1. The input-output connectivity, in cat, of tectoreticular (TRNs) and tectoreticulospinal (TRSNs) neurons [together called TR(S)Ns] suggests a role for these cells in the sensorimotor transformations necessary for controlling orienting behavior. Multimodal sensory information converges directly onto these tectal neurons, and they project to several brain stem and spinal cord centers involved in the control of eye- and head-orienting movements. In this and the following two papers, we describe the sensorimotor discharges of antidromically identified TR(S)Ns. Here we describe the process of localizing and identifying them, characteristics of both their antidromic and sensory responses, and effects of behavioral context on these responses. 2. In 13 alert, chronically prepared cats, a total of 293 neurons were antidromically identified from either the predorsal bundle (PDB) immediately rostral to abducens nucleus or the ventromedial funiculus of the spinal cord at the level of the first cervical vertebra (C1). The cell bodies of all identified TR(S)Ns were confined to the intermediate and deep laminae of the superior colliculus (SC). The antidromic nature of the action potential evoked by stimulating either the PDB or C1 was verified by the use of a number of established criteria, including collision testing. 3. The mean antidromic latency from the PDB (TRNs + TRSNs) was 0.84 +/- 0.59 (SD) ms (n = 217). The conduction velocities of all cells activated by PDB stimulation ranged from 4 to 40 m/s. The mean latency from C1 (TRSNs) was 1.03 +/- 0.52 ms (SD) (n = 64), whereas conduction velocities ranged from 14 to 80 m/s. 4. One hundred thirty-eight TR(S)Ns were studied long enough to yield significant data regarding their involvement in visuomotor-orienting behavior. Ninety-eight percent (130/133) of the TR(S)Ns tested for visual responses could be induced to discharge action potentials in response to some form of visual stimulation. The other three neurons remained silent, even in response to the most provocative stimuli. These silent neurons nevertheless were shown to be depolarized by visual stimuli. TR(S)Ns were occasionally tested for auditory and somatosensory responses and some were multimodal. 5. TR(S)Ns had visual receptive fields that conformed to the retinotopic map of the visual field that is represented within the SC. Cells found in the lateral SC had receptive fields located in the lower visual field, whereas neurons that were situated medially had receptive fields in the upper visual field. Cells found in the rostral SC had small fields that included a representation of the area centralis.(ABSTRACT TRUNCATED AT 400 WORDS)