ABSTRACT
Vocal communication is common among social vertebrates, though little is known about the neural mechanisms regulating the motivation to communicate. This study examined a possible role for dopamine and opioids in sexually motivated song in male European starlings. The dopamine reuptake inhibitor GBR-12909 increased singing behavior, whereas the D1 dopamine receptor antagonist SCH-23390 decreased song, suggesting a role for dopamine in the motivation to sing. In contrast, the opioid agonist fentanyl decreased song, and the antagonist naloxone has previously been shown to increase song, findings consistent with a role for opioids in reward associated with song production. These results suggest that dopamine and opioids play opposing roles in the regulation of the motivation to communicate.
Subject(s)
Dopamine Agents/pharmacology , Narcotic Antagonists/pharmacology , Receptors, Opioid/agonists , Sexual Behavior, Animal/drug effects , Starlings/physiology , Vocalization, Animal/drug effects , Analgesics, Opioid/pharmacology , Animals , Dopamine Uptake Inhibitors/pharmacology , Drug Implants , Female , Fentanyl/pharmacology , Male , Motivation , Naltrexone/pharmacology , Orchiectomy , Piperazines/pharmacology , Receptors, Dopamine D1/antagonists & inhibitors , Reward , Testosterone/administration & dosage , Testosterone/pharmacologyABSTRACT
Many social animals vocalize at high rates, suggesting that vocal communication is highly motivated and rewarding. In songbirds, much is known about the neural control of vocal behavior; however, little is known about neurobiological mechanisms regulating the motivation to communicate. This study examined a possible role for opioid neuropeptides in motivation and reward associated with song production in male European starlings (Sturnus vulgaris). Peripheral opioid blockade facilitated male song production. Furthermore, methionine-enkephalin immunolabeled fiber densities within brain regions in which opioids are known to regulate motivation and reward (i.e., the medial preoptic nucleus and ventral tegmental area) related positively to male song production. These data suggest that song production might be regulated by opioid activity within motivation and reward neural systems.
Subject(s)
Animal Communication , Motivation , Narcotics/pharmacology , Social Behavior , Starlings/physiology , Animals , Female , Male , Narcotic Antagonists/pharmacology , Neuropeptides , Receptors, Opioid/physiology , Reinforcement, PsychologyABSTRACT
In songbirds, a major function of song during the breeding season is mate attraction, and song in this context can be highly sexually motivated. Vocal learning, perception, and production are regulated by the song control system, but there is no evidence that this system participates in the motivation to sing. Instead, brain regions involved in sexual motivation and arousal, including the medial preoptic nucleus (POM), bed nucleus of the stria terminalis (BST), nucleus taeniae (Tn), and area ventralis of Tsai (AVT) might regulate the motivation to sing, at least in a sexual context. The role of these nuclei and song control nuclei (area X and HVC) in vocal production within a breeding context, and other courtship behaviors, was investigated using immunocytochemistry for protein products of immediate early genes (IEGs), ZENK and c-fos (Fos), in flocks of male house sparrows (Passer domesticus) presented with females. Compared to vocalizations from other perches, vocal behavior from a nest box is more likely directed toward females, and sexually motivated. The numbers of ZENK and Fos labeled cells within rostral, but not caudal POM related positively only to vocalizations produced from a nest box. In contrast, the number of ZENK-labeled cells within area X related negatively to vocalizations from a nest box. Additionally, numbers of IEG-labeled cells within rPOM, Tn and AVT related positively to mount attempts. The results support the hypothesis that the POM interacts with the song control system to regulate sexually motivated vocal expression, and are consistent with work indicating that (a) rostral and caudal POM play distinct roles in sexual behavior, and (b) involvement of area X in song is context specific.
Subject(s)
Brain/physiology , Genes, Immediate-Early/physiology , Sexual Behavior, Animal/physiology , Social Environment , Sparrows/physiology , Vocalization, Animal/physiology , Amygdala/physiology , Animals , Appetitive Behavior/physiology , Courtship , Female , Gene Expression Regulation , Immunohistochemistry , Male , Motivation , Nesting Behavior/physiology , Preoptic Area/physiology , Ventral Tegmental Area/physiologyABSTRACT
Reproduction results from a complex interplay among multiple factors including social stimuli, hormones, the brain, and an individual's physical characteristics. Male house sparrows (Passer domesticus) possess a bib of black feathers, or badge, that is associated with behaviors important for reproduction including courtship behaviors, copulation, and aggression. Such behaviors are controlled by testosterone activity within the central nervous system and are strongly influenced by social status and female behavior. To understand how multiple factors interact to coordinate reproductive activity we explored relationships among social status, badge size, gonad volume, and the volumes of brain regions involved in male courtship and dominance (HVC, robust nucleus of the archistriatum, and the medial preoptic nucleus). A trend toward a U-shaped relationship was observed between dominance status and badge size, with the most dominant and most subordinate males possessing the largest badges. Male vocal expression, copulation, and aggression were positively related to dominance status, but not badge size. In contrast, the volumes of HVC, the medial preoptic nucleus and the gonads related positively to badge size, but not dominance. Females preferentially approached large-badged males regardless of dominance status, but this interest translated into copulation for dominant rather than subordinate males, a finding possibly related to the observation that dominant males vocalized at higher rates than subordinates. Subordinate males that had large badges, attracted female interest, and possessed the neuroendocrine potential to perform courtship behaviors might have been prevented from doing so through social interactions with dominant males within the flock.