Sex, estradiol, and spatial memory in a food-caching corvid.

Estrogens significantly impact spatial memory function in mammalian species. Songbirds express the estrogen synthetic enzyme aromatase at relatively high levels in the hippocampus and there is evidence from zebra finches that estrogens facilitate performance on spatial learning and/or memory tasks. It is unknown, however, whether estrogens influence hippocampal function in songbirds that naturally exhibit memory-intensive behaviors, such as cache recovery observed in many corvid species. To address this question, we examined the impact of estradiol on spatial memory in non-breeding Western scrub-jays, a species that routinely participates in food caching and retrieval in nature and in captivity. We also asked if there were sex differences in performance or responses to estradiol. Utilizing a combination of an aromatase inhibitor, fadrozole, with estradiol implants, we found that while overall cache recovery rates were unaffected by estradiol, several other indices of spatial memory, including searching efficiency and efficiency to retrieve the first item, were impaired in the presence of estradiol. In addition, males and females differed in some performance measures, although these differences appeared to be a consequence of the nature of the task as neither sex consistently out-performed the other. Overall, our data suggest that a sustained estradiol elevation in a food-caching bird impairs some, but not all, aspects of spatial memory on an innate behavioral task, at times in a sex-specific manner.

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

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.

Patterns of phosphorylated tyrosine hydroxylase vary with song production in female starlings.

Vocal signal production in male songbirds is well studied, but the neural correlates of female song production are poorly understood. In European starlings, females sing to defend nesting resources, and song can be considered agonistically motivated. Across vertebrates catecholamines strongly influence motivated, agonistic social behaviors. The present study was designed to provide insight into a possible role for catecholamine activity in territorial song in female starlings. We presented females that were defending nest-cavities with an unfamiliar female and assessed song production. We then measured immunolabeling for phosphorylated tyrosine hydroxylase (pTH-ir), the rate-limiting enzyme for catecholamine synthesis, in brain regions in which catecholamines stimulate agonistic behavior. Females that sang had higher pTH-ir in the caudomedial ventral tegmental area and the lateral septum than females that did not sing. Furthermore, the number of songs produced correlated positively with pTH-ir in the medial preoptic nucleus. Phosphorylation of TH is thought to occur after catecholamine release, so these results link increased catecholamine activity in several brain regions governing agonistic behavior to territorial song production in females.

Patterns of FOS protein induction in singing female starlings.

Females of many songbird species produce song, but information about the neural correlates of singing behavior is limited in this sex. Although well studied in males, activity in premotor song control regions and social behavior regions has not been examined in females during song production. Here, we examined the immediate early gene protein product FOS in both song control and social behavior brain regions after female starlings defending nest boxes responded to an unfamiliar female in a naturalistic setting. We found that females that sang in response to the intruder had much higher numbers of fos-immunoreactive neurons (fos-ir) in the vocal control regions HVC, the robust nucleus of the arcopallium (RA), and the dorsomedial part of the nucleus intercollicularis (DM of the ICo). In HVC, fos-ir correlated positively with song length. In RA, DM and Area X, fos-ir correlated positively with number of songs produced. In social behavior regions, singers showed higher fos-ir in the nucleus taeniae of the amygdala, the dorsal part of the bed nucleus of the stria terminalis, and the ventromedial hypothalamus than non-singers. Overall, patterns of fos-ir in song control regions in females were similar to those reported for males, but differences in fos-ir were identified in social behavior regions. These differences may reflect a distinct role for brain regions involved in social behavior in female song, or they may reflect differences in the social function of female and male song.

Vocal parameters that indicate threat level correlate with FOS immunolabeling in social and vocal control brain regions.

Transmitting information via communicative signals is integral to interacting with conspecifics, and some species achieve this task by varying vocalizations to reflect context. Although signal variation is critical to social interactions, the underlying neural control has not been studied. In response to a predator, black-capped chickadees (Poecile atricapilla) produce mobbing calls (chick-a-dee calls) with various parameters, some of which convey information about the threat stimulus. We predicted that vocal parameters indicative of threat would be associated with distinct patterns of neuronal activity within brain areas involved in social behavior and those involved in the sensorimotor control of vocal production. To test this prediction, we measured the syntax and structural aspects of chick-a-dee call production in response to a hawk model and assessed the protein product of the immediate early gene FOS in brain regions implicated in context-specific vocal and social behavior. These regions include the medial preoptic area (POM) and lateral septum (LS), as well as regions involved in vocal motor control, including the dorsomedial nucleus of the intercollicular complex and the HVC. We found correlations linking call rate (previously demonstrated to reflect threat) to labeling in the POM and LS. Labeling in the HVC correlated with the number of D notes per call, which may also signal threat level. Labeling in the call control region dorsomedial nucleus was associated with the structure of D notes and the overall number of notes, but not call rate or type of notes produced. These results suggest that the POM and LS may influence attributes of vocalizations produced in response to predators and that the brain region implicated in song control, the HVC, also influences call production. Because variation in chick-a-dee call rate indicates predator threat, we speculate that these areas could integrate with motor control regions to imbue mobbing signals with additional information about threat level.

Signaling for food and sex? Begging by reproductive female white-throated magpie-jays.

Food begging is common in nutritionally dependent young of many animals, but structurally homologous calls recur in adult signal repertoires of many species. We propose eight functional hypotheses for begging in adults; these stem from observations in birds but apply broadly to other taxa in which begging occurs. Adult cooperatively-breeding white-throated magpie-jays (Calocitta formosa) use loud begging vocalizations, particularly near the nest site during reproduction. We analysed the social context and behavioural phenology of loud calling and allofeeding in this species and compared these with predictions from each functional hypothesis. We found that reproductive females are the primary producers of beg calls, and their begging peaks during the fertile period when reproductive conflict among males and females was highest. Loud begging rates correlated positively with provisioning rates, but females called more in the pre-incubation fertile period than after they initiated incubation. Based on the context, phenology and active space of the signal, we conclude that female loud begging vocalizations function to signal nutritional need to group members, but also have been evolutionarily co-opted to advertise fertility to potential extra-pair partners. The location of calling is likely a consequence of nest guarding by breeding females to prevent intraspecific brood parasitism.