología , Aminopiridinas/farmacología , Etanol/farmacología , Apareamiento , Receptores de Hormona Liberadora de Corticotropina/antagonistas & inhibidores , Animales , Arvicolinae , Conducta de Elección/efectos de los fármacos , Resistencia a Medicamentos/efectos de los fármacos , Femenino , Humanos , Masculino , Preferencia en el Apareamiento Animal/efectos de los fármacos , Ratones , Ratones Endogámicos C57BL , Ratas , Sensibilidad y EspecificidadRESUMEN
Physical exercise and chronic social stress are both known to impact general health and hypothalamic-pituitary-adrenal (HPA) axis function, albeit typically in opposing directions. Therefore, the question we investigated in this study was how these two factors - physical exercise and chronic social isolation - would interact when presented simultaneously in a female rodent model. Adult female prairie voles were separated into four experimental groups: (1) isolated without wheel access, (2) isolated with wheel access, (3) paired without wheel access, and (4) paired with wheel access. Plasma, hair, and adrenal glands were sampled to investigate changes in stress physiology. Our results indicate that, when isolated, wheel access had a mitigating effect on HPA activity. However, in paired animals, wheel access had the opposite effect, as both adrenal mass and increase in hair corticosterone concentrations were greater in paired animals with wheel access. Strong correlations were detected between change in hair corticosterone and adrenal mass, while no correlations were found between plasma corticosterone and either of the other markers. These results imply that the HPA axis is highly sensitive to both the social environment and the physical demands placed on the individual, and that when investigating the effects of chronic isolation, both hair corticosterone and adrenal mass may be more reliable markers than a single plasma corticosterone sample.
Asunto(s)
Sistema Hipotálamo-Hipofisario/fisiología , Condicionamiento Físico Animal/fisiología , Sistema Hipófiso-Suprarrenal/fisiología , Medio Social , Aislamiento Social , Estrés Fisiológico/fisiología , Estrés Psicológico/fisiopatología , Animales , Arvicolinae , Corticosterona/análisis , Femenino , MasculinoRESUMEN
Previous research indicates that loneliness and social isolation may contribute to behavioral disorders and neurobiological dysfunction. Environmental enrichment (EE), including both cognitive and physical stimulation, may prevent some behavioral, endocrine, and cardiovascular consequences of social isolation; however, specific neural mechanisms for these benefits are still unclear. Therefore, this study examined potential neuroendocrine protective effects of both EE and exercise. Adult female prairie voles were randomly assigned to one of four experimental conditions: paired control, social isolation/sedentary, social isolation/EE, and social isolation/voluntary exercise. All isolated animals were housed individually for 8 weeks, while paired animals were housed with their respective sibling for 8 weeks. Animals in the EE and voluntary exercise conditions received EE items (including a running wheel) and a running wheel only, respectively, at week 4 of the isolation period. At the end of the experiment, plasma and brains were collected from all animals for corticosterone and FosB and delta FosB (FosB/ΔFosB) - immunoreactivity in stress-related brain regions. Overall, social isolation increased neuroendocrine stress responses, as reflected by the elevation of corticosterone levels and increased FosB/ΔFosB-immunoreactivity in the basolateral amygdala (BLA) compared to paired animals; EE and voluntary exercise attenuated these increases. EE and exercise also increased FosB/ΔFosB-immunoreactivity in the medial prefrontal cortex (mPFC) compared to other conditions. Limbic structures statistically mediated hypothalamic immunoreactivity in EE and exercise animals. This research has translational value for socially isolated individuals by informing our understanding of neural mechanisms underlying responses to social stressors. Highlights Prolonged social isolation increased basal corticosterone levels and basolateral amygdala immunoreactivity. Environmental enrichment and exercise buffered corticosterone elevations and basolateral amygdala hyperactivity. Protective effects of environmental enrichment and exercise may be mediated by medial prefrontal cortex and limbic structures.
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Sistema Límbico/metabolismo , Sistemas Neurosecretores/metabolismo , Condicionamiento Físico Animal/fisiología , Aislamiento Social , Estrés Psicológico/metabolismo , Animales , Arvicolinae , Corticosterona/sangre , Corticosterona/metabolismo , Ambiente , Femenino , Masculino , Proteínas Proto-Oncogénicas c-fos/metabolismo , Estrés Psicológico/terapiaRESUMEN
The prairie vole has proven a valuable animal model for the neurobiological study of social monogamy and pair bonding. Previous research has focused almost exclusively on virgin prairie voles forming pair-bonds for the first time - a paradigm with limited relevance to human social behavior. In the present study, we used stud males to assess the impact of repeated pair-bond formation and dissolution on the behaviors and neurobiology relevant to subsequent pair-bond formation. Stud males were tested for behavioral and neurobiological effects of repeated pair-bonding after the 1st, 5th, and 10th pairing. Aged breeder males that experienced minimal pair-bond dissolution were included to control for the effects of aging. Results showed that male prairie voles readily form new pair-bonds after repeated pair-bond dissolution. In terms of social monogamy, old age was associated with males spending less time in close social contact with unfamiliar females. There were no effects of age nor number of lifetime pairings on depressive-like behavior or paternal behavior toward pups. Within the brain, the patterns of oxytocin (OTR) and vasopressin type 1a (V1aR) receptors were largely unaffected, with the following exceptions: 1) males with only a single pairing had higher OTR densities in the paraventricular thalamus and bed nucleus of the stria terminalis; 2) there was an age-related increase in the density of OTR in the caudate putamen and an age-related decline in the density of V1aR in the cortical amygdala. The present findings have translational relevance to human social behavior in the context of aging and social experience.
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Envejecimiento/fisiología , Arvicolinae/fisiología , Apareamiento , Maduración Sexual/fisiología , Factores de Edad , Animales , Arvicolinae/metabolismo , Encéfalo/metabolismo , Femenino , Masculino , Oxitocina/metabolismo , Conducta Paterna/fisiología , Receptores de Oxitocina/metabolismo , Receptores de Vasopresinas/metabolismo , Conducta Social , Vasopresinas/metabolismoRESUMEN
Why do members of some species live in groups while others are solitary? Group living (sociality) has often been studied from an evolutionary perspective, but less is known about the neurobiology of affiliation outside the realms of mating and parenting. Colonial species offer a valuable opportunity to study nonsexual affiliative behavior between adult peers. Meadow voles (Microtus pennsylvanicus) display environmentally induced variation in social behavior, maintaining exclusive territories in summer months, but living in social groups in winter. Research on peer relationships in female meadow voles demonstrates that these selective preferences are mediated differently than mate relationships in socially monogamous prairie voles, but are also impacted by oxytocin and HPA axis signaling. This review addresses day-length dependent variation in physiology and behavior, and presents the current understanding of the mechanisms supporting selective social relationships in meadow voles, with connections to lessons from other species.
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Arvicolinae/fisiología , Procesos de Grupo , Sistemas Neurosecretores/fisiología , Conducta Social , Animales , Distinciones y Premios , Conducta Animal/fisiología , Femenino , Sistema Hipotálamo-Hipofisario/fisiología , Masculino , Neuroendocrinología , Oxitocina/farmacología , Grupo Paritario , Sistema Hipófiso-Suprarrenal/fisiologíaRESUMEN
This is a contribution to SI: SBN/ICN meeting. In social species, relationships may form between mates, parents and their offspring, and/or social peers. Prairie voles and meadow voles both form selective relationships for familiar same-sex peers, but differ in mating system, allowing comparison of the properties of peer and mate relationships. Prairie vole mate bonds are dopamine-dependent, unlike meadow vole peer relationships, indicating potential differences in the mechanisms and motivation supporting these relationships within and/or across species. We review the role of dopamine signaling in affiliative behavior, and assess the role of behavioral reward across relationship types. We compared the reinforcing properties of mate versus peer relationships within a species (prairie voles), and peer relationships across species (meadow and prairie voles). Social reinforcement was assessed using the socially conditioned place preference test. Animals were conditioned using randomly assigned, equally preferred beddings associated with social (CS+) and solitary (CS-) housing. Prairie vole mates, but not prairie or meadow vole peers, conditioned toward the social cue. A second study in peers used counter-conditioning to enhance the capacity to detect low-level conditioning. Time spent on CS+ bedding significantly decreased in meadow voles, and showed a non-significant increase in prairie voles. These data support the conclusion that mate relationships are rewarding for prairie voles. Despite selectivity of preferences for familiar individuals in partner preference tests, peer relationships in both species appear only weakly reinforcing or non-reinforcing. This suggests important differences in the pathways underlying these relationship types, even within species.
Asunto(s)
Arvicolinae/fisiología , Recompensa , Conducta Sexual Animal/fisiología , Conducta Social , Comunicación Animal , Animales , Femenino , Masculino , Motivación , Grupo Paritario , Factores SexualesRESUMEN
Although prairie vole (Microtus ochrogaster) social behavior is well-characterized in adults, surprisingly little is known about the development of social behavior in voles. Further, the overwhelming majority of studies in prairie voles examine social behavior in a reproductive context. Here, we examine developmental plasticity in affiliation and aggression and their underlying neural correlates. Using sexually naïve males, we characterized interactions with an age-matched, novel, same-sex conspecific in four different age groups that span pre-weaning to adulthood. We found that prosocial behavior decreased and aggression increased as males matured. Additionally, pre-weaning males were more prosocial than nonsocial, whereas post-weaning males were more nonsocial than prosocial. We also examined nonapeptide neural activity in response to a novel conspecific in brain regions important for promoting sociality and aggression using the immediate early gene cFos. Assessment of developmental changes in neural activity showed that vasopressin neurons in the medial bed nucleus of the stria terminalis exhibit functional plasticity, providing a potential functional mechanism that contributes to this change in sociality as prairie voles mature. This behavioral shift corresponds to the transition from a period of allopatric cohabitation with siblings to a period of time when voles disperse and presumably attempt to establish and defend territories. Taken together our data provide a putative mechanism by which brain and behavior prepare for the opportunity to pairbond (characterized by selective affiliation with a partner and aggression toward unfamiliar conspecifics) by undergoing changes away from general affiliation and toward selective aggression, accounting for this important life history event.
Asunto(s)
Adaptación Fisiológica/fisiología , Agresión/fisiología , Arvicolinae/fisiología , Neuronas/fisiología , Maduración Sexual/fisiología , Conducta Social , Vasopresinas/metabolismo , Agresión/psicología , Animales , Encéfalo/metabolismo , Química Encefálica , Femenino , Masculino , Neuronas/metabolismo , Caracteres Sexuales , Conducta Sexual Animal/fisiologíaRESUMEN
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 group) or individually (isolated group). Active and passive behavioral responses to the forced swim test (FST) and tail-suspension test (TST), and plasma concentrations of adrenocorticotropic hormone (ACTH) and corticosterone, were measured in all prairie voles following the CMS period. Both female and male prairie voles housed with a social partner displayed lower durations of passive behavioral responses (immobility, a maladaptive behavioral response) in the FST (mean ± SEM; females: 17.3 ± 5.4 s; males: 9.3 ± 4.6 s) and TST (females: 56.8 ± 16.4 s; males: 40.2 ± 11.3 s), versus both sexes housed individually (females, FST: 98.6 ± 12.9 s; females, TST: 155.1 ± 19.3 s; males, FST: 92.4 ± 14.1 s; males, TST: 158.9 ± 22.0 s). Female (but not male) prairie voles displayed attenuated plasma stress hormones when housed with a male partner (ACTH: 945 ± 24.7 pg/ml; corticosterone: 624 ± 139.5 ng/ml), versus females housed individually (ACTH: 1100 ± 23.2 pg/ml; corticosterone: 1064 ± 121.7 ng/ml). These results may inform understanding of the benefits of social interactions on stress resilience. Lay Summary: Social stress can lead to depression. The study of social bonding and stress using an animal model will inform understanding of the protective effects of social bonds. This study showed that social bonding in a rodent model can protect against behavioral responses to stress, and may also be protective against the elevation of stress hormones. This study provides evidence that bonding and social support are valuable for protecting against stress in humans.