Marc Zirnsak

About the influence of post-saccadic mechanisms for visual stability on peri-saccadic compression of object location

Peri-saccadic perception experiments have revealed a multitude of mislocalization phenomena. For instance, a briefly flashed stimulus is perceived closer to the saccade target, whereas a displacement of the saccade target goes usually unnoticeable. This latter saccadic suppression of displacement has been explained by a built-in characteristic of the perceptual system: the assumption that during a saccade, the environment remains stable. We explored whether the mislocalization of a briefly flashed stimulus toward the saccade target also grounds in the built-in assumption of a stable environment. If the mislocalization of a peri-saccadically flashed stimulus originates from a post-saccadic alignment process, an additional location marker at the position of the upcoming flash should counteract compression. Alternatively, compression might be the result of peri-saccadic attentional phenomena. In this case, mislocalization should occur even if the position of the flashed stimulus is marked. When subjects were asked about their perceived location, they mislocalized the stimulus toward the saccade target, even though they were fully aware of the correct stimulus location. Thus, our results suggest that the uncertainty about the location of a flashed stimulus is not inherently relevant for compression.

Visual space is compressed in prefrontal cortex before eye movements

We experience the visual world through a series of saccadic eye movements, each one shifting our gaze to bring objects of interest to the fovea for further processing. Although such movements lead to frequent and substantial displacements of the retinal image, these displacements go unnoticed. It is widely assumed that a primary mechanism underlying this apparent stability is an anticipatory shifting of visual receptive fields (RFs) from their presaccadic to their postsaccadic locations before movement onset. Evidence of this predictive ‘remapping’ of RFs has been particularly apparent within brain structures involved in gaze control. However, critically absent among that evidence are detailed measurements of visual RFs before movement onset. Here we show that during saccade preparation, rather than remap, RFs of neurons in a prefrontal gaze control area massively converge towards the saccadic target. We mapped the visual RFs of prefrontal neurons during stable fixation and immediately before the onset of eye movements, using multi-electrode recordings in monkeys. Following movements from an initial fixation point to a target, RFs remained stationary in retinocentric space. However, in the period immediately before movement onset, RFs shifted by as much as 18 degrees of visual angle, and converged towards the target location. This convergence resulted in a threefold increase in the proportion of RFs responding to stimuli near the target region. In addition, like in human observers, the population of prefrontal neurons grossly mislocalized presaccadic stimuli as being closer to the target. Our results show that RF shifts do not predict the retinal displacements due to saccades, but instead reflect the overriding perception of target space during eye movements.

The peri-saccadic perception of objects and space.

Eye movements affect object localization and object recognition. Around saccade onset, briefly flashed stimuli appear compressed towards the saccade target, receptive fields dynamically change position, and the recognition of objects near the saccade target is improved. These effects have been attributed to different mechanisms. We provide a unifying account of peri-saccadic perception explaining all three phenomena by a quantitative computational approach simulating cortical cell responses on the population level. Contrary to the common view of spatial attention as a spotlight, our model suggests that oculomotor feedback alters the receptive field structure in multiple visual areas at an intermediate level of the cortical hierarchy to dynamically recruit cells for processing a relevant part of the visual field. The compression of visual space occurs at the expense of this locally enhanced processing capacity.

2006 Special Issue: V4 receptive field dynamics as predicted by a systems-level model of visual attention using feedback from the frontal eye field

Visual attention is generally considered to facilitate the processing of the attended stimulus. Its mechanisms, however, are still under debate. We have developed a systems-level model of visual attention which predicts that attentive effects emerge by the interactions between different brain areas. Recent physiological studies have provided evidence that attention also alters the receptive field structure. For example, V4 receptive fields typically shrink and shift towards the saccade target around saccade onset. We show that receptive field dynamics are inherently predicted by the mechanism of feedback in our model. According to the model an oculomotor feedback signal from an area involved in the competition for the saccade target location, e.g. the frontal eye field, enhances the gain of V4 cells. V4 receptive field dynamics can be observed after pooling the gain modulated responses to obtain a certain degree of spatial invariance. The time course of the receptive field dynamics in the model resemble those obtained from macaque V4.

Saccades and shifting receptive fields: anticipating consequences or selecting targets?

Saccadic eye movements cause frequent and substantial displacements of the retinal image, but those displacements go unnoticed. It has been widely assumed that this perceived stability emerges from the shifting of visual receptive fields from their current, presaccadic locations to their future, postsaccadic locations in anticipation of the retinal consequences of saccades. Although evidence consistent with this anticipatory remapping has accumulated over the years, more recent work suggests an alternative view. In this opinion article, we examine the evidence of presaccadic receptive field shifts and their relationship to the perceptual changes that accompany saccades. We argue that both reflect the selection of targets for saccades rather than the anticipation of a displaced retinal image.

Computational models of spatial updating in peri-saccadic perception

Perceptual phenomena that occur around the time of a saccade, such as peri-saccadic mislocalization or saccadic suppression of displacement, have often been linked to mechanisms of spatial stability. These phenomena are usually regarded as errors in processes of trans-saccadic spatial transformations and they provide important tools to study these processes. However, a true understanding of the underlying brain processes that participate in the preparation for a saccade and in the transfer of information across it requires a closer, more quantitative approach that links different perceptual phenomena with each other and with the functional requirements of ensuring spatial stability. We review a number of computational models of peri-saccadic spatial perception that provide steps in that direction. Although most models are concerned with only specific phenomena, some generalization and interconnection between them can be obtained from a comparison. Our analysis shows how different perceptual effects can coherently be brought together and linked back to neuronal mechanisms on the way to explaining vision across saccades.

Neural Mechanisms of Selective Visual Attention.

Selective visual attention describes the tendency of visual processing to be confined largely to stimuli that are relevant to behavior. It is among the most fundamental of cognitive functions, particularly in humans and other primates for whom vision is the dominant sense. We review recent progress in identifying the neural mechanisms of selective visual attention. We discuss evidence from studies of different varieties of selective attention and examine how these varieties alter the processing of stimuli by neurons within the visual system, current knowledge of their causal basis, and methods for assessing attentional dysfunctions. In addition, we identify some key questions that remain in identifying the neural mechanisms that give rise to the selective processing of visual information.

The spatial distribution of receptive field changes in a model of peri-saccadic perception: predictive remapping and shifts towards the saccade target.

At the time of an impending saccade receptive fields (RFs) undergo dynamic changes, that is, their spatial profile is altered. This phenomenon has been observed in several monkey visual areas. Although their link to eye movements is obvious, neither the exact pattern nor their function is fully clear. Several RF shifts have been interpreted in terms of predictive remapping mediating visual stability. In particular, even prior to saccade onset some cells become responsive to stimuli presented in their future, post-saccadic RF. In visual area V4, however, the overall effect of RF dynamics consists of a shrinkage and shift of RFs towards the saccade target. These observations have been linked to a pre-saccadically enhanced processing of the future fixation. In order to better understand these seemingly different outcomes, we analyzed the RF shifts predicted by a recently proposed computational model of peri-saccadic perception (Hamker, Zirnsak, Calow, & Lappe, 2008). This model unifies peri-saccadic compression, pre-saccadic attention shifts, and peri-saccadic receptive field dynamics in a common framework of oculomotor reentry signals in extrastriate visual cortical maps. According to the simulations that we present in the current paper, a spatially selective oculomotor feedback signal leads to RF dynamics which are both consistent with the observations made in studies aiming to investigate predictive remapping and saccade target shifts. Thus, the seemingly distinct experimental observations could be grounded in the same neural mechanism leading to different RF dynamics dependent on the location of the RF in visual space.

Split of spatial attention as predicted by a systems-level model of visual attention

Can we attend to multiple distinct spatial locations at the same time? According to a recent psychophysical study [J. Dubois et al. (2009)Journal of Vision, 9, 3.1–11] such a split of spatial attention might be limited to short periods of time. Following N. P. Bichot et al. [(1999)Perception & Psychophysics, 61, 403–423] subjects had to report the identity of multiple letters that were briefly presented at different locations, while two of these locations (targets) were relevant for a concurrent shape comparison task. In addition to the design used by Bichot et al. stimulus onset asynchrony between shape onset and letters was systematically varied. In general, the performance of subjects was superior at target locations. Furthermore, for short stimulus onset asynchronies, performance was simultaneously increasing at both target locations. For longer stimulus onset asynchronies, however, performance deteriorated at one of the target locations while increasing at the other target location. It was hypothesized that this dynamic deployment of attention might be caused by competitive processes in saccade‐related structures such as the frontal eye field. Here we simulated the task of Dubois et al. using a systems‐level model of attention. Our results are consistent with recent findings in the frontal eye field obtained during covert visual search, and they support the view of a transient deployment of spatial attention to multiple stimuli in the early epoch of target selection.

Anticipatory Saccade Target Processing and the Presaccadic Transfer of Visual Features

As we shift our gaze to explore the visual world, information enters cortex in a sequence of successive snapshots, interrupted by phases of blur. Our experience, in contrast, appears like a movie of a continuous stream of objects embedded in a stable world. This perception of stability across eye movements has been linked to changes in spatial sensitivity of visual neurons anticipating the upcoming saccade, often referred to as shifting receptive fields (Duhamel et al., 1992; Walker et al., 1995; Umeno and Goldberg, 1997; Nakamura and Colby, 2002). How exactly these receptive field dynamics contribute to perceptual stability is currently not clear. Anticipatory receptive field shifts toward the future, postsaccadic position may bridge the transient perisaccadic epoch (Sommer and Wurtz, 2006; Wurtz, 2008; Melcher and Colby, 2008). Alternatively, a presaccadic shift of receptive fields toward the saccade target area (Tolias et al., 2001) may serve to focus visual resources onto the most relevant objects in the postsaccadic scene (Hamker et al., 2008). In this view, shifts of feature detectors serve to facilitate the processing of the peripheral visual content before it is foveated. While this conception is consistent with previous observations on receptive field dynamics and on perisaccadic compression (Ross et al., 1997; Morrone et al., 1997; Kaiser and Lappe, 2004), it predicts that receptive fields beyond the saccade target shift toward the saccade target rather than in the direction of the saccade. We have tested this prediction in human observers via the presaccadic transfer of the tilt-aftereffect (Melcher, 2007).