Non-sensory Circuits for Auditory Perceptual Learning

PROJECT SUMMARY
Training can sharpen and refine our perceptual skills. In the auditory system, this process— termed
perceptual learning— shapes the acquisition of both native and non-native languages, and can improve
speech and music recognition in users of assisted listening devices. Previous work has highlighted important
contributions of non-sensory processes (such as attention and reward) to perceptual learning, but the
underlying neural circuit mechanisms remain poorly understood. Recent evidence suggests the involvement of
the orbitofrontal cortex (OFC), a prefrontal cortical region implicated in signaling reward and expectation, and
in exerting top-down control of sensory cortical processing. This project will explore the contribution of the OFC
to auditory perceptual learning in a classic model organism for auditory studies, the Mongolian gerbil. Our
overarching hypothesis, informed by previous and ongoing work, is that training on an auditory task
strengthens a descending projection from the OFC to the auditory cortex, leading to gradual improvements in
auditory cortical sensitivity that underlie perceptual learning. We propose three specific aims to test this
hypothesis. In Aim 1, we use multichannel electrophysiology and pathway-specific fiber photometry to
determine whether training on an auditory task strengthens a descending projection from the OFC to auditory
cortex by increasing presynaptic activity. In Aim 2, we combine pharmacological and optogenetic methods to
determine whether the OFC modulates auditory cortical processing and/or perception in behaving animals via
a descending monosynaptic projection, and reveal whether this capability is enhanced after perceptual
learning. Finally, in Aim 3 we determine whether optogenetic activation of auditory cortical-projecting neurons
in the OFC is sufficient for improving auditory cortical and perceptual sensitivity in behaving animals in the
absence of training. In summary, our experiments combine a powerful array of in vivo tools to dissect the
neural circuit mechanisms that support auditory perceptual learning. The importance of perceptual learning for
improving auditory skills in hearing impaired listeners, and the disruption of perceptual learning in individuals
with neurodevelopmental disorders, like dyslexia and autism, highlight an urgent need for a more complete
description of how perceptual learning is implemented in the brain.

Grant Number: 5R01DC020742-04
NIH Institute/Center: NIH
Principal Investigator: Melissa Caras