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To maintain a stable representation of the visual environment as we move, the brain must update the locations of targets in space using extra-retinal signals. Humans can accurately update after intervening active whole-body translations. But can they also update for passive translations (i.e., without efference copy signals of an outgoing motor command)? We asked six head-fixed subjects to remember the location of a briefly flashed target (five possible targets were located at depths of 23, 33, 43, 63, and 150 cm in front of the cyclopean eye) as they moved 10 cm left, right, up, down, forward, or backward while fixating a head-fixed target at 53 cm. After the movement, the subjects made a saccade to the remembered location of the flash with a combination of version and vergence eye movements. We computed an updating ratio where 0 indicates no updating and 1 indicates perfect updating. For lateral and vertical whole-body motion, where updating performance is judged by the size of the version movement, the updating ratios were similar for leftward and rightward translations, averaging 0.84 +/- 0.28 (mean +/- SD) as compared with 0.51 +/- 0.33 for downward and 1.05 +/- 0.50 for upward translations. For forward/backward movements, where updating performance is judged by the size of the vergence movement, the average updating ratio was 1.12 +/- 0.45. Updating ratios tended to be larger for far targets than near targets, although both intra- and intersubject variabilities were smallest for near targets. Thus in addition to self-generated movements, extra-retinal signals involving otolith and proprioceptive cues can also be used for spatial constancy.

Most of what we know about the neural control of gaze comes from experiments in head-fixed animals, but several "head-free" studies have suggested that fixing the head dramatically alters the apparent gaze command. We directly investigated this issue by quantitatively comparing head-fixed and head-free gaze trajectories evoked by electrically stimulating 52 sites in the superior colliculus (SC) of two monkeys and 23 sites in the supplementary eye fields (SEF) of two other monkeys. We found that head movements made a significant contribution to gaze shifts evoked from both neural structures. In the majority of the stimulated sites, average gaze amplitude was significantly larger and individual gaze trajectories were significantly less convergent in space with the head free to move. Our results are consistent with the hypothesis that head-fixed stimulation only reveals the oculomotor component of the gaze shift, not the true, planned goal of the movement. One implication of this finding is that when comparing stimulation data against popular gaze control models, freeing the head shifts the apparent coding of gaze away from a "spatial code" toward a simpler visual model in the SC and toward an eye-centered or fixed-vector model representation in the SEF. [ABSTRACT FROM AUTHOR]

The superior colliculus (SC) has a topographic map of visual space, but the spatial nature of its output command for orienting gaze shifts remains unclear. Here we show that the SC codes neither desired gaze displacement nor gaze direction in space (as debated previously), but rather, desired gaze direction in retinal coordinates. Electrical micro-stimulation of the SC in two head-free (nonimmobilized) monkeys evoked natural-looking, eye-head gaze shifts, with anterior sites producing small, fixed-vector movements and posterior sites producing larger, strongly converging movements. However, when correctly calculated in retinal coordinates, all of these trajectories became 'fixed-vector.' Moreover, our data show that this eye-centered SC command is then further transformed, as a function of eye and head position, by downstream mechanisms into the head- and body-centered commands for coordinated eye-head gaze shifts. [ABSTRACT FROM AUTHOR]