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Neuropeptide Regulation of Social Attachment: The Prairie Vole Model

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ABSTRACT

Social attachments are ubiquitous among humans and integral to human health. Although great efforts have been made to elucidate the neural underpinnings regulating social attachments, we still know relatively little about the neuronal and neurochemical regulation of social attachments. As a laboratory animal research model, the socially monogamous prairie vole (Microtus ochrogaster) displays behaviors paralleling human social attachments and thus has provided unique insights into the neural regulation of social behaviors. Research in prairie voles has particularly highlighted the significance of neuropeptidergic regulation of social behaviors, especially of the roles of oxytocin (OT) and vasopressin (AVP). This article aims to review these findings. We begin by discussing the role of the OT and AVP systems in regulating social behaviors relevant to social attachments, and thereafter restrict our discussion to studies in prairie voles. Specifically, we discuss the role of OT and AVP in adult mate attachments, biparental care, social isolation, and social buffering as informed by studies utilizing the prairie vole model. Not only do these studies offer insight into social attachments in humans, but they also point to dysregulated mechanisms in several mental disorders. We conclude by discussing these implications for human health. © 2017 American Physiological Society. Compr Physiol 7:81‐104, 2017.

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Figure 1. Figure 1. Schematic drawings of sagittal brain sections illustrating OT (right) and AVP (left) neurons and their projections to selected brain regions important in social behaviors. Colored brain regions also indicate the distribution and regional density of OT receptors (red) and AVP receptors (blue) in the brain. OT and AVP are released from the pituitary gland into the blood circulation to regulate peripheral functions such as the milk letdown reflex and uterine contractions in females as well as vasoconstriction and water retention in both males and females. In addition, OT and AVP are released throughout the brain to regulate a variety of complex social behaviors including social recognition, mating, bonding, parenting, and social buffering. AH, anterior hypothalamus; BNST, bed nucleus of the stria terminalis; HP, hippocampus; LS, lateral septum; MeA medial amygdala. MPOA, medial preoptic area of the hypothalamus; NAcc, nucleus accumbens; OB, olfactory bulb; PFC, prefrontal cortex; Pit, pituitary gland; SON, supraoptic nucleus; VMH, ventromedial hypothalamus; VP, ventral pallidum; VTA, ventral tegmental area.
Figure 2. Figure 2. Socially monogamous prairie voles display several types of social behaviors that have been studied in laboratory conditions. (A) Photograph of a pair of male and female prairie voles with their pups in the nest. (B) Pair bonding behavior is measured using a 3‐h partner preference test. The testing apparatus consists of three chambers connected by hollow tubes. At the beginning of the test, the subject is placed in the center cage and allowed to freely explore the other two cages containing either the partner or a conspecific stranger. (C) In both male and female prairie voles, 24‐h cohabitation with mating reliably induces an increase in side‐by‐side contact with the partner versus a stranger, and this partner preference is not observed following 6‐h cohabitation. (D) Selective aggression is another indicator of pair bonding. While sexually naïve males are not aggressive, pair‐bonded males display aggression selectively toward stranger males and females, but not toward their partners. (E) Upon litter birth, both male and female prairie voles share the natal nest and engage in parental care. Data are shown as mean ± SEM. *P < 0.05. Alphabetic letters indicate the results from a post‐hoc test following an ANOVA. Bars labeled with different letters differ significantly from each other. Data adapted, with permission, from ().
Figure 3. Figure 3. Autoradiograms showing the distribution of the OTR and vasopressin 1a receptor (V1aR) in the brain of the monogamous prairie voles and nonmonogamous montane voles. The densities of OTR binding in the nucleus accumbens (NAcc) and medial prefrontal cortex (mPFC) are higher in the prairie vole (A) than in the montane vole (B). Additionally, the density of V1aR binding is higher in the BNST and lower in the lateral septum (LS) in the prairie vole (C) compared to the montane vole (D). Data adapted, with permission, from ().
Figure 4. Figure 4. The effects of OT and AVP on partner preference behavior in prairie voles. (A) Control females that receive ICV injections of CSF do not display partner preferences after 6 h of cohabitation with a male, whereas females receiving OT injections into the ventricle (OT ICV), nucleus accumbens (OT NAcc), or viral vector injections (AAV‐OTR) for OTR over expression in the NAcc, do display partner preferences. (B) 24 h of mating and cohabitation with a male reliably induces partner preferences in control females (CSF), but this behavior is prevented by ICV or intra‐NAcc injections of an OTR antagonist (OTRA) or downregulation of OXTR by injections of interfering short hairpin RNA (OTR‐shRNA). (C) In male prairie voles, brief cohabitation does not induce partner preferences. However, AVP injections into the ventricle (ICV) and lateral septum (LS) as well as upregulation of the V1aR in the ventral pallidum (VP) via viral vector mediated gene transfer (AAV‐V1aR) facilitate partner preference formation. (D) 24‐h mating and cohabitation with a female induces partner preference in male prairie voles but this behavior is blocked by injections of the V1aR antagonist (V1aRA) into the ventricle (ICV), LS, or VP. Although OT and AVP effects are illustrated here by data from females and males, respectively, both neuropeptides have been shown to affect partner preference behavior in male and female prairie voles. Data are shown as mean ± SEM. *P < 0.05, **P < 0.01. Data adapted, with permission, from ().
Figure 5. Figure 5. The role of brain OT and AVP in the regulation of parental behaviors in prairie voles. (A) Oxytocin receptor (OTR) binding in the nucleus accumbens (NAcc) is higher in spontaneously maternal than in nonmaternal females. (B) Intra‐NAcc injections of an OTR antagonist (OTR‐NA) result in more female voles that do not display spontaneous maternal behavior compared to controls (CSF‐NA). (C) Downregulating OTR expression in the NAcc via injections of a short hairpin OTR interfering RNA (shRNA‐OTR) decreases the number of juvenile female voles displaying alloparental behavior, compared to control females (control) injected with a scrambled sequence. (D) Female voles receiving shRNA‐OTR injections into the NAcc spend less time licking and grooming pups, compared to control females. (E) Male prairie voles receiving ICV injections of AVP display a higher level of spontaneous paternal responsiveness to pups compared to males receiving control injections (Saline) or injections of AVP with an AVP receptor antagonist (antagonist/AVP). Data are shown as mean ± SEM. *P < 0.05. Data adapted, with permission, from ().
Figure 6. Figure 6. The effects of social isolation on behaviors, brain OT, and immune responses in sexually naive female prairie voles. Compared to the pair‐housed controls (paired), females that are socially isolated from cage mates for 4 weeks (isolated) spend less time in the open arms during an elevated plus maze test (EPM) (A) and more time immobile during a forced swim test (FST) (B). Isolation experience also decreases CH50, which measures the activity of the immune system's classical complement pathway (C). In addition, Isolated females show a decrease in OTR mRNA expression in the hypothalamus (D), an increase in the percentage of c‐Fos labeled OT‐immunoreactive neurons in the PVN following a 5‐min RIT (E), and an elevation in circulating OT levels (F), compared to the Paired controls. Such social isolation‐induced increases in heart rate (G) and immobile duration during the FST (H) as well as the decrease in sucrose intake (I) are prevented by daily OT administration. Data are shown as mean ± SEM. *P < 0.05. Alphabetic letters indicate the results from a post‐hoc test following an ANOVA. Bars labeled with different letters differ significantly from each other. Data adapted, with permission, from ().
Figure 7. Figure 7. The effects of partner separation on the physiology, behavior, and neurochemical staining in the brain of pair‐bonded prairie voles. Compared to the paired controls (paired), 5 days of separation from the mating partner (separated) resulted in increases in heat rate (A), immobile time during a forced swim test (FST) (B), and circulating levels of CORT following the FST (C) in both male and female prairie voles. In male prairie voles, 2 weeks of separation from their female partners led to a decreased entry to the open arms during an elevated plus maze test (EPM) (D) and an increased duration in the dark box during a light‐dark box test (E), in comparison to the Paired controls. Furthermore, these Separated males also showed an increase in social affiliation and a decrease in aggression during an RIT (F) as well as increases in the number of neurons stained for OT and AVP in the paraventricular nucleus of the hippocampus (PVN) (G, H, and I), compared to Paired controls. Data are shown as mean ± SEM. *P < 0.05. Scale bar = 100 μm. Data adapted, with permission, from ().
Figure 8. Figure 8. The effects of IMO stress and social buffering on anxiety‐like behaviors and brain OT activity in female prairie voles. Subjects experience 1‐h IMO stress, recover alone (alone) or with the male partner (partner) for 30 min, and receive a 5‐min EPM test. (A) Females that recover alone (alone) enter the open arms less frequently and spend less time there in the EPM test, compared to handled females (control) and females recovering with a partner (partner). (B) Data from in vivo brain microdialysis show that OT release in the PVN increases during IMO stress, and this increased OT release is sustained during the recovery if the subject recovers with a partner but not alone. (C and D) Intra‐PVN injections of an OTRA in the subjects recovering with the partner block social buffering effects on anxiety‐like behaviors and plasma CORT. Conversely, OT injections into the PVN of the subjects recovering alone mimic the effects of a partner by reducing anxiety like behaviors and circulating levels of CORT (D). Data are shown as mean ± SEM. *P < 0.05. Alphabetic letters indicate the results from a post‐hoc test following an ANOVA. Bars labeled with different letters differ significantly from each other. Data adapted, with permission, from ().
Figure 9. Figure 9. The effects of OT treatment in the PVN on stress induced changes in circulating CORT, anxiety‐like behaviors, and neural activity in female prairie voles. Intra‐PVN injections of OT before an EPS inhibit the stress‐induced rise in plasma CORT (A) and anxiety‐like behavior during the EPM (B). Although such OT injection does not alter the percentage of OT (C) or AVP (D) neurons in the PVN that are double‐labeled with c‐Fos, it decreases the number of CRH/Fos neurons (E) and increases the number of GABA/Fos (F) neurons in the PVN. Blue arrows point to double labeled cells. Furthermore, intra‐PVN injections of the GABAA receptor antagonist, bicuculline (Bic), prevent OT effects in reducing anxiety‐like behavior following the EPS stress (G). (H) A hypothetical model suggesting that OT release in the PVN may activate GABAergic interneurons in the PVN and GABAergic projecting neurons to the PVN, which, in turn, can inhibit CRH neurons and potentially decrease activity of the hypothalamic‐pituitary‐adrenal axis. Data are shown as mean ± SEM. *P < 0.05. Data adapted, with permission, from ().


Figure 1. Schematic drawings of sagittal brain sections illustrating OT (right) and AVP (left) neurons and their projections to selected brain regions important in social behaviors. Colored brain regions also indicate the distribution and regional density of OT receptors (red) and AVP receptors (blue) in the brain. OT and AVP are released from the pituitary gland into the blood circulation to regulate peripheral functions such as the milk letdown reflex and uterine contractions in females as well as vasoconstriction and water retention in both males and females. In addition, OT and AVP are released throughout the brain to regulate a variety of complex social behaviors including social recognition, mating, bonding, parenting, and social buffering. AH, anterior hypothalamus; BNST, bed nucleus of the stria terminalis; HP, hippocampus; LS, lateral septum; MeA medial amygdala. MPOA, medial preoptic area of the hypothalamus; NAcc, nucleus accumbens; OB, olfactory bulb; PFC, prefrontal cortex; Pit, pituitary gland; SON, supraoptic nucleus; VMH, ventromedial hypothalamus; VP, ventral pallidum; VTA, ventral tegmental area.


Figure 2. Socially monogamous prairie voles display several types of social behaviors that have been studied in laboratory conditions. (A) Photograph of a pair of male and female prairie voles with their pups in the nest. (B) Pair bonding behavior is measured using a 3‐h partner preference test. The testing apparatus consists of three chambers connected by hollow tubes. At the beginning of the test, the subject is placed in the center cage and allowed to freely explore the other two cages containing either the partner or a conspecific stranger. (C) In both male and female prairie voles, 24‐h cohabitation with mating reliably induces an increase in side‐by‐side contact with the partner versus a stranger, and this partner preference is not observed following 6‐h cohabitation. (D) Selective aggression is another indicator of pair bonding. While sexually naïve males are not aggressive, pair‐bonded males display aggression selectively toward stranger males and females, but not toward their partners. (E) Upon litter birth, both male and female prairie voles share the natal nest and engage in parental care. Data are shown as mean ± SEM. *P < 0.05. Alphabetic letters indicate the results from a post‐hoc test following an ANOVA. Bars labeled with different letters differ significantly from each other. Data adapted, with permission, from ().


Figure 3. Autoradiograms showing the distribution of the OTR and vasopressin 1a receptor (V1aR) in the brain of the monogamous prairie voles and nonmonogamous montane voles. The densities of OTR binding in the nucleus accumbens (NAcc) and medial prefrontal cortex (mPFC) are higher in the prairie vole (A) than in the montane vole (B). Additionally, the density of V1aR binding is higher in the BNST and lower in the lateral septum (LS) in the prairie vole (C) compared to the montane vole (D). Data adapted, with permission, from ().


Figure 4. The effects of OT and AVP on partner preference behavior in prairie voles. (A) Control females that receive ICV injections of CSF do not display partner preferences after 6 h of cohabitation with a male, whereas females receiving OT injections into the ventricle (OT ICV), nucleus accumbens (OT NAcc), or viral vector injections (AAV‐OTR) for OTR over expression in the NAcc, do display partner preferences. (B) 24 h of mating and cohabitation with a male reliably induces partner preferences in control females (CSF), but this behavior is prevented by ICV or intra‐NAcc injections of an OTR antagonist (OTRA) or downregulation of OXTR by injections of interfering short hairpin RNA (OTR‐shRNA). (C) In male prairie voles, brief cohabitation does not induce partner preferences. However, AVP injections into the ventricle (ICV) and lateral septum (LS) as well as upregulation of the V1aR in the ventral pallidum (VP) via viral vector mediated gene transfer (AAV‐V1aR) facilitate partner preference formation. (D) 24‐h mating and cohabitation with a female induces partner preference in male prairie voles but this behavior is blocked by injections of the V1aR antagonist (V1aRA) into the ventricle (ICV), LS, or VP. Although OT and AVP effects are illustrated here by data from females and males, respectively, both neuropeptides have been shown to affect partner preference behavior in male and female prairie voles. Data are shown as mean ± SEM. *P < 0.05, **P < 0.01. Data adapted, with permission, from ().


Figure 5. The role of brain OT and AVP in the regulation of parental behaviors in prairie voles. (A) Oxytocin receptor (OTR) binding in the nucleus accumbens (NAcc) is higher in spontaneously maternal than in nonmaternal females. (B) Intra‐NAcc injections of an OTR antagonist (OTR‐NA) result in more female voles that do not display spontaneous maternal behavior compared to controls (CSF‐NA). (C) Downregulating OTR expression in the NAcc via injections of a short hairpin OTR interfering RNA (shRNA‐OTR) decreases the number of juvenile female voles displaying alloparental behavior, compared to control females (control) injected with a scrambled sequence. (D) Female voles receiving shRNA‐OTR injections into the NAcc spend less time licking and grooming pups, compared to control females. (E) Male prairie voles receiving ICV injections of AVP display a higher level of spontaneous paternal responsiveness to pups compared to males receiving control injections (Saline) or injections of AVP with an AVP receptor antagonist (antagonist/AVP). Data are shown as mean ± SEM. *P < 0.05. Data adapted, with permission, from ().


Figure 6. The effects of social isolation on behaviors, brain OT, and immune responses in sexually naive female prairie voles. Compared to the pair‐housed controls (paired), females that are socially isolated from cage mates for 4 weeks (isolated) spend less time in the open arms during an elevated plus maze test (EPM) (A) and more time immobile during a forced swim test (FST) (B). Isolation experience also decreases CH50, which measures the activity of the immune system's classical complement pathway (C). In addition, Isolated females show a decrease in OTR mRNA expression in the hypothalamus (D), an increase in the percentage of c‐Fos labeled OT‐immunoreactive neurons in the PVN following a 5‐min RIT (E), and an elevation in circulating OT levels (F), compared to the Paired controls. Such social isolation‐induced increases in heart rate (G) and immobile duration during the FST (H) as well as the decrease in sucrose intake (I) are prevented by daily OT administration. Data are shown as mean ± SEM. *P < 0.05. Alphabetic letters indicate the results from a post‐hoc test following an ANOVA. Bars labeled with different letters differ significantly from each other. Data adapted, with permission, from ().


Figure 7. The effects of partner separation on the physiology, behavior, and neurochemical staining in the brain of pair‐bonded prairie voles. Compared to the paired controls (paired), 5 days of separation from the mating partner (separated) resulted in increases in heat rate (A), immobile time during a forced swim test (FST) (B), and circulating levels of CORT following the FST (C) in both male and female prairie voles. In male prairie voles, 2 weeks of separation from their female partners led to a decreased entry to the open arms during an elevated plus maze test (EPM) (D) and an increased duration in the dark box during a light‐dark box test (E), in comparison to the Paired controls. Furthermore, these Separated males also showed an increase in social affiliation and a decrease in aggression during an RIT (F) as well as increases in the number of neurons stained for OT and AVP in the paraventricular nucleus of the hippocampus (PVN) (G, H, and I), compared to Paired controls. Data are shown as mean ± SEM. *P < 0.05. Scale bar = 100 μm. Data adapted, with permission, from ().


Figure 8. The effects of IMO stress and social buffering on anxiety‐like behaviors and brain OT activity in female prairie voles. Subjects experience 1‐h IMO stress, recover alone (alone) or with the male partner (partner) for 30 min, and receive a 5‐min EPM test. (A) Females that recover alone (alone) enter the open arms less frequently and spend less time there in the EPM test, compared to handled females (control) and females recovering with a partner (partner). (B) Data from in vivo brain microdialysis show that OT release in the PVN increases during IMO stress, and this increased OT release is sustained during the recovery if the subject recovers with a partner but not alone. (C and D) Intra‐PVN injections of an OTRA in the subjects recovering with the partner block social buffering effects on anxiety‐like behaviors and plasma CORT. Conversely, OT injections into the PVN of the subjects recovering alone mimic the effects of a partner by reducing anxiety like behaviors and circulating levels of CORT (D). Data are shown as mean ± SEM. *P < 0.05. Alphabetic letters indicate the results from a post‐hoc test following an ANOVA. Bars labeled with different letters differ significantly from each other. Data adapted, with permission, from ().


Figure 9. The effects of OT treatment in the PVN on stress induced changes in circulating CORT, anxiety‐like behaviors, and neural activity in female prairie voles. Intra‐PVN injections of OT before an EPS inhibit the stress‐induced rise in plasma CORT (A) and anxiety‐like behavior during the EPM (B). Although such OT injection does not alter the percentage of OT (C) or AVP (D) neurons in the PVN that are double‐labeled with c‐Fos, it decreases the number of CRH/Fos neurons (E) and increases the number of GABA/Fos (F) neurons in the PVN. Blue arrows point to double labeled cells. Furthermore, intra‐PVN injections of the GABAA receptor antagonist, bicuculline (Bic), prevent OT effects in reducing anxiety‐like behavior following the EPS stress (G). (H) A hypothetical model suggesting that OT release in the PVN may activate GABAergic interneurons in the PVN and GABAergic projecting neurons to the PVN, which, in turn, can inhibit CRH neurons and potentially decrease activity of the hypothalamic‐pituitary‐adrenal axis. Data are shown as mean ± SEM. *P < 0.05. Data adapted, with permission, from ().
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Manal Tabbaa, Brennan Paedae, Yan Liu, Zuoxin Wang. Neuropeptide Regulation of Social Attachment: The Prairie Vole Model. Compr Physiol 2016, 7: 81-104. doi: 10.1002/cphy.c150055