Song Preference in Female and Juvenile Songbirds: Proximate and Ultimate Questions.

Birdsong has long been a subject of extensive research in the fields of ethology as well as neuroscience. Neural and behavioral mechanisms underlying song acquisition and production in male songbirds are particularly well studied, mainly because birdsong shares some important features with human speech such as critical dependence on vocal learning. However, birdsong, like human speech, primarily functions as communication signals. The mechanisms of song perception and recognition should also be investigated to attain a deeper understanding of the nature of complex vocal signals. Although relatively less attention has been paid to song receivers compared to signalers, recent studies on female songbirds have begun to reveal the neural basis of song preference. Moreover, there are other studies of song preference in juvenile birds which suggest possible functions of preference in social context including the sensory phase of song learning. Understanding the behavioral and neural mechanisms underlying the formation, maintenance, expression, and alteration of such song preference in birds will potentially give insight into the mechanisms of speech communication in humans. To pursue this line of research, however, it is necessary to understand current methodological challenges in defining and measuring song preference. In addition, consideration of ultimate questions can also be important for laboratory researchers in designing experiments and interpreting results. Here we summarize the current understanding of song preference in female and juvenile songbirds in the context of Tinbergen's four questions, incorporating results ranging from ethological field research to the latest neuroscience findings. We also discuss problems and remaining questions in this field and suggest some possible solutions and future directions.

Auditory and sexual preferences for a father's song can co-emerge in female Bengalese finches.

Birdsong is an important communication signal used in mate choice. In some songbird species, only the males produce songs. While the females of those species do not sing, they are sensitive to inter- and intra-species song variations, and the song preferences of females depend on their developmental experiences and/or genetic predispositions. For example, in Bengalese finches and zebra finches, adult females prefer the song to which they were exposed early in life, such as the father's song. In the current study, we aimed to test whether the preference for the father's song, as reported in previous Bengalese finch studies, can be interpreted as a mating preference. For this purpose, the subjects were raised exclusively with their family until they became sexually mature and then tested as adults. We measured copulation solicitation displays during playbacks of the father's song vs. unfamiliar conspecific songs and found that across individuals, the father's song elicited more displays than other songs. In addition, we analyzed if a bird's response to a given song could be predicted by the level of similarity of that song to the father's song. Although the birds expressed more displays to songs with greater similarity to the father's song, the effect was not statistically significant. These results suggest that female Bengalese finches can develop a strong mating preference for the father's song if they are exclusively exposed to the father's song early in life. However, it is not clear if such a preference generalizes to other cases in which birds are exposed to multiple male songs during development. In order to fully elucidate the possible contribution of experience and genetic factors in the development of female song preference in this species, future studies will need more detailed manipulation and control of the rearing conditions, including cross-fostering.

Sex differences in the development and expression of a preference for familiar vocal signals in songbirds.

Production and perception of birdsong critically depends on early developmental experience. In species where singing is a sexually dimorphic trait, early life song experience may affect later behavior differently between sexes. It is known that both male and female songbirds acquire a life-long memory of early song experience, though its function remains unclear. In this study, we hypothesized that male and female birds express a preference for their fathers' song, but do so differently depending on the developmental stage. We measured preference for their father's song over an unfamiliar one in both male and female Bengalese finches at multiple time points across ontogeny, using phonotaxis and vocal response as indices of preference. We found that in males, selective approach to their father's song decreased as they developed while in females, it remained stable regardless of age. This may correspond to a higher sensitivity to tutor song in young males while they are learning and a retained sensitivity in females because song is a courtship signal that is used throughout life. In addition, throughout development, males vocalized less frequently during presentation of their father's song compared to unfamiliar song, whereas females emitted more calls to their father's song. These findings contribute to a deeper understanding of why songbirds acquire and maintain such a robust song memory.

Auditory Responses to Vocal Sounds in the Songbird Nucleus Taeniae of the Amygdala and the Adjacent Arcopallium.

Many species of animals communicate with others through vocalizations. Over time, these species have evolved mechanisms to respond to biologically relevant vocal sounds via adaptive behaviors. Songbirds provide a good opportunity to search for the neural basis of this adaptation, because they interact with others through a variety of vocalizations in complex social relationships. The nucleus taeniae of the amygdala (TnA) is a structure located in the ventromedial arcopallium, which is akin to the mammalian medial amygdala. Studies on the anatomy and function of this nucleus have led to the speculation that the TnA is one of the possible neural substrates that represents the relevance of acoustic stimuli related to behavior. However, neural responses in this nucleus to auditory stimuli have not been studied in depth. To give a detailed description about auditory responses of the TnA in the songbird, we conducted neural recordings from the TnA and the adjacent arcopallium in adult male and female Bengalese finches under anesthesia. The birds were exposed to auditory stimuli including natural vocalizations as well as synthesized noise. We demonstrated that a substantial population of neurons in the TnA and the adjacent arcopallium responded to vocal sounds and that some neurons were selectively activated to specific stimuli. Proportions of responsive cells and stimulus-selective cells were larger in males than in females. In addition, a larger ratio of selective cells was observed in the arcopallium compared to the TnA. These findings support the idea that neuronal activity in the TnA and the neighboring area represents behavioral relevance of sounds. Further studies in electrophysiology combined with evidence from other fields, such as region-specific gene expression patterns, are required to fully understand the functions of the TnA as well as the evolution of the amygdala in songbirds and vertebrate animals.