Opposing Regulation of Pair Bond Formation by cAMP Signaling within the Nucleus Accumbens Shell

Aragona, Brandon J.; Wang, Zuoxin

doi:10.1523/jneurosci.3216-07.2007

Cited by 37 publications

(37 citation statements)

References 52 publications

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“…Here, we demonstrate that blockade of -opioid receptors (known to mediate aversion) (Mucha and Herz, 1985;Pfeiffer et al, 1986), but not -opioid receptors (known to mediate reward and positive hedonics) (Weeks, 1962;Bozarth and Wise, 1981), prevents selective aggression. These effects are specific to the NAc shell, a component of brain motivational circuitry that is critical for neural processing of both social bonding (Li and Fleming, 2003;Champagne et al, 2004;Aragona et al, 2006;Aragona and Wang, 2007) and unconditioned incentives, including those of an aversive nature (Kalivas and Duffy, 1995;Ikemoto and Panksepp, 1999;Kelley and Berridge, 2002;Everitt and Robbins, 2005;Becker, 2009). As such, the current data suggest that -opioid receptors within this region may facilitate the tagging of social stimuli as aversive and cause novel conspecifics to be aggressively rejected.…”

Section: Discussionmentioning

confidence: 99%

κ-Opioid Receptors within the Nucleus Accumbens Shell Mediate Pair Bond Maintenance

et al. 2012

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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 established that social behaviors in other species are mediated by endogenous opioid systems, opiate regulation of pair bond maintenance has never been studied. Here, we used resident-intruder testing to determine whether endogenous opioids within brain motivational circuitry mediate selective aggression in prairie voles. We first show that peripheral blockade of -opioid receptors with the antagonist norbinaltorphimine (nor-BNI; 100 mg/kg), but not with the preferential -opioid receptor antagonist naloxone (1, 10, or 30 mg/kg), decreased selective aggression in males. We then provide the first comprehensive characterization of -and -opioid receptors in the prairie vole brain. Finally, we demonstrate that blockade of -opioid receptors (500 ng nor-BNI) within the nucleus accumbens (NAc) shell abolishes selective aggression in both sexes, but blockade of these receptors within the NAc core enhances this behavior specifically in females. Blockade of -opioid receptors within the ventral pallidum or -opioid receptors with the specific -opioid receptor antagonist H-D-Phe-Cys-Tyr-D-Trp-Arg-Thr-PenThr-NH2 (1 ng CTAP) within the NAc shell had no effect in either sex. Thus, -opioid receptors within the NAc shell mediate aversive social motivation that is critical for pair bond maintenance.

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Section: Discussionmentioning

confidence: 99%

κ-Opioid Receptors within the Nucleus Accumbens Shell Mediate Pair Bond Maintenance

et al. 2012

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“…Although such electrophysiological studies are unable to identify the subtype of DA receptors expressed on individual neurons, anatomical studies demonstrate that the NAcc is comprised of projection neurons that express either D1Rs or D2Rs with very little coexpression (33). Psychostimulants preferentially activate intracellular signaling pathways downstream from D1Rs (as determined by increased phosphorylation of signaling molecules) (34) and we have previously shown that increased activation of these signaling pathways prevents partner preference formation (35). Thus, although DA transmission within the NAcc plays an important role in the response to AMPH and the formation of partner preferences, these behaviors are likely mediated through distinct microcircuitries that comprise striatal projection systems (33,36).…”

Section: Discussionmentioning

confidence: 99%

“…Specific antisense riboprobes (Table 1) were used for D1R, D2R, TH, and DAT in situ mRNA labeling. Labeling was conducted with 35 S-labeled probes and sense mRNA controls for each DA marker as previously described (51). For Western blotting analysis, DAR protein was extracted from the supernatant of NAcc tissue punches and assayed as described previously (52).…”

Section: Methodsmentioning

confidence: 99%

Nucleus accumbens dopamine mediates amphetamine-induced impairment of social bonding in a monogamous rodent species

Liang

Aragona

Young

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

119

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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, we examined the effects of repeated AMPH exposure on pair bonding. Intact and saline pretreated control males displayed mating-induced partner preferences, whereas males pretreated with AMPH at the doses effective to induce CPP failed to show mating-induced partner preferences. Such AMPH treatment also enhanced D1, but not D2, DA receptor expression in the nucleus accumbens (NAcc). Furthermore, pharmacological blockade of D1-like DA receptors in the NAcc rescued mating-induced partner preferences in AMPH-treated males. Together, our data indicate that repeated AMPH exposure may narrow the behavioral repertoire of male prairie voles via a DA receptor-specific mechanism in the NAcc, resulting in the impairment of pair bond formation.vole | CPP | D1 Receptor I t is widely accepted that motivated and emotional behaviors that promote fitness are regulated by brain reward circuitry including the mesolimbic dopamine (DA) system (1, 2). Although this system is often implicated in food intake and sexual behavior (3, 4), it has also been implicated in other naturally occurring motivated behaviors, such as social play between juveniles and social bonding between parent and offspring (5-9). Often underrepresented in research are the social bonds formed between adult mates, i.e., pair bonds. Recent investigation using a socially monogamous rodent species, the prairie vole (Microtus ochrogaster) (10-12), indicate that a great deal of the neural regulation underlying pair bond formation and maintenance occurs within the nucleus accumbens (NAcc) (13-15)-a mesolimbic brain region critical for mediating motivated behaviors (1, 2, 16).Although motivational circuitry evolved to promote fitness enhancing behavior such as feeding, mating, and social bonding (1, 17), it is vulnerable to artificial usurpation by drugs of abuse (8). For example, administration of psychostimulant drugs of abuse, such as cocaine and amphetamine (AMPH), results in persistent alterations of mesolimbic DA activity (18,19). The intense impact on this circuit by these and other addictive drugs has been suggested to decrease the perceived value of natural incentives (20), including those of a social nature (8). Although it is known that drug addicts show impaired social behavior (21), the neural regulation of interactions between drug experience and social attachment is poorly understood. This is because, in part, such interactions are difficult to model in traditional laboratory rodents that do not exhibit social bonding between adult conspecifics.The neurobiology of su...

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“…Data from prairie voles has provided strong evidence that the dopaminergic system, specifically dopamine (DA) in the nucleus accumbens (NAcc), plays a fundamental role in the formation and maintenance of pair-bonds [Aragona et al 2003; Aragona et al 2006; Aragona and Wang 2007; Curtis et al 2006; Gingrich et al 2000; Liu et al 2010; Liu et al 2011; Young et al 2011a; Young et al 2011b]. The NAcc is a key neuroanatomical structure involved in various rewarding behaviors.…”

Section: Introductionmentioning

confidence: 99%

Differences in Titi Monkey (Callicebus cupreus) Social Bonds Affect Arousal, Affiliation, and Response to Reward

Ragen

Mendoza

Mason

et al. 2012

American J Primatol

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Titi monkeys (Callicebus cupreus) are a monogamous, New World primate. Adult pair-mates form a bidirectional social bond and offspring form a selective unidirectional bond to their father. Some of the neurobiology involved in social bonds and maternal behavior is similar to the neural circuitry involved in nonsocial reward. Due to these overlapping mechanisms, social states may affect responses to external rewarding stimuli. We sought to determine whether having a social attachment, and/or being in the presence of that attachment figure, can affect an individual’s response to a rewarding stimulus. In addition, we compared affiliative bonds between pair-mates to those between offspring and fathers. Eighteen adult male titi monkeys were either living alone (Lone), with a female pair-mate (Paired), or with the natal group (Natal) (N=6/condition). Each individual went through eight 30-min preference tests for a sweet substance, Tang. For Paired and Natal males, half of the test sessions were with their attachment figure and half were alone. Lone males were always tested alone. Preference scores for Tang, time spent drinking, affiliative, and arousal behaviors were measured. Paired and Natal males emitted significantly more isolation peeps and locomoted more when tested alone compared to when tested with their attachment figure, and paired males engaged in more affiliative behavior than Natal males. Lone males engaged in significantly more behaviors indicative of behavioral arousal such as locomotion and piloerection compared to Paired and Natal males. Finally, paired males drank significantly more Tang and had a significantly greater preference for Tang compared to Lone and Natal males. These results indicate that offspring undergo a behavioral separation response upon separation from their father which persists into adulthood, Lone males are more behaviorally reactive, and that living with an attachment figure and the type of attachment relationship result in different responses to a rewarding sweet stimulus.

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Opposing Regulation of Pair Bond Formation by cAMP Signaling within the Nucleus Accumbens Shell

Cited by 37 publications

References 52 publications

κ-Opioid Receptors within the Nucleus Accumbens Shell Mediate Pair Bond Maintenance

κ-Opioid Receptors within the Nucleus Accumbens Shell Mediate Pair Bond Maintenance

Nucleus accumbens dopamine mediates amphetamine-induced impairment of social bonding in a monogamous rodent species

Differences in Titi Monkey (Callicebus cupreus) Social Bonds Affect Arousal, Affiliation, and Response to Reward

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