Sensory Constraints on Birdsong Syntax: Neural Responses to Swamp Sparrow Songs with Accelerated Trill Rates

Both sensory and motor mechanisms can constrain behavioral performance. Sensory mechanisms may be especially important for constraining behaviors that depend on experience, such as learned birdsongs. Swamp sparrows learn to sing by imitating the song of a tutor, but sparrows fail to accurately imitate artificial tutor songs with abnormally accelerated trills, instead singing brief and rapid trills interrupted by silent gaps. This "broken syntax" has been proposed to arise from vocal-motor limitations. Here we consider whether sensory limitations exist that could also contribute to broken syntax. We tested this idea by recording auditory-evoked activity of sensorimotor neurons in the swamp sparrow's brain that are known to be important for the learning, performance and perception of song. In freely behaving adult sparrows that sang songs with normal syntax, neurons were detected that exhibited precisely time-locked activity to each repetition of the syllable in a trill when presented at a natural rate. Those cells failed to faithfully follow syllables presented at an accelerated rate, however, and their failure to respond to consecutive syllables increased as a function of trill rate. This "flickering" auditory representation in animals performing normal syntax reveals a central constraint on the sensory processing of rapid trills. Furthermore, because these neurons are implicated in both song learning and perception, and because auditory flickering began to occur at accelerated trill rates previously associated with the emergence of broken song syntax, these sensory constraints may contribute to the emergence of broken syntax.