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

Abstract

Many temperate zone songbird species exhibit marked seasonal variation in song quality as well as in the motivation to sing. Two brain systems are known to mediate such annual variation in song quality and motivation: (1) the song control system (SCS), and (2) the social behavior network (SBN), respectively. How these two circuits interact to produce changes in singing behavior is not well understood. The opioid enkephalin is expressed in both the SCS and SBN and may function to modulate song quality in a socially relevant manner. Using immunocytochemistry, we examined variation in enkephalin immunoreactivity (ENK-ir) in male European starlings (Sturnus vulgaris) that were in breeding conditions (i.e. photostimulated) or non-breeding conditions (i.e. photorefractory). We also included a group of castrated photostimulated males to investigate the relationship between gonadal steroids and ENK-ir. ENK-ir in the preoptic area (POA) and lateral septum (LS) was greater in photostimulated intact birds as compared to photorefractory males, but not in other regions within the SBN. There was a significant difference in ENK-ir in two forebrain song nuclei, HVC and the lateral nucleus of the anterior medial nidopallium (lMAN), with lower expression in photostimulated intact as compared to photorefractory birds. ENK-ir did not change across breeding conditions in the Nucleus Interface (NIf). After accounting for the volumetric change in HVC and lMAN, the pattern of ENK-ir remained greater in photorefractory compared to intact photostimulated starlings. We propose that the observed regulation of ENK-ir in the POA and LS may be related to seasonal changes in the motivation to engage in singing behavior, while the change in ENK-ir in the song system are associated with the quality of the song produced. Thus seasonal changes in a single neuromodulatory system can have very different functional effects based on the neuroanatomical specificity of its expression.