Intrinsic properties, morphology, and local network circuitry of identified layer 5 and layer 6 auditory corticothalamic neurons were compared. We injected fluorescent microspheres into the mouse auditory thalamus to prelabel corticothalamic neurons, then recorded and filled labeled layer 5 or layer 6 auditory cortical neurons in vitro. We observed low-threshold bursting in adult, but not juvenile, layer 5 corticothalamic neurons that was voltage and time dependent with nonlinear input-output properties, whereas adult layer 6 corticothalamic neurons demonstrated a regular spiking. Layer 5 corticothalamic neurons had larger somata, thicker apical dendrites and were more likely to have a layer 1 apical dendrite than layer 6 neurons. Using laser photostimulation, identified layer 5 corticothalamic neurons received excitatory input from a wide area of layers 2/3, 4, and 5 with widespread gamma-aminobutyric acidergic input from layer 2/3 and lower layer 5, whereas layer 6 corticothalamic neurons from the same cortical column received circumscribed excitatory input and discrete patches of inhibition derived from layer 6 of adjacent columns. These data demonstrate that layer 5 and layer 6 corticothalamic neurons receive unique sets of inputs and process them in different manners, supporting the hypothesis that layer-specific corticothalamic projections play distinct roles in information processing.