Layer 6 is the main source of neocortical connections back to specific thalamic nuclei. Corticothalamic (CT) systems play an important role in shaping sensory input, but little is known about the functional circuitry that generates CT activity. We recorded from the two main types of neurons in layer 6, regular-spiking (RS; pyramidal neurons) and fast-spiking (FS; inhibitory interneurons) cells and compared the physiological properties of different excitatory inputs. Thalamic stimulation evoked two monosynaptic inputs with distinct properties: suspected thalamocortical (TC) synaptic events had short latencies, short-term synaptic depression, and paired-pulse responses that suggested subnormal axonal conduction. A second group of synaptic responses likely originated from intracortical collaterals of CT cells that were antidromically activated from the thalamus. These intracortical responses had longer latencies, short-term synaptic facilitation, and were transmitted by axons with supernormal conduction. Suspected TC inputs to FS cells had significantly larger amplitudes than those onto RS cells. Dual recordings from neighboring neurons in layer 6 revealed both facilitating and depressing synaptic connections; the depressing synapses were probably formed by layer 6 cells that do not project to the thalamus, and thus were not sampled by thalamic stimulation. We conclude that layer 6 neurons integrate a variety of inputs with distinct temporal dynamics that are determined by the presynaptic cell type.