Task rule and choice are reflected by layer-specific processing in rodent auditory cortical microcircuits

Marina M Zempeltzi,Frank W Ohl,Max F K Happel,Shivam Maurya,Michael G K Brunk,Matthias Deliano,Martin Kisse,Sümeyra Aksit,Lina Schneider,Claudia Glemser,Katrina E Deane

doi:10.1038/s42003-020-1073-3

Abstract

The primary auditory cortex (A1) is an essential, integrative node that encodes the behavioral relevance of acoustic stimuli, predictions, and auditory-guided decision-making. However, the realization of this integration with respect to the cortical microcircuitry is not well understood. Here, we characterize layer-specific, spatiotemporal synaptic population activity with chronic, laminar current source density analysis in Mongolian gerbils (Meriones unguiculatus) trained in an auditory decision-making Go/NoGo shuttle-box task. We demonstrate that not only sensory but also task- and choice-related information is represented in the mesoscopic neuronal population code of A1. Based on generalized linear-mixed effect models we found a layer-specific and multiplexed representation of the task rule, action selection, and the animal’s behavioral options as accumulating evidence in preparation of correct choices. The findings expand our understanding of how individual layers contribute to the integrative circuit in the sensory cortex in order to code task-relevant information and guide sensory-based decision-making.

Highlights

The primary auditory cortex (A1) is an essential, integrative node that encodes the behavioral relevance of acoustic stimuli, predictions, and auditory-guided decision-making
In the subsequent training phase, the contingency of the 4 kHz pure tone was changed to a “NoGo” stimulus (CS−), while 1 kHz was maintained as conditioned stimuli (CS)+
Animals had to abandon their initially learned strategy and “reassociate” one of the two CS with a new meaning during the discrimination phase. We found that such a switch of the task rule caused the animals to completely abandon the previous but still valuable “knowledge” about parts of the stimulus representation, i.e. the CS which kept the same meaning

Summary

Introduction

The primary auditory cortex (A1) is an essential, integrative node that encodes the behavioral relevance of acoustic stimuli, predictions, and auditory-guided decision-making. Our study thereby revealed that the relative contribution of cortical layers to the canonical columnar response is modulated by task-dependent features such as the behavioral relevance of the stimulus, its particular contingency and required action, as well as direct decision variables and the choice accuracy. This information is represented as accumulating evidence preceding the animal’s choice. This multiplexed information coded by the layer-specific cortical population activity emphasizes the integrative circuit function of the A1 between bottom-up routed task-relevant sound features and top–downcontrolled auditory-guided decision-making

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Conclusion