Eye, head, and body movements jointly control the direction of gaze and the stability of retinal images in most mammalian species. The contribution of the individual movement components, however, will largely depend on the ecological niche the animal occupies and the layout of the animal's retina, in particular its photoreceptor density distribution. Here the relative contribution of eye-in-head and head-in-world movements in cats is measured, and the results are compared to recent human data. For the cat, a lightweight custom-made head-mounted video setup was used (CatCam). Human data were acquired with the novel EyeSeeCam device, which measures eye position to control a gaze-contingent camera in real time. For both species, analysis was based on simultaneous recordings of eye and head movements during free exploration of a natural environment. Despite the substantial differences in ecological niche, photoreceptor density, and saccade frequency, eye-movement characteristics in both species are remarkably similar. Coordinated eye and head movements dominate the dynamics of the retinal input. Interestingly, compensatory (gaze-stabilizing) movements play a more dominant role in humans than they do in cats. This finding was interpreted to be a consequence of substantially different timescales for head movements, with cats' head movements showing about a 5-fold faster dynamics than humans. For both species, models and laboratory experiments therefore need to account for this rich input dynamic to obtain validity for ecologically realistic settings.
Eye movements can be broadly classified into target-selecting and gaze-stabilizing eye movements. How do the different systems interact under natural conditions? Here we investigate interactions between the optokinetic and the target-selecting system in cats and humans. We use combinations of natural and grating stimuli. The natural stimuli are movies and pictures taken from the cat's own point of view with a head-mounted camera while it moved about freely in an outdoor environment. We superimpose linear global motion on the stimuli and use measurements of optokinetic nystagmus as a probe to study the interaction between the different systems responsible for controlling eye movements. Cats display higher precision stabilizing eye movements in response to natural pictures as compared to drifting gratings. In contrast, humans perform similarly under these two conditions. This suggests an interaction of the optokinetic and the pursuit system. In cats, the natural movies elicit very weak optokinetic responses. In humans, by contrast, the natural movie stimuli elicit effectively stabilizing eye movements. In both species, we find a unimodal distribution of saccades for all stimulus velocities. This suggests an early interaction of target-selecting and gaze-stabilizing saccades. Thus, we argue for a more integrated view in humans of the different eye movement systems.
Although saccadic eye movements can radically change the retinal image, perceptually their impact is surprisingly small. Here, we investigate possible neuronal correlates of saccadic suppression in cats freely viewing natural stimuli. By comparing changes attributable to saccadic events with passive stimulus changes, we find that during saccades: (i) evoked and induced activity is reduced in areas 18 and 21a by equal amounts, (ii) the variability of neuronal activity with stimulus category is abolished in both areas, and (iii) the high-power transient induced by stimulus change is not observed. These results present electrophysiological evidence for saccadic suppression at the level of primary and higher visual cortex under natural conditions.
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