Eckart Zimmermann

Motor signals in visual localization

We demonstrate a strong sensory-motor coupling in visual localization in which experimental modification of the control of saccadic eye movements leads to an associated change in the perceived location of objects. Amplitudes of saccades to peripheral targets were altered by saccadic adaptation, induced by an artificial step of the saccade target during the eye movement, which leads the oculomotor system to recalibrate saccade parameters. Increasing saccade amplitudes induced concurrent shifts in perceived location of visual objects. The magnitude of perceptual shift depended on the size and persistence of errors between intended and actual saccade amplitudes. This tight agreement between the change of eye movement control and the change of localization shows that perceptual space is shaped by motor knowledge rather than simply constructed from visual input.

Spatiotopic neural representations develop slowly across saccades

One of the long-standing unsolved mysteries of visual neuroscience is how the world remains apparently stable in the face of continuous movements of eyes, head and body. Many factors seem to contribute to this stability, including rapid updating mechanisms that temporarily remap the visual input to compensate for the impending saccade. However, there is also a growing body of evidence pointing to more long-lasting spatiotopic neural representations, which remain solid in external rather than retinal coordinates. In this study, we show that these spatiotopic representations take hundreds of milliseconds to build up robustly.

Mislocalization of Flashed and Stationary Visual Stimuli after Adaptation of Reactive and Scanning Saccades

When we look around and register the location of visual objects, our oculomotor system continuously prepares targets for saccadic eye movements. The preparation of saccade targets may be directly involved in the perception of object location because modification of saccade amplitude by saccade adaptation leads to a distortion of the visual localization of briefly flashed spatial probes. Here, we investigated effects of adaptation on the localization of continuously visible objects. We compared adaptation-induced mislocalization of probes that were present for 20 ms during the saccade preparation period and of probes that were present for >1 s before saccade initiation. We studied the mislocalization of these probes for two different saccade types, reactive saccades to a suddenly appearing target and scanning saccades in the self-paced viewing of a stationary scene. Adaptation of reactive saccades induced mislocalization of flashed probes. Adaptation of scanning saccades induced in addition also mislocalization of stationary objects. The mislocalization occurred in the absence of visual landmarks and must therefore originate from the change in saccade motor parameters. After adaptation of one type of saccade, the saccade amplitude change and the mislocalization transferred only weakly to the other saccade type. Mislocalization of flashed and stationary probes thus followed the selectivity of saccade adaptation. Since the generation and adaptation of reactive and scanning saccades are known to involve partially different brain mechanisms, our results suggest that visual localization of objects in space is linked to saccade targeting at multiple sites in the brain.

Spatial Position Information Accumulates Steadily over Time

One of the more enduring mysteries of neuroscience is how the visual system constructs robust maps of the world that remain stable in the face of frequent eye movements. Here we show that encoding the position of objects in external space is a relatively slow process, building up over hundreds of milliseconds. We display targets to which human subjects saccade after a variable preview duration. As they saccade, the target is displaced leftwards or rightwards, and subjects report the displacement direction. When subjects saccade to targets without delay, sensitivity is poor; but if the target is viewed for 300–500 ms before saccading, sensitivity is similar to that during fixation with a strong visual mask to dampen transients. These results suggest that the poor displacement thresholds usually observed in the “saccadic suppression of displacement” paradigm are a result of the fact that the target has had insufficient time to be encoded in memory, and not a result of the action of special mechanisms conferring saccadic stability. Under more natural conditions, trans-saccadic displacement detection is as good as in fixation, when the displacement transients are masked.

Masking produces compression of space and time in the absence of eye movements

Whenever the visual stream is abruptly disturbed by eye movements, blinks, masks, or flashes of light, the visual system needs to retrieve the new locations of current targets and to reconstruct the timing of events to straddle the interruption. This process may introduce position and timing errors. We here report that very similar errors are seen in human subjects across three different paradigms when disturbances are caused by either eye movements, as is well known, or, as we now show, masking. We suggest that the characteristic effects of eye movements on position and time, spatial and temporal compression and saccadic suppression of displacement, are consequences of the interruption and the subsequent reconnection and are seen also when visual input is masked without any eye movements. Our data show that compression and suppression effects are not solely a product of ocular motor activity but instead can be properties of a correspondence process that links the targets of interest across interruptions in visual input, no matter what their source.

Eye position effects in oculomotor plasticity and visual localization.

For visual localization to remain accurate across changes of gaze, a signal representing the position of the eye in the orbita is needed to code spatial locations in a reference frame that is independent of retinal displacements. Here we report evidence that the localization of visual objects in space is coded in an extraretinal reference frame. In human subjects, we used outward saccadic adaptation, which can be induced artificially by a systematic displacement of the saccade target. This form of oculomotor plasticity is accompanied by changes in spatial perception, thus highlighting the relevance of saccade metrics for visual localization. We tested the reference frame of outward adaptation for reactive and scanning saccades and visual localization. For scanning saccades, adaptation magnitude was drastically reduced at positions distant from the adapted eye position. Changes in visual localization showed a very similar modulation of eye position. These results suggest that scanning saccade adaptation is encoded in a nonretinotopic reference frame. Eye position effects for reactive saccade adaptation were smaller, and the induced mislocalization did not vary significantly between eye positions. The different modulation of reactive and scanning saccade adaptation supports the idea that oculomotor plasticity can occur at multiple sites in the brain. The findings are also consistent with previous evidence for a stronger influence of scanning saccade adaptation on the visual localization of objects in space.

Eye position effects in saccadic adaptation

Saccades are used by the visual system to explore visual space with the high accuracy of the fovea. The visual error after the saccade is used to adapt the control of subsequent eye movements of the same amplitude and direction in order to keep saccades accurate. Saccadic adaptation is thus specific to saccade amplitude and direction. In the present study we show that saccadic adaptation is also specific to the initial position of the eye in the orbit. This is useful, because saccades are normally accompanied by head movements and the control of combined head and eye movements depends on eye position. Many parts of the saccadic system contain eye position information. Using the intrasaccadic target step paradigm, we adaptively reduced the amplitude of reactive saccades to a suddenly appearing target at a selective position of the eyes in the orbitae and tested the resulting amplitude changes for the same saccade vector at other starting positions. For central adaptation positions the saccade amplitude reduction transferred completely to eccentric starting positions. However, for adaptation at eccentric starting positions, there was a reduced transfer to saccades from central starting positions or from eccentric starting positions in the opposite hemifield. Thus eye position information modifies the transfer of saccadic amplitude changes in the adaptation of reactive saccades. A gain field mechanism may explain the eye position dependence found.

Buildup of spatial information over time and across eye-movements

To interact rapidly and effectively with our environment, our brain needs access to a neural representation of the spatial layout of the external world. However, the construction of such a map poses major challenges, as the images on our retinae depend on where the eyes are looking, and shift each time we move our eyes, head and body to explore the world. Research from many laboratories including our own suggests that the visual system does compute spatial maps that are anchored to real-world coordinates. However, the construction of these maps takes time (up to 500ms) and also attentional resources. We discuss research investigating how retinotopic reference frames are transformed into spatiotopic reference-frames, and how this transformation takes time to complete. These results have implications for theories about visual space coordinates and particularly for the current debate about the existence of spatiotopic representations.

The reference frames in saccade adaptation

Saccade adaptation is a mechanism that adjusts saccade landing positions if they systematically fail to reach their intended target. In the laboratory, saccades can be shortened or lengthened if the saccade target is displaced during execution of the saccade. In this study, saccades were performed from different positions to an adapted saccade target to dissociate adaptation to a spatiotopic position in external space from a combined retinotopic and spatiotopic coding. The presentation duration of the saccade target before saccade execution was systematically varied, during adaptation and during test trials, with a delayed saccade paradigm. Spatiotopic shifts in landing positions depended on a certain preview duration of the target before saccade execution. When saccades were performed immediately to a suddenly appearing target, no spatiotopic adaptation was observed. These results suggest that a spatiotopic representation of the visual target signal builds up as a function of the duration the saccade target is visible before saccade execution. Different coordinate frames might also explain the separate adaptability of reactive and voluntary saccades. Spatiotopic effects were found only in outward adaptation but not in inward adaptation, which is consistent with the idea that outward adaptation takes place at the level of the visual target representation, whereas inward adaptation is achieved at a purely motor level.

Numerosity perception after size adaptation.

While some researchers propose the existence of a special numerosity sense, others challenge this view and argue that numerosity is derived from low-level features as density information. Here, we used size adaptation to manipulate the apparent area size of an object set without changing its physical density. After size adaptation, two probe patches were shown, each of which contained a specific numerosity of dots. Subjects were required to report, which probe patch contained more dots. Numerosity perception was compared between conditions where probe patches were adapted to appear smaller or larger. Size adaptation affected numerosity perception in a logarithmic fashion, increasing with the numerosity in the probe patch. No changes in density perception were found after size adaptation. Data suggest that size and density information play only a minor role in the estimation of low numerosities. In stark contrast, high numerosities strongly depend on size and density information. The data reinforce recent claims of separate mechanism for the perception of low and high numerosities.