Superior Colliculus Inactivation Causes Stable Offsets in Eye Position during Tracking

Abstract

The primate superior colliculus (SC) is often viewed as composed of two distinct motor zones with complementary functions: a peripheral region that helps generate saccades to eccentric targets and a central one that maintains fixation by suppressing saccades. Here, we directly tested the alternative interpretation that topography in the SC is not strictly motor, nor does it form two distinct zones, but instead forms a single map of behaviorally relevant goal locations. Primates tracked the invisible midpoint between two moving stimuli, such that the stimuli guiding tracking were peripheral whereas the inferred movement goal was foveal and parafoveal. Temporary inactivation of neurons in the central portion of the topographic map of the SC, representing the invisible goal, caused stable offsets in eye position during tracking that were directed away from the retinotopic position encoded by the inactivated SC site. Critically, these offsets were not accompanied by a systematic inability to generate or suppress saccades, and they were not fully explained by motor deficits in saccades, smooth pursuit, or fixation. In addition, the magnitude of the offset depended on the eccentricity of the inactivated site as well as the degree of spatial uncertainty associated with the behavioral goal. These results indicate that gaze control depends on the balance of activity across a map of goal locations in the SC, and that by silencing some of the neurons in the normally active population representing the behavioral goal, focal inactivation causes a biased estimate of where to look.

Inactivation of Primate Superior Colliculus Biases Target Choice for Smooth Pursuit, Saccades, and Button Press Responses

“…The shifts in eye position for monkey V were similar to measurements made by Hafed et al (2008) for a stimulus of the same size, whereas the shifts in eye position for monkey P were larger and had greater variance. These measurements were used for control experiments in which we offset the position of fixation by the measured amount instead of performing an injection.…”

“…We found small offsets in the eye position of central fixation away from the affected visual field (see Table 1), similar to offsets in eye position reported during smooth pursuit (Hafed et al 2008). For monkey P, we measured the difference between eye position at central fixation before muscimol injection and following the collection of postinjection data.…”

“…SC inactivation is known to shift the position of central gaze a small amount away from the affected visual field when tracking a visual target (Hafed et al 2008). If offsets in central gaze occurred during fixation in our target selection tasks, they would shift stimuli placed outside the affected field closer to central gaze, which could influence the stimulus choice.…”

Inactivation and stimulation of the frontal pursuit area change pursuit metrics without affecting pursuit target selection

“…First, the day before the inactivation, we were able to evoke smooth pursuit eye movements at the target site with currents less than 50 A (tungsten electrodes, impedances 900 k⍀ to 3.0 M⍀). Second, on the day of the inactivation itself, we were able to evoke smooth pursuit eye movements at our intended depth with our custom-made injectrode (Chen et al 2001;Hafed et al 2008). The sites targeted for inactivation were the same locations at which we had previously recorded pursuit-related neuronal activity, as described in detail previously (Mahaffy and Krauzlis 2011).…”

Disruption of Fixation Reveals Latent Sensorimotor Processes in the Superior Colliculus

“…Movement suppression is controlled by so-called "fixation-related neurons" in the rostral SC (Munoz and Wurtz, 1993a). These neurons are active during fixation, which is likely maintained by preparatory activity associated with programming of microsaccades (Hafed et al, 2009). Crucially, they suppress their discharge before large saccades.…”