Although the mechanisms by which the cerebral cortex controls its ascending input are still poorly understood, it is known that cortical control at the thalamic level is via direct glutamatergic projections to relay nuclei and to the reticular nucleus. Here we confirm previous light microscopic reports of a high expression of the alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor subunit, GluR4, in reticular and ventral posterior thalamic nuclei of the rat, and moderate staining using an antibody recognizing both GluR2 and GluR3. In contrast only low levels of staining for GluR2, and barely detectable levels of GluR1 immunoreactivity were observed. After injections of biotinylated dextran, electron microscopy revealed that anterogradely-labeled cortical synapses in both thalamic nuclei were small with fewer mitochondria and more densely-packed vesicles than terminals likely to arise from intrinsic and ascending pathways. We performed post-embedding immunogold to provide quantitative data on the density of AMPA receptor subunits at morphologically-defined groups of synapses. We found that corticothalamic synapses in the reticular thalamic nucleus contain twice as much GluR2/3, and at least three times more GluR4 protein than do intrathalamic synapses. In the ventral posterior nucleus, corticothalamic synapses contain similar amounts of GluR2/3, but four times more GluR4 than do those from ascending afferents. Corticothalamic synapses in reticular nucleus contain slightly more GluR2/3, and three times more GluR4, than those in ventral posterior nucleus. We conclude that enrichment of GluR4 at morphologically-defined cortical synapses is a feature common to both thalamic nuclei, and those in the reticular nucleus express higher levels of AMPA receptors. The rapid kinetics of GluR4-rich AMPA receptors we suggest indicate that cortical descending control may be more temporally precise than previously recognized.