The nucleus ventrolateralis thalami (VLT) in pigeons receives direct retinal and forebrain projections and has reciprocal connections with the optic tectum. Although VLT is a component of the avian visual system, no study directly examined its connections or its cellular response characteristics. We, therefore, recorded from single units in the pigeon's VLT while visually stimulating the ipsi- and/or contralateral eye. In addition, tracing experiments were conducted to investigate its afferent connections. Electrophysiologically, we discovered three types of neurons, two of which were probably activated via a top-down telencephalotectal system (latencies > 100 ms). Type I neurons responded to uni- and bilateral and type II neurons exclusively to bilateral stimulation. Type III neurons were probably activated by retinal or retinotectal input (latencies < 27 ms) and responded to contra- and bilateral stimulation. Retrograde tracer injections into the VLT revealed an ipsilateral forebrain input from the visual Wulst, from subregions of the arcopallium, and bilateral afferents from the optic tectum. Most intriguing was the direct connection between the VLTs of both hemispheres. We suggest that the avian VLT is part of a system that integrates visuomotor processes which are controlled by both forebrain hemispheres and that VLT contributes to descending tectomotor mechanisms.