Feedback Learning in a Sensorimotor System

Sensory feedback plays a critical role in learning of highly complex motor skills. Maintenance of learned motor skills requires constant monitoring and recalibration for the nervous system to cope with changes in motor organs (such as fatigue, damage or development), and changes in the nervous system itself. Human speech and birdsong are remarkable examples of motor learning that result in exquisite motor control of vocal organs. Auditory feedback is essential to development and maintenance of learned vocalizations, but the mechanism whereby feedback influences learning is not well understood. Here we sought behavioral and physiological constraint on the action of sensory feedback by examining vocal learning in a songbird. To characterize properties of auditory feedback in song learning, we first investigated song development with continuous time delayed auditory feedback in juvenile zebra finches. To avoid positive feedback under conditions of high gain, we developed a computerized system to implement real-time echo cancellation. Under delayed auditory feedback, birds were able to develop songs composed of abnormally long silent intervals between the syllables. This change is adaptive in that it avoids overlap between the bird's vocalization and delayed auditory feedback from the speaker, but results in learning abnormal syntax and syllable morphology. This suggests that songbirds may detect the self-generated sound with a cue other than the timing of the auditory feedback for song development. Humans perceive self-generated speech differently from playback of recorded speech mainly because low frequency power is transmitted principally via bone conduction to the middle ear, and this component is missing in playback. In songbirds, previous studies indicate that low frequency components of auditory feedback may be particularly salient cues for song learning and maintenance. Since neurons of the avian forebrain nuclei exhibit selective auditory response to the bird's own song (BOS) under sleep or anesthesia, we examined auditory responses in urethane-anesthetized adult zebra finches to broadcasted BOS and its low frequency amplified version. By recording from two forebrain nuclei of the song system, the sensorimotor nucleus HVC and the basal ganglia nucleus Area X, we demonstrated that the mean firing rates and/or temporal structure of spike trains are sensitive to the relative power of low frequencies in the bird's own song. To directly examine the potential behavioral role of low frequencies in singing behavior, we examined the bone conduction signal recorded from singing zebra finches using a piezoelectric accelerometer. This signal resulted in clean song recording and included relatively higher power at the low frequencies where the song system neurons are sensitive. We also applied accelerometer recordings of bone conduction sounds to produce continuous delayed auditory feedback in adult zebra finches. As the accelerometer is relatively insensitive to airborne sound, the system could achieve greater gain (louder delayed auditory feedback), without contaminating the song recordings, than with echo cancellation. Under these conditions, adult zebra finches exhibited dramatic abnormal syllable sequencing including repetition of individual syllables reminiscent of stuttering in humans. These effects were observed starting within one week of delayed auditory feedback exposure. Such a marked change in song syntax within a week has not been reported in any other manipulation of auditory feedback in adult zebra finches. We also perturbed auditory feedback with frequency shifting. This allows us to probe a bird's ability to change...