Evidence That the Superior Colliculus Participates in the Feedback Control of Saccadic Eye Movements

Abstract

There is general agreement that saccades are guided to their targets by means of a motor error signal, which is produced by a local feedback circuit that calculates the difference between desired saccadic amplitude and an internal copy of actual saccadic amplitude. Although the superior colliculus (SC) is thought to provide the desired saccadic amplitude signal, it is unclear whether the SC resides in the feedback loop. To test this possibility, we injected muscimol into the brain stem region containing omnipause neurons (OPNs) to slow saccades and then determined whether the firing of neurons at different sites in the SC was altered. In 14 experiments, we produced saccadic slowing while simultaneously recording the activity of a single SC neuron. Eleven of the 14 neurons were saccade-related burst neurons (SRBNs), which discharged their most vigorous burst for saccades with an optimal amplitude and direction (optimal vector). The optimal directions for the 11 SRBNs ranged from nearly horizontal to nearly vertical, with optimal amplitudes between 4 and 17°. Although muscimol injections into the OPN region produced little change in the optimal vector, they did increase mean saccade duration by 25 to 192.8% and decrease mean saccade peak velocity by 20.5 to 69.8%. For optimal vector saccades, both the acceleration and deceleration phases increased in duration. However, during 10 of 14 experiments, the duration of deceleration increased as fast as or faster than that of acceleration as saccade duration increased, indicating that most of the increase in duration occurred during the deceleration phase. SRBNs in the SC changed their burst duration and firing rate concomitantly with changes in saccadic duration and velocity, respectively. All SRBNs showed a robust increase in burst duration as saccadic duration increased. Five of 11 SRBNs also exhibited a decrease in burst peak firing rate as saccadic velocity decreased. On average across the neurons, the number of spikes in the burst was constant. There was no consistent change in the discharge of the three SC neurons that did not exhibit bursts with saccades. Our data show that the SC receives feedback from downstream saccade-related neurons about the ongoing saccades. However, the changes in SC firing produced in our study do not suggest that the feedback is involved with producing motor error. Instead, the feedback seems to be involved with regulating the duration of the discharge of SRBNs so that the desired saccadic amplitude signal remains present throughout the saccade.

Pontine Omnipause Activity During Conjugate and Disconjugate Eye Movements in Macaques

“…The omnidirectionality of this effect and its neu- ronal origin suggest an involvement of the OPNs. Furthermore, partial lesions of the nucleus raphe interpositus, where the OPNs are located, result in abnormally long and slow saccades (Kaneko 1996;Soetedjo et al 2002). Optimal saccadic dynamics, as pointed out by Scudder (1988) and Moschovakis (1994) in explaining such OPN lesion-related saccadic slowing, require a precisely timed release of the MLBs by the OPNs.…”

“…Could the action of only a few OPNs influence behavior? The recent report of strong dynamical effects in the SC bursters observed by Soetedjo et al (2002) in association with small inhibitory injections in the OPNs suggests that there may be no need for the very large and generalized suppression of OPN activity, required by earlier models, to modify saccadic dynamics. If so, this mechanism, as also noted by Soetedjo et al must be substantially different from the one proposed in the earlier models by Scudder (1988) and Moschovakis (1994).…”

“…Surprisingly, damage to OPNs does not cause the devastating effects such as opsoclonus that might be expected by the loss of burst neuron inhibition, as an early model (Zee and Robinson 1979) and some clinical studies (Ashe et al 1991;Averbuch-Heller and Remler 1996) have suggested. The most evident effect of experimental damage to OPNs is slower but otherwise normal saccades (Kaneko 1996;Soetedjo et al 2002). Although the precise mechanism is unknown, this result has been successfully simulated by the reduction of OPN activity within contemporary models of the saccadic system (Moschovakis 1994;Scudder 1988).…”

Discharge of Monkey Nucleus Reticularis Tegmenti Pontis Neurons Changes During Saccade Adaptation

“…First, we implanted head-stabilization lugs and a preformed scleral search coil (Judge et al 1980) for the electromagnetic measurement of eye movements (Collewijn 1977;Robinson 1963). After a week of recovery, the monkeys were trained to track a jumping target spot (see Soetedjo et al 2002a for details).…”

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

“…This important test has been attempted in the head-fixed monkey. Saccade trajectories were perturbed by using either electrophysiological or pharmacological approaches (Keller and Edelman, 1994;Munoz et al, 1996;Keller et al, 2000;Soetedjo et al, 2002a) as well as with blinks (Goossens and Van Opstal, 2000a,b). In these studies, monkeys compensated accurately for the perturbation, and gaze arrived on target.…”