Neurobiology of song learning and perception in the zebra finch (Taeniopygia guttata), with a focus on the role of the hippocampus

Songbirds have become one of the most widely used model systems for the examination of neural processes underlying learning and memory. Zebra finch (Taeniopygia guttata) song is highly sexually dimorphic in that only males produce the behavior, yet perception of these vocalizations is critical to the reproductive success of both sexes. Males need to hear the vocalizations of a male tutor and, later, their own vocalizations in order to learn and develop song, but it is debatable whether experience plays a role in the development of song perception or preference in females. Vocal behavior in males is regulated by a system of interconnected nuclei that undergo dramatic morphological changes during development. However, other forebrain areas that ultimately receive input from the auditory thalamus show differential neuronal activity following conspecific or heterospecific song presentations in both sexes, suggesting that they are more important for the perception or perhaps neural storage of song. The hippocampus is also activated following playback of conspecific songs, suggesting that this area, traditionally associated with spatial memory, might play a role in song-related behavior. The present experiments began to test the role of early auditory experience in the development of female song perceptions, the development of neural responses to song in auditory regions and the hippocampus, the afferent connectivity of the hippocampal formation, and whether destruction of hippocampal tissue affects the consolidation or David J. Bailey retrieval of song templates or normal preferences for particular songs. These experiments show that (1) female zebra finches isolated from song but not biparental care during development respond like birds raised normally during conspecific song presentations but are initially limited in their ability to associate a novel environment with relevant song; (2) early in development, the sexes display different patterns of immediate early genes that may encode information about auditory stimuli but, over time, these responses become sexually monomorphic and likely remain that way in adulthood; (3) together with prior data indicating the efferent connectivity of the hippocampus, projections to the region indicate connections (some reciprocal) with nuclei involved in song behavior and suggest a role for the region in responses to vocal communications signals or auditory-related memories in the zebra finch as well as homology with the mammalian hippocampus; and (4) relatively small lesions of the hippocampus in males and females before the period song is learned, when it begins to be practiced (at least by males), or in adulthood have no effect on song preferences in males and females or song production in males, but do influence memory for a particular location. Taken together, these results indicate that the hippocampus, although not involved in song learning directly, may be integral in the consolidation of memories relating to song or the modulation of responses of other regions based on the salience of particular vocal signals or environments in which they are heard or produced.