Distinct frontal cortical pathways for the long-range processing of auditory and visual stimuli

Abstract

Frontal cortex neurons are sensory responsive and send long-range feedback to multiple different sensory cortices, but whether these functions are carried out by the same neurons or by distinct modality-specific circuits remains unknown. Using large-scale electrophysiology, two-photon calcium imaging, and viral circuit tracing in awake mice, we identify rich, modality-specific sensory coding in the frontal cortex (secondary motor/anterior cingulate cortex) that is largely dissociated from the neurons providing feedback to sensory cortex. Frontal cortex neurons exhibited robust sensory-evoked activity, with response magnitudes, latencies, and feature selectivity comparable to those observed in primary sensory cortex. Individual neurons displayed tuning for distinct sensory modalities, while population-level activity reliably decoded both sensory modality and stimulus identity. Anatomically, primary auditory (A1) and visual (V1) cortex axons were largely intermingled in anterior frontal cortex but more segregated in posterior regions, revealing spatial variation in the integration of sensory inputs. Frontal cortex neurons responsive to auditory stimuli were biased more anterior compared to visually-responsive neurons. Dual retrograde tracing identified distinct frontal cortex populations projecting back to A1 and V1 that were biased to the posterior and medial extent of the frontal cortex. A1- and V1-projecting frontal neurons were minimally sensory responsive, and no more likely to be responsive than other frontal neurons. Together, these findings reveal a division of labor within the frontal cortex, in which detailed sensory representations and corticocortical feedback arise from partially distinct neuronal populations. This circuit architecture provides a means through which specific sensory information can be transformed within the frontal cortex before being communicated back to the sensory cortex according to behavioral demands.