Prodynorphin and kappa opioid receptor mRNA expression in the brain relates to social status and behavior in male European starlings

Abstract

Numerous animal species display behavioral changes in response to changes in social status or territory possession. For example, in male European starlings only males that acquire nesting sites display high rates of sexual and agonistic behavior. Past studies show that mu and delta opioid receptors regulate behaviors associated with social ascension or defeat. Opioids also act at kappa receptors, with dynorphin binding with the highest affinity; however, the role of these opioids in social behavior has not been well studied. We observed flocks of male starlings during the breeding season and ran quantitative real-time polymerase chain reaction (qPCR) to measure expression of kappa opioid receptors (OPRK1) and prodynorphin (PDYN) in brain regions involved in social behavior and motivation (ventral tegmental area [VTA], medial preoptic nucleus [mPOA]) and vocal behavior (Area X). Males with nesting territories displayed more sexual/agonistic behavior than males without nesting territories. They also had lower OPRK1 expression in VTA and mPOA. OPRK1 expression in VTA correlated negatively with sexual/agonistic behaviors, consistent with past studies showing kappa receptors in VTA to inhibit sociosexual behaviors. PDYN in mPOA correlated negatively with a measure of nesting behavior that may also reflect sexual motivation. PDYN in Area X related positively to song. Distinct patterns of OPRK1 and PDYN expression in VTA, mPOA, and Area X related to gonad volume, suggesting that breeding condition may modify (or be modified by) OPRK1 and PDYN expression. Studies are now needed to further characterize the role of OPRK1 and PDYN in status-appropriate social behaviors.

Social status and demographic effects of the kappa opioid receptor: a PET imaging study with a novel agonist radiotracer in healthy volunteers

“…With lower social status viewed as a stressor, our findings of increased KOR levels largely fit with the extant animal literature on social processes, and more exactly, with the lone study on social status and KOR (in male European starlets) [23]. Pair bonding, an important social behavior, has been more studied and found to be influenced by KOR in monogamous animals such as titi monkeys and prairie voles [40][41][42].…”

“…Mice given a KOR antagonist, or lacking a gene for dynorphin (i.e., Pdyn), did not show a typical defeated posture after exposure to repeated social defeats compared with placebo animals [21]. In the nucleus accumbens, an area integral to rewards, KOR-mediated social aversion in prairie voles [22], social status in starlings [23], and in rats there was an upregulation with social isolation [12]. Susceptible and resilient animals have also shown different expression levels of dynorphin mRNA in response to social stressors [24,25], although differences have also been reported in this region and others [26].…”

Complex patterns of dopamine‐related gene expression in the ventral tegmental area of male zebra finches relate to dyadic interactions with long‐term female partners

“…Past studies show correlations between a variety of neuronal markers in VTA and bond‐related behaviors observed in males, including the production of courtship and nesting behaviors . Based on these studies, we expected to find that the distinct patterns of gene expression identified between males in the low and high dopamine groups would be associated with differences in the numbers of bond‐related behaviors produced by the males.…”

“…For example, the modification of dopamine release from VTA projection neurons via GABA or glutamate receptor antagonist administration directly into VTA induces pair bonding in male prairie voles . The complex interplay among neuromodulators is highlighted further by studies in songbirds, which show that multiple neuronal markers in VTA (eg, cells labeled for immediate early genes, dopamine‐beta‐hydroxylase, vasopressin V1a receptors, tyrosine hydroxylase, neurotensin, opioid neuropeptides and other measures of catecholamine activity) correlate with pairing‐related behaviors (eg, pairing status, courtship behaviors, clumping, allopreening and nesting). It is also noteworthy that markers in VTA can be associated closely with the behavior that an individual receives from a partner …”

Social creatures: Model animal systems for studying the neuroendocrine mechanisms of social behaviour

“…The brain areas originally implicated are the medial amygdala, medial bed nucleus of the stria terminalis, preoptic area, lateral septum, ventromedial and anterior hypothalamus, and the midbrain periaqueductal grey area and tegmentum . These areas are all mutually connected and use numerous hormones (including in particular prolactin and steroids) and peptides (including gonadotrophin‐releasing hormone, gonadotrophin‐inhibitory hormone, neurotensin, opioids and vasoactive intestinal polypeptide), all of which appear to be relevant to individual, species and seasonal differences in social structure …”