Thalamic ventrobasal (VB) relay neurons receive information via two major types of glutamatergic synapses, that is, from the medial lemniscus (lemniscal synapses) and primary somatosensory cortex (corticothalamic synapses). These two synapses influence and coordinate firing responses of VB neurons, but their precise operational mechanisms are not yet well understood. In this study, we compared the composition of glutamate receptors and synaptic properties of corticothalamic and lemniscal synapses. We found that the relative contribution of NMDA receptor-mediated excitatory postsynaptic currents (EPSCs) to non-NMDA receptor-mediated EPSCs was significantly greater in corticothalamic synapses than in lemniscal synapses. Furthermore, NMDA receptor 2B-containing NMDA receptor- and kainate receptor-mediated currents were observed only in corticothalamic synapses, but not in lemniscal synapses. EPSCs in corticothalamic synapses displayed the postsynaptic summation in a frequency-dependent manner, in which the summation of the NMDA receptor-mediated component was largely involved. The summation of kainate receptor-mediated currents also partially contributed to the postsynaptic summation in corticothalamic synapses. In contrast, the contribution of NMDA receptor-mediated currents to the postsynaptic summation of lemniscal EPSCs was relatively minor. Furthermore, our results indicated that the prominent NMDA receptor-mediated component in corticothalamic synapses was the key determinant for the late-persistent firing of VB neurons in response to corticothalamic stimuli. In lemniscal synapses, in contrast, the onset-transient firing in response to lemniscal stimuli was regulated mainly by AMPA receptors.