Auditory Selectivity for Spectral Contrast in Cortical Neurons and Behavior.

Abstract

Vocal communication relies on the ability of listeners to identify, process, and respond to vocal sounds produced by others in complex environments. To accurately recognize these signals, animals' auditory systems must robustly represent acoustic features that distinguish vocal sounds from other environmental sounds. Vocalizations typically have spectral structure; power regularly fluctuates along the frequency axis, creating spectral contrast. Spectral contrast is closely related to harmonicity, which refers to spectral power peaks occurring at integer multiples of a fundamental frequency. Although both spectral contrast and harmonicity typify natural sounds, they may differ in salience for communication behavior and engage distinct neural mechanisms. Therefore, it is important to understand which of these properties of vocal sounds underlie the neural processing and perception of vocalizations.Here, we test the importance of vocalization-typical spectral features in behavioral recognition and neural processing of vocal sounds, using male zebra finches. We show that behavioral responses to natural and synthesized vocalizations rely on the presence of discrete frequency components, but not on harmonic ratios between frequencies. We identify a specific population of neurons in primary auditory cortex that are sensitive to the spectral resolution of vocal sounds. We find that behavioral and neural response selectivity is explained by sensitivity to spectral contrast rather than harmonicity. This selectivity emerges within the cortex; it is absent in the thalamorecipient region and present in the deep output region. Further, deep-region neurons that are contrast-sensitive show distinct temporal responses and selectivity for modulation density compared with unselective neurons.SIGNIFICANCE STATEMENT Auditory coding and perception are critical for vocal communication. Auditory neurons must encode acoustic features that distinguish vocalizations from other sounds in the environment and generate percepts that direct behavior. The acoustic features that drive neural and behavioral selectivity for vocal sounds are unknown, however. Here, we show that vocal response behavior scales with stimulus spectral contrast but not with harmonicity, in songbirds. We identify a distinct population of auditory cortex neurons in which response selectivity parallels behavioral selectivity. This neural response selectivity is explained by sensitivity to spectral contrast rather than to harmonicity. Our findings inform the understanding of how the auditory system encodes socially-relevant signals via detection of an acoustic feature that is ubiquitous in vocalizations.