Cortical mechanisms for trans-saccadic memory and integration of multiple object features

Constructing an internal representation of the world from successive visual fixations, i.e. separated by saccadic eye movements, is known as trans-saccadic perception. Research on trans-saccadic perception (TSP) has been traditionally aimed at resolving the problems of memory capacity and visual integration across saccades. In this paper, we review this literature on TSP with a focus on research showing that egocentric measures of the saccadic eye movement can be used to integrate simple object features across saccades, and that the memory capacity for items retained across saccades, like visual working memory, is restricted to about three to four items. We also review recent transcranial magnetic stimulation experiments which suggest that the right parietal eye field and frontal eye fields play a key functional role in spatial updating of objects in TSP. We conclude by speculating on possible cortical mechanisms for governing egocentric spatial updating of multiple objects in TSP.     

Saccadic motor planning by integrating visual information and pre-information on neural dynamic fields

A functional model of target selection in the saccadic system is presented, incorporating elements of visual processing, motor planning, and motor control. We address the integration of visual information with pre-information. which is provided by manipulating the probability that a target appears at a certain location. This integration is achieved within a dynamic representation of planned eye movement which is modeled through distributions of activation on a topographic field. Visual input evokes activation, which is also constrained by lateral interaction within the field and by preshaping input representing pre-information. The model describes target selection observable in paradigms in which visual goals are presented at more than one location. Specifically, we model the transition from averaging, where endpoints of first saccades fall between two visual target locations, to decision making, where endpoints of first saccades fall accurately onto one of two simultaneously presented visual targets. We make predictions about how metrical biases of first saccades are induced by pre-information about target locations acquired by learning. When coupled to a motor control stage, activation dynamics on the planning level contribute to stabilizing gaze under fixation conditions. The neurophysiological relevance of our functional model is discussed.     

Source of the eye-movement signal reaching real-motion cells

The stability of visual perception despite eye movements suggests the existence in the visual system of neurons able to recognize whether the movement of a retinal image is due to the actual movement of an object or is self-induced by the ocular movement. We found neurons of this type in several areas of the monkey visual cortex and named them "real-motion" cells. Extracellular recordings were carried out from single neurons of the cortical prestriate area V3A of two awake macaque monkeys. Eighty-seven neurons were studied by comparing their responses during stimulus movement across the stationary receptive field, and receptive-field movement across the stationary stimulus. This visual stimulation was presented against a uniform visual background, in darkness or against a textured background. Neurons which were not real-motion in light (45/87) maintained their behaviour in darkness, while about 40% of real-motion cells lost this behaviour in darkness. Both real-motion and non real-motion cells maintained the same behaviour when tested against a uniform or textured visual background but often, texture increased the difference in the response that real-motion cells showed between stimulus and eye movement. These data suggest that the eye-movement signal which reaches real-motion cells and is responsible for their behaviour may be either retinal or extraretinal in nature. This double innervation is in good agreement with perceptual phenomena related to the detection of movement in the visual field.     

Causal Inference for Spatial Constancy across Saccades

Our ability to interact with the environment hinges on creating a stable visual world despite the continuous changes in retinal input. To achieve visual stability, the brain must distinguish the retinal image shifts caused by eye movements and shifts due to movements of the visual scene. This process appears not to be flawless: during saccades, we often fail to detect whether visual objects remain stable or move, which is called saccadic suppression of displacement (SSD). How does the brain evaluate the memorized information of the presaccadic scene and the actual visual feedback of the postsaccadic visual scene in the computations for visual stability? Using a SSD task, we test how participants localize the presaccadic position of the fixation target, the saccade target or a peripheral non-foveated target that was displaced parallel or orthogonal during a horizontal saccade, and subsequently viewed for three different durations. Results showed different localization errors of the three targets, depending on the viewing time of the postsaccadic stimulus and its spatial separation from the presaccadic location. We modeled the data through a Bayesian causal inference mechanism, in which at the trial level an optimal mixing of two possible strategies, integration vs. separation of the presaccadic memory and the postsaccadic sensory signals, is applied. Fits of this model generally outperformed other plausible decision strategies for producing SSD. Our findings suggest that humans exploit a Bayesian inference process with two causal structures to mediate visual stability.     

Different programming modes of human saccadic eye movements as a function of stimulus eccentricity: Indications of a functional subdivision of the visual field

1. Voluntary saccadic eye movements were made toward flashes of light on the horizontal meridian, whose duration and distance from the point of fixation were varied; eye movements were measured using d.c.-electrooculography.—2. Targets within 10°–15° eccentricity are usually reached by one saccadic eye movement. When the eyes turn toward targets of more than 10°–15° eccentricity, the first saccadic eye movement falls short of the target by an angle usually not exceeding 10°. The presence of the image of the target off the fovea (visual error signal) subsequent to such an undershoot elicits, after a short interval, corrective saccades (usually one) which place the image of the target on the fovea. In the absence of a visual error signal, the probability of occurrence of corrective saccades is low, but it increases with greater target eccentricities. These observations suggest that there are different, eccentricity-dependent modes of programming saccadic eye movements.—3. Saccadic eye movements appear to be programmed in retinal coordinates. This conclusion is based on the observations that, irrespective of the initial position of the eyes in the orbit, a) there are different programming modes for eye movements to targets within and beyond 10°–15° from the fixation point, and b_ the maximum velocity of saccadic eye movements is always reached at 25° to 30° target eccentricity. —4. Distributions of latency and intersaccadic interval (ISI) are frequently multimodal, with a separation between modes of 30 to 40 msec. These observations suggest that saccadic eye movements are produced by mechanisms which, at a frequency of 30 Hz, process visual information. —5. Corrective saccades may occur after extremely short intervals (30 to 60 msec) regardless of whether or not a visual error signal is present; the eyes may not even come to a complete stop during these very short intersaccadic intervals. It is suggested that these corrective saccades are triggered by errors in the programming of the initial saccadic eye movements, and not by a visual error signal. —6. The exitence of different, eccentricity-dependent programming modes of saccadic eye movements, is further supported by anatomical, physiological, psychophysical, and neuropathological observations that suggest a dissociation of visual functions dependent on retinal eccentricity. Saccadic eye movements to targets more eccentric than 10°–15° appear to be executed by a mechanism involving the superior colliculus (perhaps independent of the visual cortex), whereas saccadic eye movements to less eccentric targets appear to depend on a mechanism involving the geniculo-cortical pathway (perhaps in collaboration with the superior colliculus).     

Perisaccadic Remapping and Rescaling of Visual Responses in Macaque Superior Colliculus

Visual neurons have spatial receptive fields that encode the positions of objects relative to the fovea. Because foveate animals execute frequent saccadic eye movements, this position information is constantly changing, even though the visual world is generally stationary. Interestingly, visual receptive fields in many brain regions have been found to exhibit changes in strength, size, or position around the time of each saccade, and these changes have often been suggested to be involved in the maintenance of perceptual stability. Crucial to the circuitry underlying perisaccadic changes in visual receptive fields is the superior colliculus (SC), a brainstem structure responsible for integrating visual and oculomotor signals. In this work we have studied the time-course of receptive field changes in the SC. We find that the distribution of the latencies of SC responses to stimuli placed outside the fixation receptive field is bimodal: The first mode is comprised of early responses that are temporally locked to the onset of the visual probe stimulus and stronger for probes placed closer to the classical receptive field. We suggest that such responses are therefore consistent with a perisaccadic rescaling, or enhancement, of weak visual responses within a fixed spatial receptive field. The second mode is more similar to the remapping that has been reported in the cortex, as responses are time-locked to saccade onset and stronger for stimuli placed in the postsaccadic receptive field location. We suggest that these two temporal phases of spatial updating may represent different sources of input to the SC.     

Visuomotor origins of covert spatial attention

Covert spatial attention produces biases in perceptual performance and neural processing of behaviorally relevant stimuli in the absence of overt orienting movements. The neural mechanism that gives rise to these effects is poorly understood. This paper surveys past evidence of a relationship between oculomotor control and visual spatial attention and more recent evidence of a causal link between the control of saccadic eye movements by frontal cortex and covert visual selection. Both suggest that the mechanism of covert spatial attention emerges as a consequence of the reciprocal interactions between neural circuits primarily involved in specifying the visual properties of potential targets and those involved in specifying the movements needed to fixate them.     

Perisaccadic mislocalization orthogonal to saccade direction

Saccadic eye movements transiently distort perceptual space. Visual objects flashed shortly before or during a saccade are mislocalized along the saccade direction, resembling a compression of space around the saccade target. These mislocalizations reflect transient errors of processes that construct spatial stability across eye movements. They may arise from errors of reference signals associated with saccade direction and amplitude or from visual or visuomotor remapping processes focused on the saccade target's position. The second case would predict apparent position shifts toward the target also in directions orthogonal to the saccade. We report that such orthogonal mislocalization indeed occurs. Surprisingly, however, the orthogonal mislocalization is restricted to only part of the visual field. This part comprises distant positions in saccade direction but does not depend on the target's position. Our findings can be explained by a combination of directional and positional reference signals that varies in time course across the visual field.     

Saccadic facilitation in natural backgrounds

In visual systems with a fovea, only a small portion of the visual field can be analyzed with high accuracy. Saccadic eye movements shift that center of gaze around several times a second. Saccades have been characterized in great detail and depend critically on a number of visual properties of the stimuli. However, typical experiments have used bright spots on dark backgrounds, while our natural environment has a highly characteristic rich spatial structure. Here we show that the saccadic system, unlike the perceptual system, is able to compensate for the masking caused by structured backgrounds. Consequently, saccadic latencies in the context of natural backgrounds are much faster than unstructured backgrounds at equal levels of visibility. The results suggest that whenever a structured background acts to mask the visibility of the saccade target, it simultaneously preactivates saccadic circuitry and thus ensures a fast reaction to potentially critical stimuli that are difficult to detect in our environment.     

Fooling the Eyes: The Influence of a Sound-Induced Visual Motion Illusion on Eye Movements

The question of whether perceptual illusions influence eye movements is critical for the long-standing debate regarding the separation between action and perception. To test the role of auditory context on a visual illusion and on eye movements, we took advantage of the fact that the presence of an auditory cue can successfully modulate illusory motion perception of an otherwise static flickering object (sound-induced visual motion effect). We found that illusory motion perception modulated by an auditory context consistently affected saccadic eye movements. Specifically, the landing positions of saccades performed towards flickering static bars in the periphery were biased in the direction of illusory motion. Moreover, the magnitude of this bias was strongly correlated with the effect size of the perceptual illusion. These results show that both an audio-visual and a purely visual illusion can significantly affect visuo-motor behavior. Our findings are consistent with arguments for a tight link between perception and action in localization tasks.     

Investigation of the visual cytoscreening of conventional gynecologic smears. II. Analysis of eye movement

The perception of visual information in cytoscreening was studied: eye movements were recorded while the cytotechnologist was screening cervical smears by means of a projection screen. Four phases of eye movement could be distinguished: small, aimless movements during the stage movement; a latency period with a duration of about 180 milliseconds; saccadic movement to the position of an object; and fixation on an object. These components explain the two-phase behavior of cytoscreening found in our previous investigations of the stage movement. Visual perception during the period of latency was found to be the most important since only those objects that are recognized by peripheral vision during this period can trigger the necessary saccadic movement before fixation takes place. The scanpath of search in the stationary field of view is determined by the conspicuousness of the objects; the main features of conspicuousness are size and contrast. Even with the comparatively small fields of view (24 degrees and 29 degrees in diameter) used in these experiments, it was found that the detection threshold of peripheral vision increases towards the margin of the field of view. This raises the question of whether the use of large-field binoculars (with 40-degree visual angles) may cause higher false-negative rates for samples with only a few atypical cells.     

A motion illusion reveals mechanisms of perceptual stabilization

Visual illusions are valuable tools for the scientific examination of the mechanisms underlying perception. In the peripheral drift illusion special drift patterns appear to move although they are static. During fixation small involuntary eye movements generate retinal image slips which need to be suppressed for stable perception. Here we show that the peripheral drift illusion reveals the mechanisms of perceptual stabilization associated with these micromovements. In a series of experiments we found that illusory motion was only observed in the peripheral visual field. The strength of illusory motion varied with the degree of micromovements. However, drift patterns presented in the central (but not the peripheral) visual field modulated the strength of illusory peripheral motion. Moreover, although central drift patterns were not perceived as moving, they elicited illusory motion of neutral peripheral patterns. Central drift patterns modulated illusory peripheral motion even when micromovements remained constant. Interestingly, perceptual stabilization was only affected by static drift patterns, but not by real motion signals. Our findings suggest that perceptual instabilities caused by fixational eye movements are corrected by a mechanism that relies on visual rather than extraretinal (proprioceptive or motor) signals, and that drift patterns systematically bias this compensatory mechanism. These mechanisms may be revealed by utilizing static visual patterns that give rise to the peripheral drift illusion, but remain undetected with other patterns. Accordingly, the peripheral drift illusion is of unique value for examining processes of perceptual stabilization.     

Human areas V3A and V6 compensate for self-induced planar visual motion

Little is known about mechanisms mediating a stable perception of the world during pursuit eye movements. Here, we used fMRI to determine to what extent human motion-responsive areas integrate planar retinal motion with nonretinal eye movement signals in order to discard self-induced planar retinal motion and to respond to objective ("real") motion. In?contrast to other areas, V3A lacked responses to?self-induced planar retinal motion but responded strongly to head-centered motion, even when retinally canceled by pursuit. This indicates a near-complete multimodal integration of visual with nonvisual planar motion signals in V3A. V3A could be mapped selectively and robustly in every single subject on this basis. V6 also reported head-centered planar motion, even when 3D flow was added to it, but was suppressed by retinal planar motion. These findings suggest a dominant contribution of human areas V3A and V6 to head-centered motion perception and to perceptual stability during eye movements.     

Evidence for the lateral intraparietal area as the parietal eye field.

It has long been appreciated that the posterior parietal cortex plays a role in the processing of saccadic eye movements. Only recently has it been discovered that a small cortical area, the lateral intraparietal area, within this much larger area appears to be specialized for saccadic eye movements. Unlike other cortical areas in the posterior parietal cortex, the lateral intraparietal area has strong anatomical connections to other saccade centers, and its cells have saccade-related responses that begin before the saccades. The lateral intraparietal area appears to be neither a strictly visual nor strictly motor structure; rather it performs visuomotor integration functions including determining the spatial location of saccade targets and forming plans to make eye movements.     

Visual computation and saccadic eye movements: a theoretical perspective

A simple instance of parallel computation in neural networks occurs when the eye orients to a novel visual target. Consideration of target-elicited saccadic eye movements opens the question of how spatial position is represented in the visual pathways involved in this response. It is argued that a point-for-point retinotopic coding of spatial position (the 'local sign' approach) is inadequate to account for the characteristics of the response. An alternative approach based on distributed coding is developed.     

Eye movements modulate visual receptive fields of V4 neurons

The receptive field, defined as the spatiotemporal selectivity of neurons to sensory stimuli, is central to our understanding of the neuronal mechanisms of perception. However, despite the fact that eye movements are critical during normal vision, the influence of eye movements on the structure of receptive fields has never been characterized. Here, we map the receptive fields of macaque area V4 neurons during saccadic eye movements and find that receptive fields are remarkably dynamic. Specifically, before the initiation of a saccadic eye movement, receptive fields shrink and shift towards the saccade target. These spatiotemporal dynamics may enhance information processing of relevant stimuli during the scanning of a visual scene, thereby assisting the selection of saccade targets and accelerating the analysis of the visual scene during free viewing.     

The Pupillary Light Response Reveals the Focus of Covert Visual Attention

The pupillary light response is often assumed to be a reflex that is not susceptible to cognitive influences. In line with recent converging evidence, we show that this reflexive view is incomplete, and that the pupillary light response is modulated by covert visual attention: Covertly attending to a bright area causes a pupillary constriction, relative to attending to a dark area under identical visual input. This attention-related modulation of the pupillary light response predicts cuing effects in behavior, and can be used as an index of how strongly participants attend to a particular location. Therefore, we suggest that pupil size may offer a new way to continuously track the focus of covert visual attention, without requiring a manual response from the participant. The theoretical implication of this finding is that the pupillary light response is neither fully reflexive, nor under complete voluntary control, but is instead best characterized as a stereotyped response to a voluntarily selected target. In this sense, the pupillary light response is similar to saccadic and smooth pursuit eye movements. Together, eye movements and the pupillary light response maximize visual acuity, stabilize visual input, and selectively filter visual information as it enters the eye.     

Cortical Contributions to Saccadic Suppression

The stability of visual perception is partly maintained by saccadic suppression: the selective reduction of visual sensitivity that accompanies rapid eye movements. The neural mechanisms responsible for this reduced perisaccadic visibility remain unknown, but the Lateral Geniculate Nucleus (LGN) has been proposed as a likely site. Our data show, however, that the saccadic suppression of a target flashed in the right visual hemifield increased with an increase in background luminance in the left visual hemifield. Because each LGN only receives retinal input from a single hemifield, this hemifield interaction cannot be explained solely on the basis of neural mechanisms operating in the LGN. Instead, this suggests that saccadic suppression must involve processing in higher level cortical areas that have access to a considerable part of the ipsilateral hemifield.     

Motor-related signals support localization invariance for stable visual perception

Our ability to perceive a stable visual world in the presence of continuous movements of the body, head, and eyes has puzzled researchers in the neuroscience field for a long time. We reformulated this problem in the context of hierarchical convolutional neural networks (CNNs)—whose architectures have been inspired by the hierarchical signal processing of the mammalian visual system—and examined perceptual stability as an optimization process that identifies image-defining features for accurate image classification in the presence of movements. Movement signals, multiplexed with visual inputs along overlapping convolutional layers, aided classification invariance of shifted images by making the classification faster to learn and more robust relative to input noise. Classification invariance was reflected in activity manifolds associated with image categories emerging in late CNN layers and with network units acquiring movement-associated activity modulations as observed experimentally during saccadic eye movements. Our findings provide a computational framework that unifies a multitude of biological observations on perceptual stability under optimality principles for image classification in artificial neural networks.     

Error Correcting Mechanisms during Antisaccades: Contribution of Online Control during Primary Saccades and Offline Control via Secondary Saccades

Errors in eye movements can be corrected during the ongoing saccade through in-flight modifications (i.e., online control), or by programming a secondary eye movement (i.e., offline control). In a reflexive saccade task, the oculomotor system can use extraretinal information (i.e., efference copy) online to correct errors in the primary saccade, and offline retinal information to generate a secondary corrective saccade. The purpose of this study was to examine the error correction mechanisms in the antisaccade task. The roles of extraretinal and retinal feedback in maintaining eye movement accuracy were investigated by presenting visual feedback at the spatial goal of the antisaccade. We found that online control for antisaccade is not affected by the presence of visual feedback; that is whether visual feedback is present or not, the duration of the deceleration interval was extended and significantly correlated with reduced antisaccade endpoint error. We postulate that the extended duration of deceleration is a feature of online control during volitional saccades to improve their endpoint accuracy. We found that secondary saccades were generated more frequently in the antisaccade task compared to the reflexive saccade task. Furthermore, we found evidence for a greater contribution from extraretinal sources of feedback in programming the secondary “corrective” saccades in the antisaccade task. Nonetheless, secondary saccades were more corrective for the remaining antisaccade amplitude error in the presence of visual feedback of the target. Taken together, our results reveal a distinctive online error control strategy through an extension of the deceleration interval in the antisaccade task. Target feedback does not improve online control, rather it improves the accuracy of secondary saccades in the antisaccade task.