A parallel tonotopically arranged thalamocortical circuit for sound processing

The perception of the sensory world in mammals requires information flow from the thalamus to the cortex. Although the first-order sensory thalamus and its surrounding nuclei are considered the major hub for feedforward thalamocortical transmission, it remains unknown whether any other thalamic input could also contribute to this transmission. We found a thalamic region, the basal region of the ventromedial nucleus of the thalamus (bVM), that sends dense, tonotopically arranged projections to auditory cortex (AuC) fields. Silencing these AuC-projecting neurons severely impaired the mouse's ability to discriminate sound frequencies. These projections exhibited strong frequency-tuning preferences that matched the cortical tonotopic map. Moreover, bVM inputs were excitatory and primarily terminated on neuron-derived neurotrophic factor-positive interneurons in cortical layer 1. Silencing these inputs significantly reduced sound-evoked responses of AuC neurons. Our results reveal a non-canonical, tonotopically arranged thalamic input to cortical layer 1 that contributes to sound processing, in parallel to the classic auditory thalamocortical pathway.