Specialized layer 5 cortical terminals target functional thalamic spines

Dendritic spines are ubiquitous morpho-functional elements of excitatory synaptic transmission and plasticity. Whether axo-spinous communication exists in the thalamus is presently unclear. Here we find that layer 5 (L5) corticothalamic terminals arising from frontal cortices selectively target thalamic spines with classical head and neck dimensions. The synapses of the L5 axo-spinous contacts were enriched in GluR1 subunit of AMPA receptor and their size correlated with their spine head volume. Synaptic stimulation of thalamic spines resulted in compartmentalized Ca2+ responses similar to that of hippocampal spines. Optogenetic activation of the frontal L5-thalamus pathway had strong impact on thalamic spiking even at high stimulation frequencies and could selectively recruit a subnetwork of thalamic cells in a behavioral state dependent manner. Optogenetic interference with the small L5-thalamic pathway perturbed motor learning. Our study reveals a hitherto unrecognized, effective top-down communication channel between the frontal cortex and thalamus that involves highly variable axo-spinous contacts