Modulation power and phase spectrum of natural sounds enhance neural encoding performed by single auditory neurons

We examined the neural encoding of synthetic and natural sounds by single neurons in the auditory system of male zebra finches by estimating the mutual information in the time-varying mean firing rate of the neuronal response. Using a novel parametric method for estimating mutual information with limited data, we tested the hypothesis that song and song-like synthetic sounds would be preferentially encoded relative to other complex, but non-song-like synthetic sounds. To test this hypothesis, we designed two synthetic stimuli: synthetic songs that matched the power of spectral-temporal modulations but lacked the modulation phase structure of zebra finch song and noise with uniform band-limited spectral-temporal modulations. By defining neural selectivity as relative mutual information, we found that the auditory system of songbirds showed selectivity for song-like sounds. This selectivity increased in a hierarchical manner along ascending processing stages in the auditory system. Midbrain neurons responded with highest information rates and efficiency to synthetic songs and thus were selective for the spectral-temporal modulations of song. Primary forebrain neurons showed increased information to zebra finch song and synthetic song equally over noise stimuli. Secondary forebrain neurons responded with the highest information to zebra finch song relative to other stimuli and thus were selective for its specific modulation phase relationships. We also assessed the relative contribution of three response properties to this selectivity: (1) spiking reliability, (2) rate distribution entropy, and (3) bandwidth. We found that rate distribution and bandwidth but not reliability were responsible for the higher average information rates found for song-like sounds.