Conditioned place preferences induced by hearing song outside the breeding season relate to neural dopamine D1 and cannabinoid CB1 receptor gene expression in female European starlings (Sturnus vulgaris)

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The affective state induced by sensory stimuli changes to adaptively modify behaviors that are critical for survival and reproduction. In European starlings, during the spring breeding season, male courtship song is rewarding to females, but only to those that possess resources that are necessary for reproduction (i.e., nesting sites). In fall, starling song is non-sexual and proposed to maintain flocks. This suggests that in fall it may be adaptive for females to be rewarded by fall rather than spring, courtship song. We used a conditioned place preference (CPP) test to evaluate song-induced affective state in fall condition females and quantitative real-time PCR to measure expression of genes that modulate affective state (CB1 endocannabinoid and D1 dopamine receptors) in brain regions that were previously implicated in song-induced reward (i.e., the medial preoptic nucleus (mPOA) and ventromedial hypothalamus (VMH)). Fall condition females developed an aversion to a place that had been paired with playback of both male fall and courtship song, indicating that in general male song induces a negative affective state outside the breeding season. Song-induced aversion was stronger in birds conditioned towards an initial place preference. For mPOA, CB1 receptor expression correlated positively with fall and spring song-induced CPP. D1 receptor expression correlated negatively with fall (but not spring) song-induced CPP, and the ratio of CB1 to D1 receptor expression correlated positively with fall (but not spring) song-induced CPP. These correlations suggest that interactions between D1 and CB1 receptors in mPOA may play a role in modifying affective responses to song.