Bird brains and songs : Neural mechanisms of auditory memory and perception in zebra finches

Abstract

Songbirds, such as zebra finches, learn their songs from a ‘tutor’ (usually the father), early in life. There are strong parallels between the behavioural, cognitive and neural processes that underlie vocal learning in humans and songbirds. In both cases there is a sensitive period for auditory learning, during which the young individuals memorize the vocalizations of adult conspecifics to which they are exposed. After this memorization phase, vocal learning proceeds through a sensorimotor learning phase that is called ‘babbling’ in human infants and ‘subsong' in songbirds. There are homologies between the brains of birds and mammals, which makes the songbird a suitable model organism for studying the neural mechanisms of vocal learning and memory. In songbirds, a network of interconnected nuclei, known as the ‘song system’ is involved in song production and sensorimotor learning. In contrast, it has been suggested that a forebrain region outside the song system, the caudomedial nidopallium (NCM), may contain the neural substrate for the representation of auditory memory acquired in the first phase of song learning. In zebra finches, males learn their vocalisations (calls and songs) while females do not sing, but produce only unlearned calls. Studying the perception of vocalisations in males as well as females may provide clues about how the neural substrate of perception and memory functions in both sexes. This thesis describes three studies investigating the neural mechanisms of auditory memory and perception in zebra finches. First, I have shown that, in adult zebra finch males, the NCM is necessary for recognition of tutor song, but not for song production. In addition, I demonstrated that in juvenile zebra finches the NCM is activated during auditory memory formation. These experiments confirm that the NCM is the likely neural substrate for the representation of tutor song memory. In juvenile male zebra finches, there is neuronal activation in the song system of birds that are singing themselves but not when they are exposed to songs. Thus, in songbirds the cognitive systems underlying vocal production and auditory recognition memory are subserved by distinct brain regions in juveniles as well as adults. These brain regions may functionally interact continually throughout life. Finally, I have shown that the neuronal processing of auditory signals such as the long call appears to differ between males and females. Unravelling the underlying processes related to the perception and memorization of vocalisations that differ between males and females can increase our understanding of how vocalisations are learned. The localization of the neural substrate of tutor song memory presented in this thesis is a necessary prerequisite for the investigation of the neural mechanisms of auditory memory at the molecular and cellular level. The dissociation of brain regions involved in vocal production and in memory in the human as well as in the avian brain, suggests convergent evolution of the mechanisms underlying auditory-vocal learning. Thus, by investigating the neural mechanisms underlying birdsong learning, we may gain important insights into the general mechanisms of auditory-vocal learning.