Synthetic stimuli reveal a predictive and switch-like activation of the songbird’s vocal motor program

Acquisition and maintenance of complex vocal behaviors like human speech and oscine birdsong require continuous auditory feedback. The exact way in which this feedback is integrated into the vocal motor programs is not completely understood. Here we show that in sleeping zebra finches ( Taeniopygia guttata ), the activity of the song system selectively evoked by playbacks of their own song can be detected in the syrinx. Measuring the electrical activity of syringeal muscles, we found playback-evoked patterns identical to those recorded during song execution. Using this global and continuous readout we studied the activation dynamics of the song system elicited by different auditory stimuli. We found that a synthetic version of the bird’s song, rendered by a physical model of the avian phonation apparatus, evoked exactly the same response, albeit with lower efficiency. Analysis of these responses reveal a predictive and switch-like activation of the motor program, with preferred activation instants within the song. Significance The study of the integration between sensory inputs and motor commands has greatly benefited from the finding that in sleeping oscine birds, playback of their own song evokes highly specific firing patterns in neurons also involved in the production of that song. Nevertheless, the sparse spiking patterns that can be recorded from few single neurons gives limited information of the overall activity of the song system. Here we show that this response is not limited to the central nervous system, but reaches vocal muscles. Combining this integrated measure of the activity of the system with surrogate synthetic songs, we found an all-or-nothing and predictive activation of the system, suggesting the existence of a pre-programmed internal dynamics.