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Our visual systems rapidly perceive and integrate information about object identities and locations. There is long-standing debate about if and how we achieve world-centered (spatiotopic) object representations across eye movements, with many studies reporting persistent retinotopic (eye-centered) effects even for higher level object-location binding. But these studies are generally conducted in fairly static experimental contexts. Might spatiotopic object-location binding only emerge in more dynamic saccade contexts? In the present study, we investigated this using the spatial congruency bias paradigm in healthy adults. In the static (single-saccade) context, we found purely retinotopic binding, as before. However, robust spatiotopic binding emerged in the dynamic saccade context (multiple frequent saccades and saccades during stimulus presentation). We further isolated specific factors that modulate retinotopic and spatiotopic binding. Our results provide strong evidence that dynamic saccade context can trigger more stable object-location binding in ecologically relevant spatiotopic coordinates, perhaps via a more flexible brain state that accommodates improved visual stability in the dynamic world. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

We can focus visuospatial attention by covertly attending to relevant locations, moving our eyes, or both simultaneously. How does shifting versus holding covert attention during fixation compare with maintaining covert attention across saccades? We acquired human fMRI data during a combined saccade and covert attention task. On Eyes-fixed trials, participants either held attention at the same initial location ("hold attention") or shifted attention to another location midway through the trial ("shift attention"). On Eyes-move trials, participants made a saccade midway through the trial, while maintaining attention in one of two reference frames: the "retinotopic attention" condition involved holding attention at a fixation-relative location but shifting to a different screen-centered location, whereas the "spatiotopic attention" condition involved holding attention on the same screen-centered location but shifting relative to fixation. We localized the brain network sensitive to attention shifts (shift > hold attention), and used multivoxel pattern time course (MVPTC) analyses to investigate the patterns of brain activity for spatiotopic and retinotopic attention across saccades. In the attention shift network, we found transient information about both whether covert shifts were made and whether saccades were executed. Moreover, in this network, both retinotopic and spatiotopic conditions were represented more similarly to shifting than to holding covert attention. An exploratory searchlight analysis revealed additional regions where spatiotopic was relatively more similar to shifting and retinotopic more to holding. Thus, maintaining retinotopic and spatiotopic attention across saccades may involve different types of updating that vary in similarity to covert attention "hold" and "shift" signals across different regions., (Copyright © 2021 Zhang and Golomb.)

To interact successfully with objects, we must maintain stable representations of their locations in the world. However, their images on the retina may be displaced several times per second by large, rapid eye movements. A number of studies have demonstrated that visual processing is heavily influenced by gaze-centered (retinotopic) information, including a recent finding that memory for an object's location is more accurate and precise in gaze-centered (retinotopic) than world-centered (spatiotopic) coordinates (Golomb & Kanwisher, 2012b). This effect is somewhat surprising, given our intuition that behavior is successfully guided by spatiotopic representations. In the present experiment, we asked whether the visual system may rely on a more spatiotopic memory store depending on the mode of responding. Specifically, we tested whether reaching toward and tapping directly on an object's location could improve memory for its spatiotopic location. Participants performed a spatial working memory task under four conditions: retinotopic vs. spatiotopic task, and computer mouse click vs. touchscreen reaching response. When participants responded by clicking with a mouse on the screen, we replicated Golomb & Kanwisher's original results, finding that memory was more accurate in retinotopic than spatiotopic coordinates and that the accuracy of spatiotopic memory deteriorated substantially more than retinotopic memory with additional eye movements during the memory delay. Critically, we found the same pattern of results when participants responded by using their finger to reach and tap the remembered location on the monitor. These results further support the hypothesis that spatial memory is natively retinotopic; we found no evidence that engaging the motor system improves spatiotopic memory across saccades.

Despite frequent eye movements that rapidly shift the locations of objects on our retinas, our visual system creates a stable perception of the world. To do this, it must convert eye-centered (retinotopic) input to world-centered (spatiotopic) percepts. Moreover, for successful behavior we must also incorporate information about object features/identities during this updating - a fundamental challenge that remains to be understood. Here we adapted a recent behavioral paradigm, the "spatial congruency bias," to investigate object-location binding across an eye movement. In two initial baseline experiments, we showed that the spatial congruency bias was present for both gabor and face stimuli in addition to the object stimuli used in the original paradigm. Then, across three main experiments, we found the bias was preserved across an eye movement, but only in retinotopic coordinates: Subjects were more likely to perceive two stimuli as having the same features/identity when they were presented in the same retinotopic location. Strikingly, there was no evidence of location binding in the more ecologically relevant spatiotopic (world-centered) coordinates; the reference frame did not update to spatiotopic even at longer post-saccade delays, nor did it transition to spatiotopic with more complex stimuli (gabors, shapes, and faces all showed a retinotopic congruency bias). Our results suggest that object-location binding may be tied to retinotopic coordinates, and that it may need to be re-established following each eye movement rather than being automatically updated to spatiotopic coordinates.

The crux of vision is to identify objects and determine their locations in the environment. Although initial visual representations are necessarily retinotopic (eye centered), interaction with the real world requires spatiotopic (absolute) location information. We asked whether higher level human visual cortex-important for stable object recognition and action-contains information about retinotopic and/or spatiotopic object position. Using functional magnetic resonance imaging multivariate pattern analysis techniques, we found information about both object category and object location in each of the ventral, dorsal, and early visual regions tested, replicating previous reports. By manipulating fixation position and stimulus position, we then tested whether these location representations were retinotopic or spatiotopic. Crucially, all location information was purely retinotopic. This pattern persisted when location information was irrelevant to the task, and even when spatiotopic (not retinotopic) stimulus position was explicitly emphasized. We also conducted a "searchlight" analysis across our entire scanned volume to explore additional cortex but again found predominantly retinotopic representations. The lack of explicit spatiotopic representations suggests that spatiotopic object position may instead be computed indirectly and continually reconstructed with each eye movement. Thus, despite our subjective impression that visual information is spatiotopic, even in higher level visual cortex, object location continues to be represented in retinotopic coordinates.

Successful visually guided behavior requires information about spatiotopic (i.e., world-centered) locations, but how accurately is this information actually derived from initial retinotopic (i.e., eye-centered) visual input? We conducted a spatial working memory task in which subjects remembered a cued location in spatiotopic or retinotopic coordinates while making guided eye movements during the memory delay. Surprisingly, after a saccade, subjects were significantly more accurate and precise at reporting retinotopic locations than spatiotopic locations. This difference grew with each eye movement, such that spatiotopic memory continued to deteriorate, whereas retinotopic memory did not accumulate error. The loss in spatiotopic fidelity is therefore not a generic consequence of eye movements, but a direct result of converting visual information from native retinotopic coordinates. Thus, despite our conscious experience of an effortlessly stable spatiotopic world and our lifetime of practice with spatiotopic tasks, memory is actually more reliable in raw retinotopic coordinates than in ecologically relevant spatiotopic coordinates.

During natural vision, eye movements can drastically alter the retinotopic (eye-centered) coordinates of locations and objects, yet the spatiotopic (world-centered) percept remains stable. Maintaining visuospatial attention in spatiotopic coordinates requires updating of attentional representations following each eye movement. However, this updating is not instantaneous; attentional facilitation temporarily lingers at the previous retinotopic location after a saccade, a phenomenon known as the retinotopic attentional trace. At various times after a saccade, we probed attention at an intermediate location between the retinotopic and spatiotopic locations to determine whether a single locus of attentional facilitation slides progressively from the previous retinotopic location to the appropriate spatiotopic location, or whether retinotopic facilitation decays while a new, independent spatiotopic locus concurrently becomes active. Facilitation at the intermediate location was not significant at any time, suggesting that top-down attention can result in enhancement of discrete retinotopic and spatiotopic locations without passing through intermediate locations.

With each eye movement, the image of the world received by the visual system changes dramatically. To maintain stable spatiotopic (world-centered) visual representations, the retinotopic (eye-centered) coordinates of visual stimuli are continually remapped, even before the eye movement is completed. Recent psychophysical work has suggested that updating of attended locations occurs as well, although on a slower timescale, such that sustained attention lingers in retinotopic coordinates for several hundred milliseconds after each saccade. To explore where and when this "retinotopic attentional trace" resides in the cortical visual processing hierarchy, we conducted complementary functional magnetic resonance imaging and event-related potential (ERP) experiments using a novel gaze-contingent task. Human subjects executed visually guided saccades while covertly monitoring a fixed spatiotopic target location. Although subjects responded only to stimuli appearing at the attended spatiotopic location, blood oxygen level-dependent responses to stimuli appearing after the eye movement at the previously, but no longer, attended retinotopic location were enhanced in visual cortical area V4 and throughout visual cortex. This retinotopic attentional trace was also detectable with higher temporal resolution in the anterior N1 component of the ERP data, a well established signature of attentional modulation. Together, these results demonstrate that, when top-down spatiotopic signals act to redirect visuospatial attention to new retinotopic locations after eye movements, facilitation transiently persists in the cortical regions representing the previously relevant retinotopic location.

With each eye movement, the image received by the visual system changes drastically. To maintain stable spatiotopic (world-centered) representations, the relevant retinotopic (eye-centered) coordinates must be continually updated. Although updating or remapping of visual scene representations can occur very rapidly, J. D. Golomb, M. M. Chun, and J. A. Mazer (2008) demonstrated that representations of sustained attention update more slowly than the remapping literature would predict; attentional benefits at previously attended retinotopic locations linger after completion of the saccade, even when this location is no longer behaviorally relevant. The present study explores the robustness of this "retinotopic attentional trace." We report significant retinotopic facilitation despite attempts to eliminate or reduce it by enhancing spatiotopic reference frames with permanent visual cues in the stimulus display and by introducing a different task where the attended location is the saccade target itself. Our results support and extend our earlier model of native retinotopically organized salience maps that must be dynamically updated to reflect the task-relevant spatiotopic location with each saccade. Consistent with the idea that attentional facilitation arises from persistent, recurrent neural activity, it takes measurable time for this facilitation to decay, leaving behind a retinotopic attentional trace after the saccade has been executed, regardless of conflicting task demands.

Visual processing can be facilitated by covert attention at behaviorally relevant locations. If the eyes move while a location in the visual field is facilitated, what happens to the internal representation of the attended location? With each eye movement, the retinotopic (eye-centered) coordinates of the attended location change while the spatiotopic (world-centered) coordinates remain stable. To investigate whether the neural substrates of spatial attention reside in retinotopically and/or spatiotopically organized maps, we used a novel gaze-contingent behavioral paradigm that probed spatial attention at various times after eye movements. When task demands required maintaining a spatiotopic representation after the eye movement, we found facilitation at the retinotopic location of the spatial cue for 100-200 ms after the saccade, although this location had no behavioral significance. This task-irrelevant retinotopic representation dominated immediately after the saccade, whereas at later delays, the task-relevant spatiotopic representation prevailed. However, when task demands required maintaining the cue in retinotopic coordinates, a strong retinotopic benefit persisted long after the saccade, and there was no evidence of spatiotopic facilitation. These data suggest that the cortical and subcortical substrates of spatial attention primarily reside in retinotopically organized maps that must be dynamically updated to compensate for eye movements when behavioral demands require a spatiotopic representation of attention. Our conclusion is that the visual system's native or low-level representation of endogenously maintained spatial attention is retinotopic, and remapping of attention to spatiotopic coordinates occurs slowly and only when behaviorally necessary.