The paralaminar nuclei, including the medial division of the medial geniculate nucleus, surround the auditory thalamus medially and ventrally. This multimodal area receives convergent inputs from auditory, visual, and somatosensory structures and sends divergent outputs to cortical layer 1, amygdala, basal ganglia, and elsewhere. Studies implicate this region in the modulation of cortical 40-Hz oscillations, cortical information binding, and the conditioned fear response. We recently showed that the basic anatomy and intrinsic physiology of paralaminar cells are unlike that of neurons elsewhere in sensory thalamus. Here we evaluate the synaptic inputs to paralaminar cells from the inferior and superior colliculi and the cortex. Combined physiological and anatomical evidence indicates that paralaminar cells receive both excitatory and inhibitory inputs from both colliculi and excitatory cortical inputs. Excitatory inputs from all three sources typically generate small summating EPSPs composed of AMPA and NMDA components and terminate primarily on smaller dendrites and occasionally on dendritic spines. The cortical input shows strong paired-pulse facilitation (PPF), whereas both collicular inputs show weak PPF or paired-pulse depression (PPD). EPSPs of cells with no low-threshold calcium conductance do not evoke a burst response when the cell is hyperpolarized. Longer-latency EPSPs were seen and our evidence indicates that these arise from axon collateral inputs of other synaptically activated paralaminar cells. The inhibitory collicular inputs are GABAergic, activate GABA(A) receptors, and terminate on dendrites. Their activation can greatly alter EPSP-generated spike number and timing.