Top-down corticothalamic layer 5 afferents (L5) have profound impact on the activity of their thalamic targets. However, L5 afferents were mainly studied in sensory corticothalamic circuits. In this project we asked whether the characteristics of L5 corticothalamic inputs in sensory and frontal cortical regions have similar properties. We found that L5-thalamus pathways display regional specificity. Sensory L5-thalamic axons establish giant terminals, as described, but the frontal L5-thalamic boutons are small, their size distribution is closer to that of the L6 boutons. Small L5 terminals are as effective in driving thalamic spiking as large L5 terminals in vivo and displayed less short-term depression in vitro and in vivo. Despite their similarity in size, the ultrastructural properties of small L5 terminals are distinct from that of the small L6 terminals. Small, frontal L5 boutons target dendritic spines with similar ultrastructural characteristics to the spines of cortical pyramidal cells. In vitro two photon glutamate uncaging demonstrated that glutamate evoked Ca2+ transients in thalamic spines are compartmentalized similar to CA1 hippocampal pyramidal cell spines. Synapses formed by small L5 are enriched in GLUR1 AMPA receptor subunit. Optogenetic inhibition of small L5 terminals from the secondary motor cortex in the thalamic ventromedial nucleus affected the improvement of the motor performance of mice in a horizontal wheel running learning experiment.We conclude that the presence of functional spines on thalamic dendrites with a specialized cortical input can potentially endow thalamocortical cells with the ability of scaling and plastic regulation of incoming cortical inputs.