André Bergeron

Superior colliculus encodes distance to target, not saccade amplitude, in multi-step gaze shifts

The superior colliculus (SC) is important for generating coordinated eye–head gaze saccades. Its deeper layers contain a retinotopically organized motor map in which each site is thought to encode a specific gaze saccade vector. Here we show that this fundamental assumption in current models of collicular function does not hold true during horizontal multi-step gaze shifts in darkness that are directed to a goal and composed of a sequence of gaze saccades separated by periods of steady fixation. At the start of a multi-step gaze shift in cats, neural activity on the SCs map was located caudally to encode the overall amplitude of the gaze displacement, not the first saccade in the sequence. As the gaze shift progressed, the locus of activity moved to encode the error between the goal and the current gaze position. Contrary to common belief, the locus of activity never encoded gaze saccade amplitude, except for the last saccade in the sequence.

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

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 (≈50°) 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 brake-induced 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 cats SC lies in a gaze feedback loop and that it encodes GPE.

Fixation neurons in the superior colliculus encode distance between current and desired gaze positions.

A visual scene is scrutinized during sequential periods of steady fixation, connected by saccades that shift the visual axis (gaze) to new positions. During such exploratory scan paths, gaze frequently strays from and then returns to salient features. How the brain keeps track of major end-goals and intermediate subgoals is not understood. We studied the discharge of fixation neurons of the brainstems superior colliculus during multiple-step gaze shifts composed of a sequence of saccades made in the dark and separated by short periods of steady fixation. Cells were initially silent. As sequential gaze saccades approached the goal, firing began; its frequency increased progressively and peaked when gaze was on the remembered target location. We conclude that these fixation neurons encode the error between desired and actual gaze positions, irrespective of trajectory characteristics.

Ipsilateral head and centring eye movements evoked from monkey premotor cortex.

Recent studies in monkeys have identified a ‘polysensory, defensive zone’, in the ventral premotor cortex, stimulation of which results in coordinated multisegmental movements reminiscent of those normally produced by animals that react to head-directed threatening stimuli. Here, we describe gaze movements evoked in the head-fixed and head-unrestrained monkey by electrical stimulation of the polysensory zone. Centring eye movements were elicited at all sites and under both conditions. With the head free to move, ipsilateral head movements always accompanied evoked eye movements and carried gaze into a final steady-state position in ipsilateral body space. Our results support the hypothesis that stimulation of the polysensory zone generates avoidance behaviours in which gaze is moved away from a head-directed threatening stimulus.