A novel architecture of PT neuron-based corticothalamic connectivity in the auditory system

Abstract

Largely topographical projections from different modules of the thalamus, such as the primary, secondary and association sensory thalamus, to hierarchically defined cortical areas have been recognized across sensory systems. However, how corticothalamic projections, which are believed to be crucial for the remarkable flexibility and precision exhibited by our sensory systems, are organized remained poorly understood compared with the thalamocortical counterpart. Here we report that, first, the primary auditory thalamus received direct inputs from cortical L5 neurons. Second, in contrast to the robust thalamocortical topography, L5 neurons in each of the primary, secondary and association auditory cortical regions project to each individual module of the auditory thalamus at the macroscale. Third, the association cortex provided the most L5 inputs to all thalamic modules followed by the secondary and primary auditory cortices. Lastly, L5 axon terminals were mainly varicosity-type and evenly distributed across thalamic modules, but those in the polymodal association module were the largest. Our data suggest that all the modules of the auditory thalamus may be under the modulation of common L5 inputs. This fully-connected-like corticothalamic architecture urges a revision of the traditional hierarchical model in the sensory systems.