Emergence and function of cortical offset responses in sound termination detection.

Magdalena Solyga,Tania Rinaldi Barkat

doi:10.7554/elife.72240

Abstract

Offset responses in auditory processing appear after a sound terminates. They arise in neuronal circuits within the peripheral auditory system, but their role in the central auditory system remains unknown. Here, we ask what the behavioral relevance of cortical offset responses is and what circuit mechanisms drive them. At the perceptual level, our results reveal that experimentally minimizing auditory cortical offset responses decreases the mouse performance to detect sound termination, assigning a behavioral role to offset responses. By combining in vivo electrophysiology in the auditory cortex and thalamus of awake mice, we also demonstrate that cortical offset responses are not only inherited from the periphery but also amplified and generated de novo. Finally, we show that offset responses code more than silence, including relevant changes in sound trajectories. Together, our results reveal the importance of cortical offset responses in encoding sound termination and detecting changes within temporally discontinuous sounds crucial for speech and vocalization.

Highlights

To assess the behavioral relevance of auditory offset responses, we developed a sound termination detection task in which mice expressing channelrhodopsin-2 (ChR2) in parvalbumin-p ositive (PV+) cells learned to detect the end of 9 kHz pure tones (PT; Figure 1a)
As the auditory system very robustly represents timing information, it is a model of choice to study neural offset responses evoked by the disappearance of a stimulus
We show that minimizing anterior auditory field (AAF) offset responses decreases the mouse performance to detect sound termination, revealing their importance at the behavioral level

Summary

Introduction

Offset-responsive neurons are present through the whole auditory pathway starting from the cochlear nucleus (CN; Ding et al, 1999; Suga, 1964; Young and Brownell, 1976) to the superior paraolivary nucleus (SPN; Dehmel et al, 2002; Kulesza et al, 2003), the inferior colliculus (IC; Akimov et al, 2017; Kasai et al, 2012), the medial geniculate body (MGB; Anderson and Linden, 2016; He, 2001; He, 2002; Yu et al, 2004), and the auditory cortex (ACx; Qin et al, 2007; Recanzone, 2000; Scholl et al, 2010; Takahashi et al, 2004). Offset responses in MGB and the ACx are generally thought to be driven by excitatory/inhibitory inputs from IC rather than by other neural mechanisms (Kopp-S cheinpflug et al, 2018). The amplitude, duration, frequency, fall-time, and spectral complexity of the sound have all been reported to influence auditory offset responses (He, 2002; Scholl et al, 2010; Sołyga and Barkat, 2019; Takahashi et al, 2004). By studying the influence of different sound parameters on AAF and MGB offset responses, we demonstrate that cortical offsets are inherited, amplified, and sometimes even generated de novo. Our findings suggest a particular involvement of AAF offset responses in sound termination processing and point to the importance of this cortical subfield for advanced processing such as tracking sound duration or detecting changes in frequency and level within temporally discontinuous sounds

Results

Discussion

Materials and methods

Surgical procedures

Funding Funder