Task-specific invariant representation in auditory cortex

Reviewer #1 (Public Review):

This is a very interesting paper which addresses how auditory cortex represents sound while an animal is performing an auditory task. The study involves psychometric and neurophysiological measurement from ferrets engaged in a challenging tone in noise discrimination task, and relates these measurements using neurometric analysis. A novel neural decoding technique (decoding-based dimensionality reduction or dDR, introduced in a previous paper by two of the authors) is used to reduce bias so that stimulus parameters can be read out from neuronal responses.

The central finding of the study is that, when an animal is engaged in a task, non-primary auditory cortex represents task-relevant sound features in a categorical way. In primary cortex, task engagement also affects representations, but in a different way - the decoding is improved (suggesting that representations have been enhanced), but is not categorical in nature. The authors argue that these results are compatible with a model where early sensory representations form an overcomplete representation of the world, and downstream neurons flexibly read out behaviourally relevant information from these representations.

I find the concept and execution of the study very interesting and elegant. The paper is also commendably clear and readable. The differences between primary and higher cortex are compelling and I am largely convinced by the authors' claim that they have found evidence that broadly supports a mixed selectivity model of neural disentanglement along the lines of Rigotti et al (2013). I think that the increasing body of evidence for these kinds of representations is a significant development in our understanding of higher sensory representations. I also think that the dDR method is likely to be useful to researchers in a variety of fields who are looking to perform similar types of neural decoding analysis.

Reviewer #2 (Public Review):

This study compares the activity of neural populations in the primary and non-primary auditory cortex of ferrets while the animals actively behaved or passively listened to a sound discrimination task. Using a variety of methods, the authors convincingly show differential effects of task engagement on population neural activity in primary vs non-primary auditory cortex; notably that in the primary auditory cortex, task-engagement (1) improves discriminability for both task-relevant and non-task relevant dimensions, and (2) improves the alignment between covariability and sound discrimination axes; whereas in the non-primary auditory cortex, task-engagement (1) improves discriminability for only task-relevant dimensions, and (2) does not affect the alignment between covariability and sound discrimination axes. They additionally show that task-engagement changes in gain can account for the selectivity noted in the discriminability of non-primary auditory neurons. They also admirably attempt to isolate task-engagement from arousal fluctuations, by using fluctuations in pupil size as a proxy for physiological arousal. This is a well-carried out study with thoughtful analyses which in large part achieves its aims to evaluate how task-engagement changes neural activity across multiple auditory regions. As with all work, there are several caveats or areas for future study/analysis. First, the sounds used here (tones, and narrow-band noise) are relatively simple sounds; previous work suggests that exactly what activity is observed within each region (e.g., sensory only, decision-related, etc) may depend in part upon what stimuli are used. Therefore, while the current study adds importantly to the literature, future work may consider the use of more varied stimuli. Second, the animals here were engaged in a behavioral task; but apart from an initial calculation of behavioral d', the task performance (and its effect on neural activity) is largely unaddressed.