Emergence and function of cortical offset responses in sound termination detection
Curation statements for this article:-
Curated by eLife
Evaluation Summary:
There has been a great deal of recent interest in the neural basis for offset responses given their hypothesised importance to perception. This tests the relevance of offset responses to duration perception in a mouse model in addition to examining the brain basis. The work is thorough and well executed. The work demonstrates offset responses that occurs for the first time in auditory cortex distinct from A1 where prevention of offsets by activating cells causes worsening of behavioural performance.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.)
This article has been Reviewed by the following groups
Discuss this preprint
Start a discussion What are Sciety discussions?Listed in
- Evaluated articles (eLife)
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.
Article activity feed
-
Evaluation Summary:
There has been a great deal of recent interest in the neural basis for offset responses given their hypothesised importance to perception. This tests the relevance of offset responses to duration perception in a mouse model in addition to examining the brain basis. The work is thorough and well executed. The work demonstrates offset responses that occurs for the first time in auditory cortex distinct from A1 where prevention of offsets by activating cells causes worsening of behavioural performance.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.)
-
Reviewer #1 (Public Review):
There has been a great deal of recent interest in the neural basis for offset responses given their hypothesised importance to perception. The possible behavioural relevance to cues like sound duration and gap duration has been taken as a self-evident truth in some work. I found this work attractive in actually testing the relevance of offset responses to duration perception in a mouse model in addition to examining the brain basis. The work is thorough and well executed. The work demonstrates offset responses that occurs for the first time in auditory cortex distinct from A1 where prevention of offsets by activating cells causes worsening of behavioural performance.
-
Reviewer #2 (Public Review):
In this study, the authors examine: 1) whether offset responses, where neurons respond upon termination of a stimulus, are behaviorally relevant; 2) whether offset responses are merely inherited from subcortical stations or are generated and amplified in cortex; and 3) whether offset responses simply encode sound termination or if they carry stimulus identity information as well. They show, using a combination of optogenetics and behavior, that suppressing offset responses in auditory field AAF results in an impairment of sound termination detection. They then show, using single- and multi-unit recordings, that the behavioral choice of the animal can be decoded on a trial-by-trial basis from the offset and late response phases. Finally, using antidromic stimulation and using multiple stimuli, the authors …
Reviewer #2 (Public Review):
In this study, the authors examine: 1) whether offset responses, where neurons respond upon termination of a stimulus, are behaviorally relevant; 2) whether offset responses are merely inherited from subcortical stations or are generated and amplified in cortex; and 3) whether offset responses simply encode sound termination or if they carry stimulus identity information as well. They show, using a combination of optogenetics and behavior, that suppressing offset responses in auditory field AAF results in an impairment of sound termination detection. They then show, using single- and multi-unit recordings, that the behavioral choice of the animal can be decoded on a trial-by-trial basis from the offset and late response phases. Finally, using antidromic stimulation and using multiple stimuli, the authors show that AAF offset responses are not wholly inherited from the auditory thalamus.
The electrophysiological elements of the study seem solid and well-performed. Some weaknesses of the study include the effectiveness of task acquisition by the behavioral subjects, and behavioral analyses that discard trials with potentially useful information. Some statistical tests may not be appropriate and brings into question the results of the decoding analysis. Very recent and highly relevant publications are not discussed in the study. Additional control analyses would strengthen the manuscript.
-
Reviewer #3 (Public Review):
The paper represents an innovative and comprehensive body of work aimed to assess the function of cortical offset responses in the anterior auditory field (SSF) in sound perception. Whereas the majority of work to date in auditory neuroscience has focused on the sound onset responses (largely due to the quick adaptation of cortical responses), the offset responses, which are present in the cortex, and especially, as the authors show, in AAF, have received less attention. The offset responses can play an important role in sound segregation and auditory scene analysis. The authors used a combination of behavioral, electrophysiological and optogenetic techniques to study the properties of cortical offset responses. The authors first test whether and how offset responses correlate and affect behavioral detection …
Reviewer #3 (Public Review):
The paper represents an innovative and comprehensive body of work aimed to assess the function of cortical offset responses in the anterior auditory field (SSF) in sound perception. Whereas the majority of work to date in auditory neuroscience has focused on the sound onset responses (largely due to the quick adaptation of cortical responses), the offset responses, which are present in the cortex, and especially, as the authors show, in AAF, have received less attention. The offset responses can play an important role in sound segregation and auditory scene analysis. The authors used a combination of behavioral, electrophysiological and optogenetic techniques to study the properties of cortical offset responses. The authors first test whether and how offset responses correlate and affect behavioral detection of sound offsets. They find that suppressing offset responses in AAF reduces the responses of mice to sound offsets and that there is a significant correlation between cortical responses and behavioral report. The authors next use elegant electrophysiological and manipulation methods to find that cortical offset responses have a component that is generated in the AAF and therefore not only inherited from the periphery. The authors also find that offset responses increase with sounds that have longer duration and therefore do not simply encode for silence. Such an extensive description of these types of responses provides for an advance in our understanding of cortical function in audition.
-
-
