Dopamine regulation of social choice in a monogamous rodent species

“Such behaviors are the result of selection processes that favored reciprocity among close social groups, in which it was adaptive for individuals to spend relatively small amounts of energy to help unrelated members of the group in order to receive relatively large benefi ts of the resulting social organization (Pfeif…”

“…voles show high levels of parental care (Getz and Carter, 1996; Thomas and Birney, 1979) and it has been suggested that both parents are necessary for pup survival which selected for highly enduring pair bonds (Emlen and Oring, 1977; Kleiman, 1977; McGuire et al., 1993; Wang and Novak, 1992).”

“In particular, DA transmission within the NAc is critical for important aspects of reward processing (Berridge and Robinson, 2003; Everitt and Robbins, 2005; Roitman et al., 2005, 2008; Salamone and Correa, 2002; Wheeler et al., 2008) that may underlie cost-benefi t analyses related to choice…”

“Finally, we compare these fi ndings to studies that have examined the neural regulation of social decision-making in humans (Fisher et al., 2005; Kosfeld et al., 2005; Rilling et al., 2002).”

“While apomorphine binds both D1 and D2-like receptors, it binds D2-like receptors with a much greater affi nity (Missale et al., 1998).”

“, 2006; Wang and Aragona, 2004; Young and Wang, 2004) and associative learning is signifi cantly regulated by mesolimbic DA transmission (Di Chiara and Bassareo, 2007; Kelley, 2004; Wise, 2004).”

“…because it involves more than one agent and thus requires more sophisticated learning alorithms (Lee, 2008), or if it is more informative to regard social decision-making as largely guided by emotional social motivation and hedonic processing (Sanfey et al., 2003; Skuse and Gallagher, 2009).”

“These data indicate that, under natural circumstances, DA transmission is not uniformly increased as it is under certainly laboratory conditionings (Schultz, 2002).”

“Thus, DA transmission within the NAc shell may regulate partner preference formation through enhanced reward processing or incentive motivation (Berridge, 2007; Di Chiara and Bassareo, 2007).”

“However, the dynamic interplay between these two peptides and a host of other molecules, such as dopamine (Aragona & Wang 2009, Young et al. 2011) and endogenous opioids (Burkett et al. 2011), supports social behaviors, especially in the face of challenge.”

“to maintain the existing pair bond [8,10] and to limit extra-pair copulations.”

“Pair bonded males will then exhibit affiliative behavior towards their mates while expressing aggressive behavior towards strangers that can be blocked through antagonism of D1-like receptors within the nucleus accumbens (Aragona and Wang, 2009).”

“Many studies have also investigated the role of the mesolimbic dopamine system and opioid regulation of rewarding social behaviors such as pair-bonds between mates (Aragona, 2009; Resendez et al., 2012); we describe these and additional research avenues throughout.”

“These data suggest that the plastic change in D1R that occurs during pair bonding is causative in the development of selective aggression behavior , which helps to prevent the formation of a new pair bond with a new potential mate ( these topics are reviewed in Aragona and Wang 2009 ) .”

“Ever increasing evidence from diverse organisms ranging from worms to insects to vertebrates suggests that the evaluation of stimulus salience is regulated by catecholamines, particularly DA [7,22,157,196,263].”

“Also, we have focused our discussion on appetitive cue processing, but dopamine is also involved in processing aversive or dysphoric motivational states (Aragona and Wang, 2009; Badrinarayan et al., 2012; Chaudhury et al., 2012; Faure et al., 2008; Kapur et al., 2005; Lemos et al., 2012; Oleson et al., 2012; Pezze and…”

“The roles of oxytocin, vasopressin, dopamine, and CRF in social cognition have been explored using the partner preference test (PPT) as a laboratory proxy for pair bond formation (Lim et al, 2004, 2007; Curtis et al, 2006; Aragona and Wang, 2009; Ross and Young, 2009).”

“Moreover, DA is also involved beyond motor learning in the representation of social cues in mammals (Wang et al., 1999; Anstrom et al., 2009; Aragona and Wang, 2009).”

“For this reason, the present study characterized the relationships between mating onset and pregnancy as well as the relationship between pregnancy status of the female and selective aggression (i.e., the behavioral index of pair bond maintenance) (Carter and Getz, 1993; Aragona and Wang, 2009).”

“There is also evidence that the mesolimbic DA system can play a critical role in at least some forms of social behavior (Aragona et al., 2003, 2006; Aragona and Wang, 2009; Curtis and Wang, 2005).”

“, 1993) that are regulated by reward circuitry (Aragona and Wang, 2009).”

“…University of Washington, United States Copyright Resendez et al. This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited. behavioral and anatomical…”

“OTR in the nucleus accumbens has been associated with reward-mediated affiliative behavior and parental care (e.g. Aragona and Wang, 2009; Olazábal and Young, 2006), and receptors in the ventromedial hypothalamus have been implicated in sexual behavior and vary with reproductive status (Bale et…”

“These are described elsewhere in the context of social monogamy and maternal behavior (Aragona and Wang, 2009; Burkett and Young, 2012).”

“Its release and actions depend on many other neurochemicals, including endogenous opioids and dopamine [9].”

“However, unlike OXTR, there are multiple dopamine receptors, and more selective pharmacological manipulations suggest that D2-like dopamine receptor (D2R) stimulation facilitates bonding while D1-like receptor (D1R) stimulation impairs preference formation in male and female prairie voles (42, 43, 45, 46).”

“Adapted from Aragona & Wang 2009, Liu & Wang 2003, Ross et al., 2009b, Sun et al., 2014, Young et al., 2011a. Horm Behav.”

“…monogamous prairie vole (Microtus ochrogaster), and we know a limited amount about the critical variables that differentiate prairie voles from other non-monogamous vole species (Carter et al., 2008; Donaldson and Young, 2008; Aragona and Wang, 2009; Ross and Young, 2009; McGraw and Young, 2010).”

“Dopamine D1 receptors in the NAc shell play an intriguing role in the formation and maintenance of pair bonds between male and female prairie voles (Aragona and Wang, 2009).”

“Data adapted, with permission, from (11, 102, 274, 283).”

“…across vertebrates, have shown that reciprocity, cooperativeness and social rewards activate reward processing areas with strong dopaminergic (DA) input (for instance, Schultz et al., 1997; Salamone and Correa, 2002; Wickens et al., 2007; Aragona and Wang, 2009; O’Connell and Hofmann, 2011, 2012).”

“It has been appreciated that the activation of D2 receptors is particularly important in social reactivity (Gingrich, Liu, Cascio, Wang, and Insel, 2000; Aragona et al., 2006; Aragona and Wang, 2009; Cibrian-Llanderal et al., 2012).”

“…produce long term alterations of receptor signaling and cellular physiology in the nucleus accumbens (Aragona et al., 2003; Aragona et al., 2006; Aragona and Wang, 2007, 2009; Bradley and Meisel, 2001; Bradley et al., 2004; Bradley et al., 2005; Hedges et al., 2009; Meisel and Mullins, 2006;…”

“Previous studies in rats have shown that infusion of AMPH into the NAc shell increases USVs (Burgdorf et al. 2001) and DA regulation of pair bonding is also specific to the NAc shell (Aragona et al. 2003, 2006; Aragona & Wang 2007, 2009).”

“Co-activation of OT or AVP (i.e. for social memory) and D2 (i.e. for Motivational) results in pair bond formation (Aragona et al., 2003, Aragona and Wang, 2009).”

“…cingulate cortex (ACC; Johnson et al., 2022), insular cortex (Dolensek et al., 2020), and subcortical deep brain structures such as the amygdala (Joëls et al., 2018; Wu et al., 2021), nucleus accumbens (NAc; Aragona and Wang, 2009), and periaqueductal gray (Buhle et al., 2013; Reis et al., 2021).”

“Through modulation of dopamine signaling, oxytocin may have shifted the salience of facial stimuli (Aragona and Wang, 2009; Groppe et al., 2013), boosting motivation to pursue social information (Caldwell and Albers, 2016) and thereby enhancing eye gaze among patients.”

“, 2001), dopamine (Aragona and Wang, 2009; Hostetler et al., 2011; Resendez et al., 2016), and opioid systems (Burkett et al.”

“…involving the D2-like receptor pathway in other animals, in male prairie voles, activation of the D2-like receptors D.F. Antunes et al. Molecular and Cellular Endocrinology 550 (2022) 111649 in the nucleus accumbens lead to an increase of time spent in contact with a familiar mate (Aragona, 2009).”

“And the NAcc D1 receptors play an important role in maintenance of monogamous social bonding in prairie voles (Aragona et al., 2006; Aragona and Wang, 2009).”

“Although drugs of abuse hijack the dopamine reward system, its natural function appears to be the evaluation of stimulus valence (Aragona & Wang, 2009; O’Connell & Hofmann, 2011a, 2011b; Reiner et al., 1998; Wise, 2004b).”

“Because mesocorticolimbic DA underlies partner preference formation (Wang et al. 1999; Gingrich et al. 2000; Aragona et al. 2003; Gobrogge et al. 2008; Aragona and Wang 2009), studies 244 K.”

“…and may provide a reinforcement signal to the BG (Schultz et al., 1993; Phillips et al., 2003), while tonic dopaminergic signaling would be involved in the representation of motivational state related to social cues and contexts (Wang et al., 1999; Anstrom et al., 2009; Aragona and Wang, 2009).”

“…of social stimuli is extremely impor - tant in view of increasing evidence that the MDS can play a critical role in a wide range of social phenomenon ranging from pair bonding to peer relationships (Aragona and Wang 2009 ; Forero et al. 2024 ; Lee and Beery 2021; Loth and Donaldson 2021 ).”

“The second network is the mesolimbic reward system, which is involved in motivation and reward seeking behaviors, the facilitation of reinforcement, decision-making, hedonic processing, and social choice (Wickens et al., 2007; Aragona and Wang, 2009; Báez-Mendoza et al., 2021).”

“In voles, and likely other mammals, dopamine interacts with neuropeptides such as oxytocin and vasotocin to facilitate formation of social bonds between mates, between parents and offspring, and during other affiliative interactions with conspecifics [62,74,75].”

“OT also affects the NAc (which has dense dopamine and OT receptors) that through its connectivity with the mPFC is involved in decision utility estimation, allowing computation of salience value ("Is this social cue rewarding?") (MeyerLindenberg et al. 2011; Chevallier et al., 2012; Adolphs, 2008; Aragona and Wang, 20…”

“D1 receptor signaling may promote pair bonding in part through its role in promoting selective aggression toward non-partners following pair bonding (Aragona and Wang, 2009).”

“These findings, aligned with previous studies on DR1 signalling in pair bond maintenance (Aragona and Wang, 2009), reveal a novel DA-mediated mechanism for partner-seeking behaviour during partner loss in female prairie voles.”

“These subtypes differentially regulate bond formation and maintenance in prairie vole pairs (Curtis et al., 2006; Aragona and Wang, 2009): activation of the D2 system facilitates selective social preferences and thereby formation (Wang et al.”

“Although much attention has been focused upon the roles of vasopressin and oxytocin in causing differences in cooperative behavior (Donaldson and Young 2008; Goodson et al. 2009; Okhovat et al. 2015), there are a number of other candidate neural and neuroendocrine systems that may regulate the expression of cooperativ…”

“…that, in diverse species, modulates the selection of behavior patterns such as basic motor programs (Joshua, Adler, & Bergman, 2009; Vidal‐Gadea et al., 2011), social behavior (Aragona & Wang, 2009; O’Connell & Hofmann, 2011b), and learning and memory (Hyman, Malenka, & Nestler, 2006; Wise, 2004).”

“Taken together, in voles, D2R signaling is essential for social memory formation and/or pair bonding, whereas D1R signaling is required for the maintenance of formed memories and/or the behavioral change after pair bonding (Aragona and Wang, 2009).”