Control of orienting gaze shifts by the tectoreticulospinal system in the head-free cat. II. Sustained discharges during motor preparation and fixation.

1. We recorded from electrophysiologically identified output neurons of the superior colliculus (SC)--tectoreticular and tectoreticulospinal neurons [together called TR(S)Ns]--in the alert cat with head either unrestrained or immobilized. A cat actively exploring its visual surrounds typically makes a series of coordinated eye-head orienting movements that rapidly shift the visual axis from one point to another. These single-step shifts in gaze position (gaze = eye-in-space = eye-in-head + head-in-space) are separated by periods in which the visual axis remains stationary with respect to surrounding space. 2. Eighty-seven percent (86/99) of the TR(S)Ns studied during periods when the visual axis was stationary presented a sustained discharge, the intensity of which depended on the magnitude and direction of the vector drawn between current gaze position and the gaze position required to fixate a target of interest (gaze position error or GPE). The maximum sustained discharge recorded from each TR(S)N corresponded to a specific GPE vector and was correlated with the cell's position on the SC's retinotopically coded motor map. 3. The 86 TR(S)Ns could be divided into two classes. "Fixation TR(S)Ns" [fTR(S)Ns, n = 12] discharged maximally when the animal attentively fixated a target of interest, (i.e. GPE = 0 degrees). These neurons were located in the rostral SC and had visual receptive fields that included a representation of the area centralis. "Orientation TR(S)Ns" [oTR(S)Ns, n = 62] had visual receptive fields that excluded the area centralis and discharged for nonzero GPEs. The oTR(S)Ns were recorded more caudally on the SC's map. 4. For a given value of GPE, an ensemble of TR(S)Ns was active. When the cat changed its gaze position relative to a fixed target of interest, the zone of sustained activity shifted to a new collicular site. Thus, to maintain the maximum sustained discharge of a TR(S)N when target position was changed relative to the fixed body, it was necessary that gaze move to a new position that reestablished the preferred GPE. 5. The areal extent of GPEs for which a TR(S)N discharged defined a gaze position error field (GPEF) that was approximately coaligned with the cell's visual receptive field. The maximum sustained discharge occurred when GPE corresponded approximately to the center of the cell's GPEF. 6. The diameter of a TR(S)N's GPEF was related to the magnitude of that cell's optimal GPE. fTR(S)Ns had the smallest GPEFs, approximately 15-20 degrees; GPEF diameter was larger for oTR(S)Ns.(ABSTRACT TRUNCATED AT 400 WORDS)