Links between breeding readiness, opioid immunolabeling, and the affective state induced by hearing male courtship song in female European starlings (Sturnus vulgaris)

Abstract

Male courtship vocalizations represent a potent signal designed to attract females; however, not all females find male signals equally attractive. We explored the possibility that the affective state induced by hearing courtship vocalizations depends on the motivational state of a receiver. We used a conditioned place preference test of reward to determine the extent to which the rewarding properties of hearing male courtship song differed in female European starlings categorized as nest box owners (a sign of breeding readiness) or non-owners. Nest box owners developed a preference for a chamber in which they previously heard male courtship song. Non-owners displayed no preference for a chamber in which they previously heard song. Positive correlations were identified between the preference a female developed for the song-paired chamber and female nesting and dominance behaviors observed prior to conditioning (indices of the motivation to breed). Immunolabeling for met-enkephalin (an opioid neuropeptide involved in reward) in the medial preoptic nucleus, ventromedial nucleus of the hypothalamus, nucleus accumbens, and periaqueductal gray was higher in females with compared to those without nest boxes. Both nest box entries and song-induced place preference also correlated positively with met-enkephalin labeling in the ventromedial nucleus of the hypothalamus. These findings indicate that the reward value of vocal signals is linked to individual differences in motivational state; and that differences in enkephalin activity may play a role in modifying an individual’s motivational state and/or the reward value of song.

Nest box exploration may stimulate breeding physiology and alter mRNA expression in the medial preoptic area of female European starlings

“…the nest cavity exploration principal components factor). These findings are consistent with a previous study in starlings demonstrating greater immunolabeling measurements for the protein product of PENK, met-enkephalin, in the mPOA of female starlings that explored nest boxes compared with those that did not (Riters et al, 2013). We also found that PENK mRNA correlated positively with ERα mRNA expression in the mPOA.…”

“…In female starlings, measurements of immunolabeling for met-enkephalin were higher in mPOA and VMH in females that explored compared with those that did not explore nest cavities (Riters et al, 2013). Met-enkephalin labeling measurements in VMH also correlated positively with the number of times females entered nest cavities and with reward induced by hearing male song (measured using conditioned place preference; Riters et al, 2013). Opioids in both the mPOA and VMH underlie reward induced by paced mating behavior in female rats (García-Horsman et al, 2008).…”

“…those that cannot create their own nest sites), such as starlings, cannot breed without access to cavities (Feare, 1984;Kessel, 1957;Newton, 1994;Scott et al, 1977). In starlings, studies using a conditioned place preference test of reward show that only females with nest cavities find hearing male courtship song to be rewarding (Riters et al, 2013). Furthermore, the reward value of hearing male song correlated positively with the number of times a female was observed entering and exiting a nest cavity (Riters et al, 2013).…”

“…In starlings, studies using a conditioned place preference test of reward show that only females with nest cavities find hearing male courtship song to be rewarding (Riters et al, 2013). Furthermore, the reward value of hearing male song correlated positively with the number of times a female was observed entering and exiting a nest cavity (Riters et al, 2013). It is likely that physiological changes that occur at the onset of the breeding season (e.g.…”

“…Neuromodulators such as opioids are also implicated in the control of female sexual behavior (Acosta-Martinez and Etgen, 2002;García-Horsman et al, 2008;Maney and Wingfield, 1998;Nicot et al, 1997). In female starlings, measurements of immunolabeling for met-enkephalin were higher in mPOA and VMH in females that explored compared with those that did not explore nest cavities (Riters et al, 2013). Met-enkephalin labeling measurements in VMH also correlated positively with the number of times females entered nest cavities and with reward induced by hearing male song (measured using conditioned place preference; Riters et al, 2013).…”