A Sensorimotor Pathway via Higher-Order Thalamus

<jats:p>We now know that sensory processing in cortex occurs not only via direct communication between primary to secondary areas, but also via their parallel cortico-thalamo-cortical (i.e.,<jats:italic>trans</jats:italic>-thalamic) pathways. Both corticocortical and<jats:italic>trans</jats:italic>-thalamic pathways mainly signal through glutamatergic class 1 (driver) synapses, which have robust and efficient synaptic dynamics suited for the transfer of information such as receptive field properties, suggesting the importance of class 1 synapses in feedforward, hierarchical processing. However, such a parallel arrangement has only been identified in sensory cortical areas: visual, somatosensory, and auditory. To test the generality of<jats:italic>trans</jats:italic>-thalamic pathways, we sought to establish its presence beyond purely sensory cortices to determine whether there is a<jats:italic>trans</jats:italic>-thalamic pathway parallel to the established primary somatosensory (S1) to primary motor (M1) pathway. We used<jats:italic>trans</jats:italic>-synaptic viral tracing, optogenetics in slice preparations, and bouton size analysis in the mouse (both sexes) to document that a circuit exists from layer 5 of S1 through the posterior medial nucleus of the thalamus to M1 with glutamatergic class 1 properties. This represents a hitherto unknown, robust sensorimotor linkage and suggests that the arrangement of parallel direct and<jats:italic>trans</jats:italic>-thalamic corticocortical circuits may be present as a general feature of cortical functioning.</jats:p><jats:p><jats:bold>SIGNIFICANCE STATEMENT</jats:bold>During sensory processing, feedforward pathways carry information such as receptive field properties via glutamatergic class 1 synapses, which have robust and efficient synaptic dynamics. As expected, class 1 synapses subserve the feedforward projection from primary to secondary sensory cortex, but also a route through specific higher-order thalamic nuclei, creating a parallel feedforward<jats:italic>trans</jats:italic>-thalamic pathway. We now extend the concept of cortical areas being connected via parallel, direct, and<jats:italic>trans</jats:italic>-thalamic circuits from purely sensory cortices to a sensorimotor cortical circuit (i.e., primary sensory cortex to primary motor cortex). This suggests a generalized arrangement for corticocortical communication.</jats:p>