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

The primary auditory cortex (A1) is an essential node in the integrative brain network that encodes the behavioral relevance of acoustic stimuli, predictions, and auditory-guided decision making. Previous studies have revealed task-related information being present at both the single-unit and population activity. However, its realization with respect to the cortical microcircuitry is less well understood. In this study, we used chronic, laminar current source density (CSD) analysis from the A1 of behaving Mongolian gerbils (Meriones unguiculatus) in order to characterize layer-specific, spatiotemporal synaptic population activity. Animals were trained to first detect and subsequently to discriminate two pure tone frequencies in consecutive training phases in a 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 distributed across cortical layers. Based on a single-trial analysis using generalized linear-mixed effect models (GLMM), we found infragranular layers to be involved in auditory-guided action initiation during tone detection. Supragranular layers, particularly, are involved in the coding of choice options during tone discrimination. Further, we found that the overall columnar synaptic network activity represents the accuracy of the opted choice. Our study thereby suggests a multiplexed representation of stimulus features in dependence of the task, action selection, and the behavioral options of the animal in preparation of correct choices. The findings expand our understanding of how individual layers contribute to the integrative circuit of the A1 in order to code task-relevant information and guide sensory-based decision making.