Conserved mechanisms of vocalization coding in mammalian and songbird auditory midbrain

Abstract

The ubiquity of social vocalization among animals provides the opportunity to identify conserved mechanisms of auditory processing that subserve vocal communication. Identifying auditory coding properties that are shared across vocal communicators will provide insight into how human auditory processing leads to speech perception. Here, we compare auditory response properties and neural coding of social vocalizations in auditory midbrain neurons of mammalian and avian vocal communicators. The auditory midbrain is a nexus of auditory processing because it receives and integrates information from multiple parallel pathways and provides the ascending auditory input to the thalamus. The auditory midbrain is also the first region in the ascending auditory system where neurons show complex tuning properties that are correlated with the acoustics of social vocalizations. Single unit studies in mice, bats and zebra finches reveal shared principles of auditory coding including tonotopy, excitatory and inhibitory interactions that shape responses to vocal signals, nonlinear response properties that are important for auditory coding of social vocalizations and modulation tuning. Additionally, single neuron responses in the mouse and songbird midbrain are reliable, selective for specific syllables, and rely on spike timing for neural discrimination of distinct vocalizations. We propose that future research on auditory coding of vocalizations in mouse and songbird midbrain neurons adopt similar experimental and analytical approaches so that conserved principles of vocalization coding may be distinguished from those that are specialized for each species.

Midbrain Synchrony to Envelope Structure Supports Behavioral Sensitivity to Single-Formant Vowel-Like Sounds in Noise

“…The ability of these models to predict IC responses in the budgerigar highlights an emerging pattern of broad similarities in auditory function between birds and mammals up to at least the level of the auditory midbrain (Ryugo and Parks 2003;Woolley and Portfors 2013). While birds and mammals exhibit differences in the anatomy of the cochlea related to extension of the upper frequency limit of hearing in mammals (Manley 2010), auditory nerve fibers in both groups show similar ranges of spontaneous activity, minimum thresholds for tone stimuli, frequency tuning bandwidth as a function of BF, and dynamic range/rate saturation (Sachs et al 1974;Manley et al 1985).…”

BOLD fMRI study of ultrahigh frequency encoding in the inferior colliculus

“…If only the combination or distortion were encoded, neurons might not accurately differentiate UHFs from lower frequencies. Such complexity may have been developed by animals while they evolved to emit UHF vocalizations to avoid predation, such that auditory neurons originally tuned to lower frequencies can encode their vocalizations with high efficiency and fidelity (Woolley and Portfors, 2013). The combination of different mechanisms also emphasized a critical role of the IC in processing UHF related sounds.…”

Seasonal Plasticity of Precise Spike Timing in the Avian Auditory System

“…Despite decades of work establishing the importance of precise spike timing in the auditory nerve (Kiang, 1965;Rose et al, 1967;Young and Sachs, 1979), the role of temporal coding has only recently been explored in more central regions: midbrain (Holmstrom et al, 2010;Woolley and Portfors, 2013), thalamus (Huetz et al, 2009), and forebrain (Narayan et al, 2006;Schnupp et al, 2006;Engineer et al, 2008;Kayser et al, 2010).…”