| Birdsong learning is a model system for the study of learning of complex behavior. The songbird's brain contains the song system, which is a collection of distinct brain nuclei, which are specialized for song learning and production. Neurons within the song nuclei HVc and robustus archistriatalis (RA) display premotor spiking activity preceding song syllables (components of song). These neurons have been reported to also demonstrate song-selective auditory response properties. We studied behavioral state modulation of RA neuronal properties in the zebra finch (Taeniopygia guttata).; We compared auditory and ongoing activity of RA neurons under anesthesia and in waking and sleeping, unrestrained birds. In waking animals, RA neurons displayed fast, highly regular firing that does not respond to auditory stimulation. After anesthesia or during sleep, the same neurons became slower, irregular, demonstrated complex spontaneous bursting activity, and responded robustly to auditory stimuli. The bursts evident in the spontaneous activity of RA neurons during sleep were found to actually correspond to the individual neurons' motor activity patterns: i.e., RA neurons appear to be attempting to produce song during sleep. Also surprisingly, we found that RA auditory responses during sleep were matched to motor activity—i.e., auditory responses of an RA unit looked like the motor activity of the same unit. Auditory and motor activity were aligned with a small delay (8 ± 2 ms), which is surprising given that there is at least a 70 ms delay between RA premotor activity, the generation of a sound, the perception of that sound, and auditory responses reaching RA. The song system appears to integrate auditory input over tens to hundreds of milliseconds to generate a prediction of the motor activity for future syllables.; On the basis of these observations, we developed a conceptual model of birdsong learning that suggested an important role for sleep in sensorimotor learning. Using concepts developed from the theory of reinforcement learning, we believe that sensory feedback is evaluated during the day, and that the song system may get modified during sleep, using the complex bursting activity observed throughout HVc and RA. |
