Experience-dependent coding of time-dependent frequency trajectories by off responses in secondary auditory cortex

• Type of Material: Article
• Authors: Kelly K. Chong, Emory University; Dakshitha B. Anandakumar, Emory University; Alex G. Dunlap, Emory University; Dorottya Kacsoh, Emory University; Robert Liu, Emory University
• Language: English
• Date: 2020-06-03
• Publisher: Society for Neuroscience
• Publication Version: Final Published Version
• Copyright Statement: © 2020 Chong et al.
• License: Creative Commons Attribution 4.0 International
• Final Published Version (URL): http://dx.doi.org/10.1523/JNEUROSCI.2665-19.2020
• Title of Journal or Parent Work: The Journal of Neuroscience
• Volume: 40
• Issue: 23
• Start Page: 4469
• End Page: 4482
• Grant/Funding Information: This work was supported by the National Institutes of Health Grants R01-DC-8343 to R.C.L. and T32-HD-071845 to K.K.C.
• Keywords: Pitch Perception; pitch; Random Allocation; Acoustic Stimulation; USV; Female; Reaction Time; Mice, Inbred CBA; Action Potentials; maternal behavior; Electrodes, Implanted; Animals; Mice; offset response; Auditory Cortex; belt; secondary auditory cortex; Age Factors
• Research Categories: Biology, Bioinformatics; Engineering, Biomedical; Biology, Neuroscience

Abstract

Time-dependent frequency trajectories are an inherent feature of many behaviorally relevant sounds, such as species-specific vocalizations. Dynamic frequency trajectories, even in short sounds, often convey meaningful information, which may be used to differentiate sound categories. However, it is not clear what and where neural responses in the auditory cortical pathway are critical for conveying information about behaviorally relevant frequency trajectories, and how these responses change with experience. Here, we uncover tuning to subtle variations in frequency trajectories in auditory cortex of female mice. We found that auditory cortical responses could be modulated by variations in a pure tone trajectory as small as 1/24th of an octave, comparable to what has been reported in primates. In particular, late spiking after the end of a sound stimulus was more often sensitive to the sound's subtle frequency variation compared to spiking during the sound. Such “Off” responses in the adult A2, but not those in core auditory cortex, were plastic in a way that may enhance the representation of a newly acquired, behaviorally relevant sound category. We illustrate this with the maternal mouse paradigm for natural vocalization learning. By using an ethologically inspired paradigm to drive auditory responses in higher-order neurons, our results demonstrate that mouse auditory cortex can track fine frequency changes, which allows A2 Off responses in particular to better respond to pitch trajectories that distinguish behaviorally relevant, natural sound categories.