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Abstract: Songbirds are a great model for studying how the brain solves the challenges of vocal imitation, because, like human infants, young songbirds learn to produce complex vocal sequences that are exact copies of those of adult conspecifics. To study how this feat is accomplished, we experimentally induce birds to perform song learning tasks, by exposing them sequentially to two different songs and recording their entire vocal output during the process. Applying this methodology to vocal combinatorial learning, we trained juvenile zebra finches to swap syllable order in their song, or insert a new syllable into a string. Birds solved these permutation tasks gradually, by a series of steps in which novel pair-wise transitions between syllables were acquired one by one. This effect was confirmed in the development of vocal babbling in human infants, suggesting the existence of a common generative process of acquiring vocal combinatorial ability that is conserved across species.
We next used the same methodology to study the conversion of an auditory memory of a target song into a motor program performing the same song, a long-standing hypothesis in vocal learning. To do this, we induced birds to change both global song structure (syllable order) and its local structure (pitch of individual syllables). We found that birds matched the pitch of syllables to the most acoustically similar target in the tutor song, regardless of global context, resulting in an intermediate-stage song in which the correct syllables were sung in the wrong order. These results refute a sensory-motor learning mechanism where a target song memory is recalled by temporal order, and suggest that instead, parts of the song memory are recalled in a motor driven way, according to their similarity to sung syllables.
Consequently, two distinct mechanisms are required to accomplish the learning of a vocal sequence: 1. Local matching of the acoustic structure of individual units in the sequence; and 2. Global matching of sequence order. Our results present the first experimental evidence of how an internal sensory template is used to guide the development of the motor program for song.