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 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 naloxone 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 ENK activity and neural substrate sensitivity to opioids in POM.
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