Variation in enkephalin immunoreactivity in the social behavior network and song control system of male European starlings (Sturnus vulgaris) is dependent on breeding state and gonadal condition

Stevenson, Tyler J.; Calabrese, Marc D.; Ball, Gregory F.

doi:10.1016/j.jchemneu.2011.12.001

Cited by 5 publications

(4 citation statements)

References 78 publications

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“…If opioid activity underlies song-associated reward, then we predicted that only brain areas involved in song in which opioids are known to induce reward (such as POM) would relate to CPP. To gain insight into this prediction we included as a negative control in our analyses measures of MOR and PENK mRNA expression in HVC, a song control region that contains enkephalin and mu opioid receptors [46] , [62] , [63] but plays no known role in reward. Analyses including MOR and PENK mRNA expression in HVC returned no significant models, indicating that relationships between opioids, CPP, and undirected singing behavior are specific to the POM.…”

Section: Discussionmentioning

confidence: 99%

Reward Associated with Singing Behavior Correlates with Opioid-Related Gene Expression in the Medial Preoptic Nucleus in Male European Starlings

et al. 2014

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Birdsong consists of species-specific learned vocal sequences that are used primarily to attract mates and to repel competitors during the breeding season. However, many birds continue to sing at times when vocal production has no immediate or obvious impact on conspecific behavior. The mechanisms that ensure that animals produce important behaviors in contexts in which the function of these behaviors is not immediate or obvious are not known. One possibility is that animals engage in such behaviors because they are associated with pleasure. Here we examined the hypothesis that male European starlings sing outside of the breeding season in part because the act of singing in this context is facilitated and/or maintained by opioid-mediated reward. We measured song-associated reward using a conditioned place preference (CPP) test in male starlings producing fall, non-breeding season-typical song. We used quantitative real time PCR to measure expression of the enkephalin opioid precursor preproenkephalin (PENK) and mu opioid receptors (MOR) in the medial preoptic nucleus (POM; a region in which opioids are implicated in both reward and starling fall song) and additionally the song control region HVC as a control. Starlings developed a strong preference for a place that had been paired previously with the act of producing fall-typical song, indicating that fall song production was associated with a positive affective state. Both PENK and MOR mRNA expression in the POM, but not HVC, correlated positively with both individual reward state (as reflected in CPP) and undirected singing behavior. These results suggest that singing induces opioid receptor and enkephalin expression in the POM and consequent reward, and/or that opioid release in the POM induced by individual or environmental factors (e.g., the presence of food, safety of a flock or the absence of predators) induces a positive affective state which then facilitates singing behavior.

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Section: Discussionmentioning

confidence: 99%

Reward Associated with Singing Behavior Correlates with Opioid-Related Gene Expression in the Medial Preoptic Nucleus in Male European Starlings

et al. 2014

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“…This antibody has also been validated in starling brain tissue using preadsoption tests (Ball, Absil, & Balthazart, 1995), and in male zebra finches specificity was validated using Western immunoblots (Wada et al, 2006). In a more recent study, pretreatment with leu-ENK also partially blocked immunoreactive staining (Stevenson, Calabrese, & Ball, 2012), therefore, we refer to immunolabeling generally as ENK.…”

Section: Methodsmentioning

confidence: 99%

Modulation of male song by naloxone in the medial preoptic nucleus.

Kelm‐Nelson¹,

Stevenson²,

Cordes³

et al. 2013

Behavioral Neuroscience

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Studies in songbirds implicate opioid neuropeptides in singing behavior, however past results are contradictory. In starlings, the effect of opioid manipulations on sexually-motivated courtship song differed in birds naturally singing at low compared to high rates, and mu-opioid receptors were denser in several regions, including the medial preoptic nucleus (POM) in low singing males. In the present study we found that low singing male starlings also had significantly higher enkephalin (ENK) immunolabeling densities in the POM than high singers. We then blocked opioid receptor activity in the POM with naloxone injections and found that this increased both song rate and song bout length in low singers, suggesting that high densities of mu receptors and ENK in the POM actively suppress song in these males. In contrast to its effects on low singers, naloxone in the POM of high singers dose dependently decreased song rate and tended to reduce song bout length. This suggests that at least some level of opioid activity in POM is necessary for song production. Our results are the first to demonstrate that direct administration of opioids into the POM influences sexually-motivated song and that effects differ depending on an individual’s initial rate of song and associated density of ENK. We suggest that differential effects seen in past studies of opioids and song may in part be explained by differences in the natural song rate of subjects and accompanying differences in enkephalin activity and neural substrate sensitivity to opioids in POM.

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“…After three PBSt washes, sections were incubated with a biotinylated secondary antibody appropriate for the species that the primary antibody was raised in for 1 hour at room temperature. In the present study, the Tyramide Signal Amplification (TSA) Biotin system was used to amplify the signal (NEL700A001; Perkin Elmer, Waltham, MA, USA) . Briefly, once slides had been incubated with the respective biotinylated secondary antibody, they were washed in PBSt and then incubated with streptavidin‐horseradish peroxidase conjugate for 30 minutes at room temperature.…”

Section: Methodsmentioning

confidence: 99%

“…In the present study, the Tyramide Signal Amplification (TSA) Biotin system was used to amplify the signal (NEL700A001; Perkin Elmer, Waltham, MA, USA). 34…”

Section: Immunohistochemistrymentioning

confidence: 99%

Ovarian hormones induce de novo DNA methyltransferase expression in the Siberian hamster suprachiasmatic nucleus

Coyle

Caso

Tolla

et al. 2020

J Neuroendocrinology

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The present study investigated neuroanatomically localised changes in de novo DNA methyltransferase expression in the female Siberian hamster (Phodopus sungorus). The objectives were to identify the neuroendocrine substrates that exhibit rhythmic Dnmt3a and Dnmt3b expression across the oestrous cycle and also examine the role of ovarian steroids. Hypothalamic Dnmt3a expression was observed to significantly increase during the transition from pro‐oestrous to oestrous. A single bolus injection of diethylstilbestrol and progesterone was sufficient to increase Dnmt3a cell numbers and Dnmt3b immunoreactive intensity in the suprachiasmatic nucleus. In vitro analyses using an embryonic rodent cell line revealed that diethylstilbestrol was sufficient to induce Dnmt3b expression. Up‐regulating DNA methylation in vitro reduced the expression of vasoactive intestinal polypeptide, Vip, and the circadian clock gene, Bmal1. Together, these data indicate that ovarian steroids drive de novo DNA methyltransferase expression in the mammalian suprachiasmatic nucleus and increased methylation may regulate genes involved in the circadian timing of oestrous: Vip and Bmal1. Overall, epigenetically mediated neuroendocrine reproductive events may reflect an evolutionarily ancient process involved in the timing of female fertility.

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Variation in enkephalin immunoreactivity in the social behavior network and song control system of male European starlings (Sturnus vulgaris) is dependent on breeding state and gonadal condition

Cited by 5 publications

References 78 publications

Reward Associated with Singing Behavior Correlates with Opioid-Related Gene Expression in the Medial Preoptic Nucleus in Male European Starlings

Reward Associated with Singing Behavior Correlates with Opioid-Related Gene Expression in the Medial Preoptic Nucleus in Male European Starlings

Modulation of male song by naloxone in the medial preoptic nucleus.

Ovarian hormones induce de novo DNA methyltransferase expression in the Siberian hamster suprachiasmatic nucleus

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