The neurobiology of pair bonding.

“Similar patterns of activity occur when mothers view images of their own children, suggesting some overlap between the neural mechanisms of maternal attachment and those of romantic lov”

“For instance, how olfactory information about a mate interacts with reward systems during mating to result in pair-bonding behavior of prairie voles has been worked out in spectacular detail (Insel & Young 2001, Young & Wang 2004).”

“The neuropeptide oxytocin (OT) has received considerable attention in preclinical and human research for its role in mediating social affiliation, mother–child attachment, social support and trust (Young and Wang, 2004; Kosfeld et al., 2005).”

“— which is in line with animal studies indicating that central OXT facilitates pair bonding behaviou”

“In rodents, most studies on social behavior have focused on socio-sexual behaviors, such as pair bonding and behaviors related to sexual competition (Aragona et al., 2006; Curtis and Wang, 2005; Gingrich et al., 2000; Leypold et al., 2002; Liu and Wang, 2003; Young et al., 2001; Young and Wang, 2004).”

“Evidence for the key role of oxytocin in prosocial behavior and affiliation has come primarily from studies in animals (Bartz and Hollander, in press; Carter 1998; Ferguson et al 2000; Young and Wang 2004).”

“During pairbond formation in monogamous female voles (Microtus ochrogaster), a process involving the mesolimbic reward system (Young and Wang, 2004), neuronal activity as measured by c-fos induction increases in the BNST (Curtis and Wang, 2003).”

“These effects seem to be consistent with observations that indicate general effects of oxytocin on social behaviour”

“More recently, OT and AVP have been identified as essential chemical mediators of social bonding in animals (Insel 2003, Keverne & Curley 2004, Young & Wang 2004).”

“We hypothesize that pair bond formation is the result of an association between the rewarding mating experience and the olfactory signature of the partner [55].”

“Neural models for parental care in rats are indicated by broken black lines and for pair bonding formation in prairie voles by dotted black lines [10,19,80].”

“005 E D P R O O F studies have previously shown an association between the AVPR1a receptor gene and autism [90,143,156], as well as partner preference in the male prairie vole [165].”

“…to form and maintain social bonds plays an integral role in functional interpretations of many aspects of behaviour, such as reconciliation in monkeys (Aureli & de Waal 2000), coalitions in cetaceans (Connor et al. 1998; Connor 2007) and pair bonding in microtine rodents (Young & Wang 2004).”

“For instance, there is some evidence that AVP plays particular roles in prosocial behavior in males, and it has also been shown to mediate aggressive behaviors and territoriality in many species (Caldwell et al., 2008; Donaldson & Young, 2008; Young & Wang, 2004).”

“In prairie voles, this is sufficient time for a pair bond to form (41).”

“These stimulations increase oxytocin release in mesocorticolimbic pathways; blocking the oxytocin neurotransmission abolished social attachment, indicating that an oxytocin pathway is indispensable for attachment (Insel et al. 1997; Kendrick 2004; Wang & Aragona 2004; Young & Wang 2004).”

“Sexual differentiation of the brain in adulthood Arginine vasopressin fibers innervate the septal region in rats and contribute to pair bonding and parental behavior in a variety of rodents (see accompanying revie”

“…vole animal model of social attachment is complemented by the natural comparison of two other vole species, the non-monogamous montane and meadow voles (Microtus montanus and Microtus pennsylvanicus), in addition to the monogamous pine vole (Microtus pinetorum) (reviewed in Young and Wang, 2004).”

“Furthermore, the strong impact of OT on female social behavior (3), and the disproportionately high risk of men for social disorders (80), suggest sexdependent genotype effects at the neural systems level, particularly as emotional deficits have been previously associated with male, but not female, rs53576A carriers (…”

“OXT is especially involved in mating, pair bonding, and mother—offspring attachment in mammals (Insel and Young, 2001; Young and Wang, 2004).”

“, 2000a) and promotes social behavior, including pair bonding, maternal behavior, sexual behavior, and social attachment in animals (Carter, 1998; Uvnas-Moberg, 1998a; Insel and Young, 2001; Pedersen and Boccia, 2003; Young and Wang, 2004).”

“3 The neuropeptide oxytocin (OT), found in the hypothalamus and limbic brain regions, has received considerable attention in preclinical and human research for its role in mediating social affiliation, attachment, social support, maternal behavior and trust”

“For a more in depth review on pair bonding and its genetic regulation, see (Insel, 2003; Aragona and Wang, 2004; Young and Wang, 2004; Lim et al., 2004a; Young et al., 2005; Hammock and Young, 2006; Lim and Young, 2006; Nair and Young, 2006).”

“has proven to be an excellent model for neurobiological investigations of pair bondin”

“…in other forms of reward processing (e.g., food, drugs, etc.), underlie social processes such as pair-bonding [Young, Murphy Young, & Hammock, 2005; Young & Wang, 2004] and mother–offspring bonding [Levy, Kendrick, Goode, Guevara-Guzman, & Keverne, 1995] in small rodents [Febo, Numan, & Ferris,…”

“, montane voles (Microtus montanus), meadow voles (Microtus pennsylvanicus), and prairie voles (Microtus ochrogaster) (2).”

“OT and AVP have been shown to play a critical role in the regulation of social behaviors (Insel et al., 1994) and monogamous pair-bonding in rodent mammals (Young et al., 2001; Lim and Young, 2004; Young and Wang, 2004).”

“In the remainder of this section, we describe this attachment formation process and the resulting physiological coregulation in detail.”

“DAergic cells in the ventral tegmental area (VTA) project to the NAcc and prefrontal cortex (PFC), as well as other forebrain regions.”

“…stimulate the production of oxytocin, vasopressin or endorphines: neuropeptide mechanisms underlying social-bonding processes in different species (Young and Wang, 2004; Dunbar, 2010); last but not least, (3) during ventroventral contact, mouth-to-mouth kissing can act as a means for the…”

“Animal studies have convincingly demonstrated an interaction between sexual activity, the release of the anterior pituitary neuropeptides oxytocin and vasopressin, and pair bond formation (Young and Wang, 2004).”

“In non-human mammals, research shows that central administration of OT agonists enhances social recognition, memory for peers, the development of partner preference, and partner bonding (for a review see (Young and Wang, 2004)).”

“Multiple lines of evidence indicate oxytocin is also key neurobiological substrate underlying the development of partner preferences (see review Young and Wang, 2004).”

“While the roles of OT, vasopressin, and DA in the NAs and VP in regulating pair bonding have been well documented (Young et al., 2011; Young and Wang, 2004), the precise neural mechanisms by which these molecules lead to the formation of a selective social preference for the partner has yet to be determined, and is th…”

“OT is involved in social recognition and maternal behavior (116, 117).”

“Vasopressin activity has been associated with aggression, anxiety, and social behavior (reviewed in Kelly and Goodson, 2014), as well partner preference formation in male prairie voles (Cho et al., 1999; Young and Wang, 2004).”

“The monogamous prairie vole is highly social, craves social contact, and forms enduring social bonds with its mate (Carter et al., 1995; Young and Wang, 2004).”

“These functions include, for example, learning and memory (de Wied et al., 1993), reproductive and other social behaviors (Goodson and Bass, 2001; Panzica et al., 2002; Rose and Moore, 2002; Young and Wang, 2004).”

“Further, words such as “infidelity” and “adultery” are frequently used to describe CNM relationships; these terms, of course, discount the possibility that extradyadic relationships may have been agreed upon by both members of a couple (Finch, 2009; Young & Wang, 2004).”

“For example, the links between attachment and sexual motivations have been recognized (Diamond, 2003), and animal models of this have been proposed (Young & Wang, 2004).”

“Species differences in OTR density in the NAcc have been associated with species differences in mating strategy (social monogamy vs polygamy) and alloparental behavior, suggesting that variation in OTR receptor expression may underlie species differences in social organization and behavior (Insel et al., 1991; Young a…”

“As noted by Wang and Young (Lim et al., 2004b; Young and Wang, 2004), the cellular mechanism might be the co-activation of D2-expressing accumbal neurons by vasopressin and/or oxytocin.”

“For example, studies show that prairie voles have high levels of oxytocin and vasopressin receptors in the prelimbic cortex, nucleus accumbens and ventral pallidum–regions involved in the mesolimbic dopamine reward system–and some researchers theorize that pair-bonding may be a specialized form of conditioned reward l…”

“Figure adapted from Young and Wang ( 2004 ) lower than in prairie voles ( Insel et al .”

“…animal studies showing an involvement of the neuropeptides oxytocin and vasopressin in social behavior, anxiety, and stress regulation (Insel, 2010; Young & Wang, 2004), there is growing literature suggesting that these very same mechanisms are involved in the regulation of human sociality…”

“A key example is Oxt release into the vStr, which promotes affiliative social behavior (Liu and Wang, 2003; Shahrokh et al., 2010; Young and Wang, 2004).”

“…Bale et al., 1995 The most obvious link between the dopamine (DA) and OT system stems from the fact that, at least in humans, social affiliative behaviour (which is modulated by OT) is accompanied by modulation of dopaminergic reward pathways (Skuse and Gallagher, 2009; Young and Wang, 2004).”

“…the brain circuits involved in motivation and reward, it has been hypothesized that both oxytocin and vasopressin may be facilitating affiliation and social attachment in monogamous species by modulating these reward pathways (Insel & Young 2001; Young et al. 2001; Insel 2003; Young & Wang 2004).”

“For example, non-monogomous male Montane voles have few V1a receptors in the ventral pallidum (VP) compared to monogamous Prairie voles, and induction of V1a receptors in the VP of Montane voles by viral vector gene transfer results in pair bonding similar to that seen in Prairie voles (Young and Wang, 2004).”

“Both pregnancy and oestrus provide the endocrine context for the synthesis of OT and the OT receptors (Thomas et al. 1996; Bale & Dorsa 1997; Young et al. 1997).”

“…mammals, receptors for the neuropeptide oxytocin are distributed in various brain regions that are associated with the ability to form normal social attachments and affiliation, including parental care, pair bonding, and social memory (Carter, 1998; Uvnas-Moberg, 1998; Young and Wang, 2004).”

“Hence, OT is known to facilitate partner preference formation (Insel and Hulihan, 1995), and microinjection of CRF into the NAc accelerates partner preference formation in male prairie voles, an effect mediated by CRFR2 (Young and Wang, 2004; Lim and Young, 2006).”

“Our first studies of the role of the AVPR1a gene in social cognition exemplified by a simple laboratory paradigm converges with a wide range of both animal and human experimentation showing that arginine vasopressin (AVP) and the closely related oxytocin (OT) are key neuropeptides that facilitate social communication,…”

“This hypothesis gains further support from the high receptor concentrations in this region for neuropeptides such as oxytocin (Freedman et al., 2000; Young and Wang, 2004), which are known to enhance trust and cooperation among humans (Zak et al.”

“In support, across species, it has been found that the AVP system may predominantly regulate male social behaviors, while the OXT system is primarily required for female social behaviors (de Vries and Miller, 1998; Gimpl and Fahrenholz, 2001; Keverne and Curley, 2004; Lim et al., 2004; Young and Wang, 2004; Bielsky et…”

“…however, it is important to note that variation n region-specific OT- and AVP-like receptor expression has been inked to individual and/or species diversity in social behaviors in ultiple vertebrate lineages (Goodson et al., 2009; Okhovat et al., 015; Ophir et al., 2012; Young and Wang, 2004).”

“More specific, research has shown that it is associated with the ability to form social attachments and with affiliation, including parental care, pair bonding, sexual behavior, and social memory (Carter, 1998; Insel & Young, 2001; Lim & Young, 2006; Young & Wang, 2004 ).”

“…responses around the aOFC area, which has also been shown to be the neural correlate of attachment in other animal studies of rhesus monkeys, rats, and voles (Young and Wang 2004; Moriceau and Sullivan 2005; Goursaud and Bachevalier 2006), supports the aforementioned interpretation in this study.”

“Still, animal studies affirm that remarkably complex social tendencies can be strongly influenced by single genes in creatures as diverse as flies (Demir and Dickson, 2005) and rodents (Young and Wang, 2004).”

“…reward processes have nevertheless been shown in social contexts that include mating (Agmo & Gomez 1993; Drewett 1973), monogamous pair-bonding (Young & Wang 2004), aggression (Fish et al. 2005), maternal–infant attachment (Insel 2003; Lee et al. 1999) and rough-and-tumble play among…”