Evidence for Gaze Feedback to the Cat Superior Colliculus: Discharges Reflect Gaze Trajectory Perturbations

Abstract

Rapid coordinated eye-head movements, called saccadic gaze shifts, displace the line of sight from one location to another. A critical structure in the gaze control circuitry is the superior colliculus (SC) of the midbrain, which drives gaze saccades by relaying cortical commands to brainstem eye and head motor circuits. We proposed that the SC lies within a gaze feedback loop and generates an error signal specifying gaze position error (GPE), the distance between target and current gaze positions. We investigated this feedback hypothesis in cats by briefly stopping head motion during large (Ϸ50°) gaze saccades made in the dark. This maneuver interrupted intended gaze saccades and briefly immobilized gaze (a plateau). After brake release, a corrective gaze saccade brought the gaze on goal. In the caudal SC, the firing frequency of a cell gradually increased to a maximum that just preceded the optimal gaze saccade encoded by the position of the cell and then declined back to zero near gaze saccade end. In brake trials, the activity level just preceding a brakeinduced plateau continued steadily during the plateau and waned to zero only near the end of the corrective saccade. The duration of neural activity was stretched to reflect the increased time to target acquisition, and firing frequency during a plateau was proportional to the GPE of the plateau. In comparison, in the rostral SC, the duration of saccade-related pauses in fixation cell activity increased as plateau duration increased. The data show that the cat's SC lies in a gaze feedback loop and that it encodes GPE.

Firing Patterns in Superior Colliculus of Head-Unrestrained Monkey during Normal and Perturbed Gaze Saccades Reveal Short-Latency Feedback and a Sluggish Rostral Shift in Activity

“…In the head-unrestrained cat, tectoreticular neurons carry the moving hill (Munoz et al, 1991;Bergeron et al, 2003;Matsuo et al, 2004). Our map discharges were also probably efferent signals because their temporal discharge properties were similar to those of tectoreticular neurons in the headfixed monkey (Rodgers et al, 2006).…”

“…In the head-unrestrained cat, the STT seems solved using feedback to the SC during a gaze saccade (Roucoux et al, 1980;Munoz et al, 1991;Lefèvre and Galiana, 1992;Bergeron and Guitton, 2000;Bergeron et al, 2003;Matsuo et al, 2004). If the level of firing frequency in the SC is represented as a relief map, then at gaze shift onset there is a bell-shaped "hill" of activity whose peak is centered on the appropriate site that encodes the desired saccade vector.…”

“…In cat, to show that the hill of activity is moved by feedback, we perturbed gaze shifts (Matsuo et al, 2004) by mechanically braking head movements, a procedure that mimics the natural occurrence of variable transient loads to the head (Laurutis and Robinson 1986;Guitton and Volle, 1987;Tomlinson, 1990;Choi and Guitton, 2006;Sylvestre and Cullen, 2006). We use the same approach here in monkey to show short-latency responses on the map to gaze trajectory perturbations and a gaze saccade amplitude-dependent moving hill.…”

Premotor Correlates of Integrated Feedback Control for Eye–Head Gaze Shifts

“…However, because the mechanical (Choi and Guitton, 2002;Matsuo et al, 2004) or electrical (Quaia et al, 1999) perturbations used in these previous studies interrupted gaze movements (i.e., rendered gaze stable for hundreds of milliseconds), it has not been possible to resolve whether the effects of the perturbations represented dynamic corrections to the ongoing gaze shift or the programming of a second corrective movement. In contrast, the relatively short time frame of the effects described here and the absence of gaze shift interruptions rule out the central programming of a corrective movement.…”

“…Previous reports have provided evidence that the combined comparator that controls gaze shifts might be centered on the superior colliculus (Choi and Guitton, 2002;Matsuo et al, 2004) and/or cerebellum (Quaia et al, 1999). However, because the mechanical (Choi and Guitton, 2002;Matsuo et al, 2004) or electrical (Quaia et al, 1999) perturbations used in these previous studies interrupted gaze movements (i.e., rendered gaze stable for hundreds of milliseconds), it has not been possible to resolve whether the effects of the perturbations represented dynamic corrections to the ongoing gaze shift or the programming of a second corrective movement.…”