Real Saccades Research Articles

Neural substrates for saccadic modulation of visual representations in mouse superior colliculus.

How do sensory systems account for stimuli generated by natural behavior? We addressed this question by examining how an ethologically relevant class of saccades modulates visual representations in the mouse superior colliculus (SC), a key region for sensorimotor integration. We quantified saccadic modulation by recording SC responses to visual probes presented at stochastic saccade-probe latencies. Saccades significantly impacted population representations of the probes, with early enhancement that began prior to saccades and pronounced suppression for several hundred milliseconds following saccades, independent of units' visual response properties or directional tuning. To determine the cause of saccadic modulation, we presented fictive saccades that simulated the visual experience during saccades without motor output. Some units exhibited similar modulation by fictive and real saccades, suggesting a sensory-driven origin of saccadic modulation, while others had dissimilar modulation, indicating a motor contribution. These findings advance our understanding of the neural basis of natural visual coding.

Probing correlates of saccadic suppression in the primate superior colliculus and primary visual cortex using simulated and real saccades

Probing correlates of saccadic suppression in the primate superior colliculus and primary visual cortex using simulated and real saccades

Perceptual enhancement and suppression correlate with V1 neural activity during active sensing

Perception in multiple sensory modalities is an active process that involves exploratory behaviors. In humans and other primates, vision results from sensory sampling guided by saccadic eye movements. Saccades are known to modulate visual perception, and a corollary discharge signal associated with saccades appears to establish a sense of visual stability. Neural recordings have shown that saccades also modulate activity widely across the brain. To investigate the neural basis of saccadic effects on perception, simultaneous recordings from multiple neurons in area V1 were made as animals performed a contrast detection task. Perceptual and neural measures were compared when the animal made real saccades that brought a stimulus into V1 receptive fields and when simulated saccades were made (identical retinal stimulation but no eye movement). When real saccades were made and low spatial frequency stimuli were presented, we observed a reduction in both perceptual sensitivity and neural activity compared with simulated saccades; conversely, with higher spatial frequency stimuli, saccades increased visual sensitivity and neural activity. The performance of neural decoders, which used the activity of the population of simultaneously recorded neurons, showed saccade effects on sensitivity that mirrored the frequency-dependent perceptual changes, suggesting that the V1 population activity could support the perceptual effects. A minority of V1 neurons had significant choice probabilities, and the saccades decreased both average choice probability and pairwise noise correlations. Taken together, the findings suggest that a signal related to saccadic eye movements alters V1 spiking to increase the independence of spiking neurons and bias the system toward processing higher spatial frequencies, presumably to enhance object recognition. The effects of saccades on visual perception and noise correlations appear to parallel effects observed in other sensory modalities, suggesting a general principle of active sensory processing.

Dependence of perceptual saccadic suppression on peri-saccadic image flow properties and luminance contrast polarity

Perceptual detectability of brief visual stimuli is strongly diminished across saccades. Recent work showed that this perceptual suppression phenomenon is jumpstarted in the retina (Idrees et al., 2020), suggesting that the phenomenon might be significantly more visual in nature than normally acknowledged. Here, we explored the details of visual-visual interactions underlying saccadic suppression, and we did so by comparing suppression strength when saccades were made across a uniform image of constant luminance versus when saccades were made across image patches of different luminance, width, and trans-saccadic luminance polarity. In 6 human subjects, we measured perceptual contrast thresholds for brief peri-saccadic flashes of positive (luminance increments) or negative (luminance decrements) polarity. In different conditions, gaze crossed a luminance edge or stripe before landing on a uniform background like in the control condition. Perceptual thresholds were >6-7 times higher when saccades translated a luminance stripe or edge across the retina than when the movements were made over a completely uniform image patch. Moreover, both background luminance and flash luminance polarity relative to the background strongly modulated peri-saccadic contrast thresholds: dark backgrounds were associated with the strongest suppression, and negative polarity flashes over dark backgrounds caused stronger suppression than positive polarity flashes over the same backgrounds. Most importantly, we repeated the same experiments on all subjects with rapid image translations (simulating saccadic visual flows on the retina) without any real saccades. All of the image dependencies that we observed with real saccades (e.g. suppression with gaze crossing an edge or stripe versus suppression with a uniform background) also occurred. Our results indicate that perceptual saccadic suppression may be fundamentally a visual phenomenon. They also strongly motivate revisiting both the movement-related and visual components of saccadic suppression, and investigating how saccade movement commands may interact with visual-visual interactions in shaping trans-saccadic visual perception.

Detection of normal and slow saccades using implicit piecewise polynomial approximation.

The quantitative analysis of saccades in eye movement data unveils information associated with intention, cognition, and health status. Abnormally slow saccades are indicative of neurological disorders and often imply a specific pathological disturbance. However, conventional saccade detection algorithms are not designed to detect slow saccades, and are correspondingly unreliable when saccades are unusually slow. In this article, we propose an algorithm that is effective for the detection of both normal and slow saccades. The proposed algorithm is partly based on modeling saccadic waveforms as piecewise-quadratic signals. The algorithm first decreases noise in acquired eye-tracking data using optimization to minimize a prescribed objective function, then uses velocity thresholding to detect saccades. Using both simulated saccades and real saccades generated by healthy subjects and patients, we evaluate the performance of the proposed algorithm and 10 other detection algorithms. We show the proposed algorithm is more accurate in detecting both normal and slow saccades than other algorithms.

The effect of sampling rate and lowpass filters on saccades - A modeling approach.

The study of eye movements has become popular in many fields of science. However, using the preprocessed output of an eye tracker without scrutiny can lead to low-quality or even erroneous data. For example, the sampling rate of the eye tracker influences saccadic peak velocity, while inadequate filters fail to suppress noise or introduce artifacts. Despite previously published guiding values, most filter choices still seem motivated by a trial-and-error approach, and a thorough analysis of filter effects is missing. Therefore, we developed a simple and easy-to-use saccade model that incorporates measured amplitude-velocity main sequences and produces saccades with a similar frequency content to real saccades. We also derived a velocity divergence measure to rate deviations between velocity profiles. In total, we simulated 155 saccades ranging from 0.5° to 60° and subjected them to different sampling rates, noise compositions, and various filter settings. The final goal was to compile a list with the best filter settings for each of these conditions. Replicating previous findings, we observed reduced peak velocities at lower sampling rates. However, this effect was highly non-linear over amplitudes and increasingly stronger for smaller saccades. Interpolating the data to a higher sampling rate significantly reduced this effect. We hope that our model and the velocity divergence measure will be used to provide a quickly accessible ground truth without the need for recording and manually labeling saccades. The comprehensive list of filters allows one to choose the correct filter for analyzing saccade data without resorting to trial-and-error methods.

Saccade-induced image motion cannot account for post-saccadic enhancement of visual processing in primate MST.

Primates use saccadic eye movements to make gaze changes. In many visual areas, including the dorsal medial superior temporal area (MSTd) of macaques, neural responses to visual stimuli are reduced during saccades but enhanced afterwards. How does this enhancement arise—from an internal mechanism associated with saccade generation or through visual mechanisms activated by the saccade sweeping the image of the visual scene across the retina? Spontaneous activity in MSTd is elevated even after saccades made in darkness, suggesting a central mechanism for post-saccadic enhancement. However, based on the timing of this effect, it may arise from a different mechanism than occurs in normal vision. Like neural responses in MSTd, initial ocular following eye speed is enhanced after saccades, with evidence suggesting both internal and visually mediated mechanisms. Here we recorded from visual neurons in MSTd and measured responses to motion stimuli presented soon after saccades and soon after simulated saccades—saccade-like displacements of the background image during fixation. We found that neural responses in MSTd were enhanced when preceded by real saccades but not when preceded by simulated saccades. Furthermore, we also observed enhancement following real saccades made across a blank screen that generated no motion signal within the recorded neurons' receptive fields. We conclude that in MSTd the mechanism leading to post-saccadic enhancement has internal origins.

Estimating peak velocity of rapid eye movements from video recordings

Although video offers many advantages for recording human eye orientation, it involves such low temporal resolution (60 Hz) that it seems an unpromising method for evaluating the dynamics of rapid (saccadic) eye movements. This study demonstrates, nevertheless, that such measurements can provide surprisingly reliable estimates of the peak velocity of larger saccades. Simulations of 60-Hz sampling of eye position during idealized saccades provided replicated estimates of “apparent peak velocity.” The results indicate that when saccadic amplitude is about 10° or larger, estimates of peak velocity would on average be biased downward by less than 10%, with standard deviations due to measurement timing of less than 5%. Experimental data (from recordings of 10° and 20° saccades with customized video) demonstrate that these theoretical sources of uncertainty are considerably smaller than the trialto- trial variability in performance of real saccades. Reliability of video recording, however, rapidly deteriorates when saccades become smaller than about 10°.

Open-loop simulations of the primate saccadic system using burst cell discharge from the superior colliculus.

Saccade-related burst neurons (SRBNs) in the monkey superior colliculus (SC) have been hypothesized to provide the brainstem saccadic burst generator with the dynamic error signal and the movement initiating trigger signal. To test this claim, we performed two sets of open-loop simulations on a burst generator model with the local feedback disconnected using experimentally obtained SRBN activity as both the driving and trigger signal inputs to the model. First, using neural data obtained from cells located near the middle of the rostral to caudal extent of the SC, the internal parameters of the model were optimized by means of a stochastic hill-climbing algorithm to produce an intermediate-sized saccade. The parameter values obtained from the optimization were then fixed and additional simulations were done using the experimental data from rostral collicular neurons (small saccades) and from more caudal neurons (large saccades); the model generated realistic saccades, matching both position and velocity profiles of real saccades to the centers of the movement fields of all these cells. Second, the model was driven by SRBN activity affiliated with interrupted saccades, the resumed eye movements observed following electrical stimulation of the omnipause region. Once again, the model produced eye movements that closely resembled the interrupted saccades produced by such simulations, but minor readjustment of parameters reflecting the weight of the projection of the trigger signal was required. Our study demonstrates that a model of the burst generator produces reasonably realistic saccades when driven with actual samples of SRBN discharges.

Short latency ocular-following responses in man

The ocular-following responses elicited by brief unexpected movements of the visual scene were studied in human subjects. Response latencies varied with the type of stimulus and decreased systematically with increasing stimulus speed but, unlike those of monkeys, were not solely determined by the temporal frequency generated by sine-wave stimuli. Minimum latencies (70-75 ms) were considerably shorter than those reported for other visually driven eye movements. The magnitude of the responses to sine-wave stimuli changed markedly with stimulus speed and only slightly with spatial frequency over the ranges used. When normalized with respect to spatial frequency, all responses shared the same dependence on temporal frequency (band-pass characteristics with a peak at 16 Hz), indicating that temporal frequency, rather than speed per se, was the limiting factor over the entire range examined. This suggests that the underlying motion detectors respond to the local changes in luminance associated with the motion of the scene. Movements of the scene in the immediate wake of a saccadic eye movement were on average twice as effective as movements 600 ms later: post-saccadic enhancement. Less enhancement was seen in the wake of saccade-like shifts of the scene, which themselves elicited weak ocular following, something not seen in the wake of real saccades. We suggest that there are central mechanisms that, on the one hand, prevent the ocular-following system from tracking the visual disturbances created by saccades but, on the other, promote tracking of any subsequent disturbance and thereby help to suppress post-saccadic drift. Partitioning the visual scene into central and peripheral regions revealed that motion in the periphery can exert a weak modulatory influence on ocular-following responses resulting from motion at the center. We suggest that this may help the moving observer to stabilize his/her eyes on nearby stationary objects.

Short-latency ocular following responses of monkey. II. Dependence on a prior saccadic eye movement.

The ocular following responses elicited by brief unexpected movements of the visual scene were studied in eight rhesus monkeys. Test patterns were random dots except in one experiment when sine-wave gratings were used. Test stimuli were velocity steps of 100-ms duration applied after spontaneous saccades. Two response measures were used: the initial peak in the eye velocity profile (ei), and the average final eye velocity over the period of 110-140 ms measured from stimulus onset (ef). Responses were best when the test ramps began soon after saccades and attenuated progressively as the postsaccadic delay interval was increased: postsaccadic enhancement of ocular following. The decline in ei was roughly exponential: average time constant, 60 ms; average asymptote, 22%. Later measures (ef) were generally less affected. We suggest that this transient enhancement aids the visual suppression of postsaccadic ocular drifts (glissades) and the tracking of moving images newly acquired with a saccade. The magnitude of the postsaccadic enhancement was dependent on the amount of retinal stimulation during the antecedent saccade; when this stimulation was compromised, as when a vertical saccade was made while viewing a grating pattern with vertically oriented stripes, subsequent enhancement of ocular following was much reduced. Further, saccade-like conditioning movements of the visual scene resulted in an enhancement of the ocular following, elicited by subsequent test ramps, that was similar in magnitude and time course to that in the wake of real saccades. We conclude that the postsaccadic enhancement of ocular following is largely due to the visual stimulation produced by the saccade sweeping the scene across the retina. Data obtained with the visual field partitioned into central and peripheral regions (center 20-60 degrees diam) and with gaze centered suggested that the short-latency ocular following system and the enhancement mechanism that modulates it both receive their major inputs from the central 40 degrees of the retina. Further, when this central region was partitioned, enhancement was obtained only when the conditioning and test stimuli were presented to the same region of retina. Visual enhancement showed only weak interocular transfer: the conditioning and test stimuli had to be seen by the same eye to produce appreciable enhancement. These data suggest that the enhancement involves local spatial interactions at an "early" point in the visual pathway before the inputs from the two eyes have converged. When the conditioning and test stimuli impinged on different regions of the retina, brief powerful suppression of ocular following was obtained.(ABSTRACT TRUNCATED AT 400 WORDS)

Backward and forward masking associated with saccadic eye movement.

Visual masking effects on test flash thresholds were measured under real and simulated eye movement conditions to determine whether visual masking is primarily responsible for elevations in threshold that are sometimes associated with saccadic eye movements. Brief luminous flashes presented to the central retina before, during, and after saccades were masked by stimuli presented either pre- or postsaccadically. The amount and time course of masking were quantitatively dependent on stimulus parameters of intensity and temporal separation and were unaffected by eye movement parameters (amplitude, velocity, direction) as long as retinal stimulus conditions were constant. The duration of forward masking was longer than that of backward masking. When retinal conditions during saccades were mimicked while the eyes were held steady, masking interactions were identical to those obtained during real saccades. These results indicate that masking effects during saccades in ordinary environments are determined solely by the stimulus situation at the retina. Putative nonvisual, centrally originating saccadic suppression suggested by other authors is evidently not additive with visually determined masking during saccades.