Neural Mechanisms of Auditory Pattern Processing and Pattern Learning in Songbirds

Temporal sequence is a rich and essential component of information in vocalizations of animals and humans. As part of a larger effort to characterize nonlinear receptive field properties of higher-order auditory neurons we have been studying sensitivity of starlings to sequences of naturally-occurring "motifs". After achieving baseline performance on a go/nogo task that contrasted sets of strings drawn from finite-state and context-free grammars (CFG), birds were transferred to novel sets of strings of the same order, and probed with higher-order grammatical strings and agrammatical strings. The results indicate that birds learned a simple CFG, a level of perceptual syntactic complexity which has previously been posited to be uniquely available to humans. Starlings performed equally well on strings of human syllables whereas humans easily solved the problem when exposed to strings of syllables but struggled with strings of starling motifs. Specific learning exposure greatly facilitated human performance. These results emphasize the importance of species specificity in all animal behavior including language and challenge dogma that places language outside the realm of biological experimentation. Higher-order neurons in the starling auditory system respond electively to motifs depending on learning and eward contingencies. Although we know little yet regarding temporal sequence sensitivity of these neurons, such analysis is likely to provide mechanistic insight into complex pattern perception in birds, which may constrain theories of the evolution of such behaviors.