Task difficulty in mental arithmetic affects microsaccadic rates and magnitudes

Microsaccades are involuntary, small‐magnitude saccadic eye movements that occur during attempted visual fixation. Recent research has found that attention can modulate microsaccade dynamics, but few studies have addressed the effects of task difficulty on microsaccade parameters, and those have obtained contradictory results. Further, no study to date has investigated the influence of task difficulty on microsaccade production during the performance of non‐visual tasks. Thus, the effects of task difficulty on microsaccades, isolated from sensory modality, remain unclear. Here we investigated the effects of task difficulty on microsaccades during the performance of a non‐visual, mental arithmetic task with two levels of complexity. We found that microsaccade rates decreased and microsaccade magnitudes increased with increased task difficulty. We propose that changes in microsaccade rates and magnitudes with task difficulty are mediated by the effects of varying attentional inputs on the rostral superior colliculus activity map.     

Fast and nonuniform dynamics of perisaccadic vision in the central fovea

Humans use rapid eye movements (saccades) to inspect stimuli with the foveola, the region of the retina where receptors are most densely packed. It is well established that visual sensitivity is generally attenuated during these movements, a phenomenon known as saccadic suppression. This effect is commonly studied with large, often peripheral, stimuli presented during instructed saccades. However, little is known about how saccades modulate the foveola and how the resulting dynamics unfold during natural visual exploration. Here we measured the foveal dynamics of saccadic suppression in a naturalistic high-acuity task, a task designed after primates’ social grooming, which—like most explorations of fine patterns—primarily elicits minute saccades (microsaccades). Leveraging on recent advances in gaze-contingent display control, we were able to systematically map the perisaccadic time course of sensitivity across the foveola. We show that contrast sensitivity is not uniform across this region and that both the extent and dynamics of saccadic suppression vary within the foveola. Suppression is stronger and faster in the most central portion, where sensitivity is generally higher and selectively rebounds at the onset of a new fixation. These results shed light on the modulations experienced by foveal vision during the saccade-fixation cycle and explain some of the benefits of microsaccades.

Human vision is not uniform across space. While the retina collects information from a broad field, only a minuscule fraction—less than 0.01%—is examined at high resolution. This is the area covered by the foveola, the region void of rods and capillaries, where cones are most densely packed. Because of this organization, rapid eye movements, known as saccades, are necessary to redirect gaze toward the objects of interest, abruptly translating the image across the retina every few hundreds of milliseconds. It is remarkable that the visual system appears unperturbed by these sudden visual transitions and seamlessly integrates fixations into a stable representation of the visual scene.It has long been observed that visual sensitivity is transiently attenuated around the time of saccades, a phenomenon believed to play a role in perceptually suppressing retinal image motion during eye movements. This effect, known as “saccadic suppression”, consists of the elevation of contrast thresholds to briefly flashed stimuli, which precedes the initiation of the saccade and outlasts it by as much as 100 ms (1–5). Saccadic suppression is typically investigated with stimuli that cover large portions of the visual field, often in the periphery. However, limitations in the precision of stimulus delivery, both spatial and temporal, have so far prevented mapping of the saccade-induced dynamics of visibility within the foveola. Thus, despite the disproportionate importance of foveal vision, little is currently known about its time course around the time of saccades.Studies on saccadic suppression also commonly focus on large saccades under well-controlled, but artificial, laboratory conditions. However, an examination of the time course of foveal vision needs to take into account that natural execution of high-acuity tasks—the tasks that require foveal vision—normally tends to elicit saccades with very small amplitudes (6). Microsaccades, gaze shifts so small that the attended stimulus remains within the foveola, are the most frequent saccades when examining a distant face (7), threading a needle (8), or reading fine print (9), tasks in which they shift the line of sight with surprising precision. Because of their minute amplitudes, microsaccades pose specific challenges to the mechanisms traditionally held responsible for saccadic suppression (10–19). These movements yield broadly overlapping pre- and postsaccadic images within the fovea, which would appear to provide little masking in visual stimulation (20). They also result in reduced retinal smear (21), as they rotate the eye at much lower speeds than larger saccades, delivering luminance modulations that are well within the range of human temporal sensitivity. Furthermore, it is unknown whether possible corollary discharges associated with microsaccades exert similar effects to those of their larger counterparts (22).Despite these observations, microsaccades have been found to suppress sensitivity to relatively large test stimuli (23–25). However, the only two studies that specifically examined foveal vision during microsaccades reached diametrically opposite conclusions, with one arguing for a normal reduction in sensitivity (26) and the other for a complete lack of suppression (27), leaving open the question of whether suppression extends to the foveola. While several factors could have been responsible for these discrepant results, two important considerations are worth emphasizing. First, selectively testing foveal dynamics is technically challenging, since the entire foveola is comparable in size to the region of uncertainty in gaze localization resulting from standard eye-tracking methods. Second, the common intuition gained by conceptualizing the visual signals delivered by saccades as uniform—i.e., constant-velocity—translations of the image on the retina (28) does not apply well to microsaccades, whose relatively brief durations and well-defined dynamics yield substantially lower power on the retina than predicted by a uniform translation (29). Thus, even a moderate suppression may be sufficient to prevent visibility of stationary scenes during small saccades.Recent advances in methods for gaze-contingent display control now enable determination of the line of sight with accuracy sufficient to selectively test a desired foveal region during normal eye movements. Leveraging on these recent advances, here we mapped the perisaccadic dynamics of contrast sensitivity across the foveola during natural visual exploration. We developed a gaze-contingent high-acuity task that resembles primate social grooming, a task that very naturally integrates visual search and detection of brief stimuli and that spontaneously elicits frequent microsaccades, and presented probes at desired retinal locations with high spatial and temporal resolution. Our results show that microsaccades are accompanied by an elevation of visual thresholds at the center of gaze that starts before the initiation of the movement but dissipates very rapidly as the saccade ends. The extent and dynamics of this suppression vary with eccentricity across the foveola, so that a stronger modulation occurs in the most central region, where vision is selectively enhanced after a saccade.     

Individual neurons in the caudal fastigial oculomotor region convey information on both macro‐ and microsaccades

Recent studies have suggested that microsaccades, the small amplitude saccades made during fixation, are precisely controlled. Two lines of evidence suggest that the cerebellum plays a key role not only in improving the accuracy of macrosaccades but also of microsaccades. First, lesions of the fastigial oculomotor regions (FOR) cause horizontal dysmetria of both micro‐ and macrosaccades. Secondly, our previous work on Purkinje cell simple spikes in the oculomotor vermis (OV) has established qualitatively similar response preferences for these two groups of saccades. In this work, we investigated the control signals for micro‐ and macrosaccades in the FOR, the target of OV Purkinje cell axons. We found that the same FOR neurons discharged for micro‐ and macrosaccades. For both groups of saccades, FOR neurons exhibited very similar dependencies of their discharge strength on direction and amplitude and very similar burst onset time differences for ipsi‐ and contraversive saccades and, in both, response duration reflected saccade duration, at least at the population level. An intriguing characteristic of microsaccade‐related responses is that immediate pre‐saccadic firing rates decreased with distance to the target center, a pattern that strikingly parallels the eye position dependency of both microsaccade metrics and frequency, which may suggest a potential neural mechanism underlying the role of FOR in fixation. Irrespective of this specific consideration, our study supports the view that microsaccades and macrosaccades share the same cerebellar circuitry and, in general, further strengthens the notion of a microsaccade–macrosaccade continuum.     

Regression-based analysis of combined EEG and eye-tracking data: Theory and applications

Fixation-related potentials (FRPs), neural responses aligned to the end of saccades, are a promising tool for studying the dynamics of attention and cognition under natural viewing conditions. In the past, four methodological problems have complicated the analysis of such combined eye-tracking/electroencephalogram experiments: (1) the synchronization of data streams, (2) the removal of ocular artifacts, (3) the condition-specific temporal overlap between the brain responses evoked by consecutive fixations, and (4) the fact that numerous low-level stimulus and saccade properties also influence the postsaccadic neural responses. Although effective solutions exist for the first two problems, the latter two are only beginning to be addressed. In the current paper, we present and review a unified regression-based framework for FRP analysis that allows us to deconvolve overlapping potentials while also controlling for both linear and nonlinear confounds on the FRP waveform. An open software implementation is provided for all procedures. We then demonstrate the advantages of this proposed (non)linear deconvolution modeling approach for data from three commonly studied paradigms: face perception, scene viewing, and reading. First, for a traditional event-related potential (ERP) face recognition experiment, we show how this technique can separate stimulus ERPs from overlapping muscle and brain potentials produced by small (micro)saccades on the face. Second, in natural scene viewing, we model and isolate multiple nonlinear effects of saccade parameters on the FRP. Finally, for a natural sentence reading experiment using the boundary paradigm, we show how it is possible to study the neural correlates of parafoveal preview after removing spurious overlap effects caused by the associated difference in average fixation time. Our results suggest a principal way of measuring reliable eye movement-related brain activity during natural vision.     

Severe distortion in the representation of foveal visual image locations in short-term memory

The foveal visual image region provides the human visual system with the highest acuity. However, it is unclear whether such a high fidelity representational advantage is maintained when foveal image locations are committed to short-term memory. Here, we describe a paradoxically large distortion in foveal target location recall by humans. We briefly presented small, but high contrast, points of light at eccentricities ranging from 0.1 to 12°, while subjects maintained their line of sight on a stable target. After a brief memory period, the subjects indicated the remembered target locations via computer controlled cursors. The biggest localization errors, in terms of both directional deviations and amplitude percentage overshoots or undershoots, occurred for the most foveal targets, and such distortions were still present, albeit with qualitatively different patterns, when subjects shifted their gaze to indicate the remembered target locations. Foveal visual images are severely distorted in short-term memory.

The representation of visual spatial locations in short-term memory has been one of the most classic means for studying the neural mechanisms of cognitive control in modern-day systems neuroscience (1–6). Experimentally, reporting a remembered target location with a saccadic eye movement has proven extremely useful in demonstrating how different cortical and subcortical brain regions may maintain a memory trace of visual targets (7), and it has also been equally important for oculomotor control studies in dissociating sensory and motor responses (8–11).One mechanism for short-term memory maintenance in multiple brain areas is the persistence of neural activity associated with remembered stimulus locations, even in the absence of sensory drive (7, 12). Such persistence, with temporal drift, can help explain a variety of distortions in memory-based task performance, for example, as a function of how long a location needs to be maintained in short-term memory (12). In addition, such persistence can reveal certain systematic biases with respect to whether stimuli occupy a single visual quadrant or multiple visual quadrants (13), which in turn enables linking visual field asymmetries in perception to representations of remembered target locations. For example, visual performance along the horizontal and vertical retinotopic meridians is different (14–16), and this difference is maintained in tasks involving short-term memory (17). The fact that such visual meridian effects may be related to tissue magnification in visual cortical areas (18–20) might then suggest that other known distortions in short-term memory tasks, such as foveal biases in remembering peripheral target locations (21–23), may also be related to how visual space is represented in topographic maps.If remembering visual target locations depends on both how visual space is topographically represented as well as on how memory information is neurally maintained, then an important remaining open question is whether foveal visual locations are recalled veridically or not, given the normally very high acuity nature of foveal vision in humans. Here, we investigated this question and found that remembering a foveal visual location as near to the line of sight as 0.1° (6 min arc) is subject to severe distortion, even after very short memory delay intervals. This paradoxical foveal distortion in visual short-term memory emerges with or without a constant landmark being available during the response phase of the task, and, perhaps most importantly, it is also qualitatively different depending on whether the remembered location is reported with an eye movement response or with another response modality.     

Learning to silence saccadic suppression

Perceptual stability is facilitated by a decrease in visual sensitivity during rapid eye movements, called saccadic suppression. While a large body of evidence demonstrates that saccadic programming is plastic, little is known about whether the perceptual consequences of saccades can be modified. Here, we demonstrate that saccadic suppression is attenuated during learning on a standard visual detection-in-noise task, to the point that it is effectively silenced. Across a period of 7 days, 44 participants were trained to detect brief, low-contrast stimuli embedded within dynamic noise, while eye position was tracked. Although instructed to fixate, participants regularly made small fixational saccades. Data were accumulated over a large number of trials, allowing us to assess changes in performance as a function of the temporal proximity of stimuli and saccades. This analysis revealed that improvements in sensitivity over the training period were accompanied by a systematic change in the impact of saccades on performance—robust saccadic suppression on day 1 declined gradually over subsequent days until its magnitude became indistinguishable from zero. This silencing of suppression was not explained by learning-related changes in saccade characteristics and generalized to an untrained retinal location and stimulus orientation. Suppression was restored when learned stimulus timing was perturbed, consistent with the operation of a mechanism that temporarily reduces or eliminates saccadic suppression, but only when it is behaviorally advantageous to do so. Our results indicate that learning can circumvent saccadic suppression to improve performance, without compromising its functional benefits in other viewing contexts.

Humans continuously sample the external world using frequent and rapid gaze shifts called saccades, which cause the image of the visual scene to sweep across the retina. The fact that we remain unaware of these frequent disruptions to visual input and maintain a stable perception of the world has intrigued generations of vision scientists (1–9). While early researchers attributed the lack of awareness of intrasaccadic stimulation to a form of central anesthesia (6), it is most commonly associated with the phenomenon of saccadic suppression—a reduction in the visibility of brief flashes presented around the time of a saccade. A large number of studies spanning more than a century have reported changes in the threshold for, or probability of detecting, brief perisaccadic stimuli. These effects have been demonstrated for different classes of saccadic eye movements and under a range of experimental conditions; for example, with large reactive saccades initiated under instruction, smaller spontaneous saccades during attempted fixation (10–12), targets presented on clear (11, 13) and textured (10, 14, 15) backgrounds, and in both the central (16, 17) and peripheral (11, 14, 18, 19) visual field. Despite widespread agreement that saccadic suppression is a robust phenomenon, consensus regarding its underlying mechanisms has proved elusive. During natural viewing, it is likely that the postsaccadic visual scene acts to mask the intrasaccadic image, which has been blurred by its rapid translation across the retina (4, 20–24). However, some researchers have argued for an active form of suppression, triggered by an extraretinal signal or corollary discharge of the saccadic eye movement (refs. 8 and 25–28; for counter arguments, see refs. 3, 4, and 23).Saccades were classically considered to be highly stereotyped movements, reflecting the fact that they have relatively stable kinematic properties that are resistant to voluntary control and modification by training (29, 30). However, it is becoming increasingly clear that most characteristics of saccades can be modified. Evidence for saccadic plasticity comes from a variety of sources. Rather than being fixed, the “main sequence” relationship between saccade velocity and amplitude can be manipulated by visual stimulation (31) or reward (32, 33). When saccadic targets are consistently displaced by an experimenter during flight, individuals quickly adapt the amplitude (34–36) or direction (37) of future saccades to minimize landing errors. Repeated training on oculomotor tasks has been shown to decrease saccadic reaction times and increase the frequency of a variety of saccade types (38–41). In addition, close examination of eye movements has revealed that saccade production adjusts to meet current behavioral goals. During the threading of a needle, for example, small spontaneous saccades move the eye regularly between the tip of the thread and the eye of the needle in order to estimate relative alignment between the two (42). In addition, saccade rate and amplitude distributions are influenced by a variety of factors such as task complexity (43, 44), whether an individual is performing free-viewing or visual search (45), the size of the visual scene (46), and how informative an image region is (47).In contrast to the growing literature documenting different forms of oculomotor plasticity, far less is known about the extent to which the perceptual consequences of saccades can be modified. This is partly due to ongoing debate over the relative contribution of active (extraretinal) and passive (masking) mechanisms to saccadic suppression, which has dominated much of the work in this area. Given its hypothesized functional role in maintaining visual stability across eye movements, it is tempting to assume that saccadic suppression must be a stable, perhaps even hard-wired effect that is impervious to training. Empirical validation of this assumption is lacking, however, as most studies aggregate perisaccadic visual judgements (often in a small number of well-trained observers) across multiple testing sessions. Two recent studies have reported learned improvements in visual task performance following training with stimuli consistently presented before (48) or during (49) saccades. While these findings demonstrate that perceptual learning is possible around the time of saccades, the role of suppression in this process remains unclear. Is saccadic suppression impervious to learning, placing an upper limit on the amount of improvement that is achievable with training? Or can learning modify saccadic suppression in a manner that actively contributes to improvements in sensory performance?To address these questions, we measured visual sensitivity to a brief peripheral target stimulus embedded in luminance noise. This task consistently shows large improvements in performance with practice, and variants have been used extensively to investigate the characteristics and mechanisms of perceptual learning. Rather than direct subjects to make large saccades around the time of stimulus presentation, we instead exploited spontaneously occurring saccades during attempted fixation. This approach had several advantages. From a practical perspective, it enabled us to make use of a standard perceptual learning paradigm, with the only addition being noninvasive monitoring of eye position. Moreover, it avoided the conflict of having to instruct subjects to perform the task as accurately as possible, while also making eye movements that would likely impair their ability to do so. While the majority of suppression studies focus on a small number of highly trained individuals, we were able to instead use a larger group of completely naive subjects without the need for any eye movement training. Although saccadic suppression has generally been investigated using large voluntary saccades, a body of evidence suggests that the visual consequences of fixational and voluntary saccades are comparable (12, 25, 26, 50–53), consistent with a view that fixational saccades are part of a saccadic continuum that is simply delineated by the magnitude of the eye movement (28, 51, 54–57).     

Fixational eye movements following concussion

The purpose of this study was to evaluate fixational eye movements (FEMs) with high spatial and temporal resolution following concussion, where oculomotor symptoms and impairments are common. Concussion diagnosis was determined using current consensus guidelines. A retinal eye-tracking device, the tracking scanning laser ophthalmoscope (TSLO), was used to measure FEMs in adolescents and young adults following a concussion and in an unaffected control population. FEMs were quantified in two fixational paradigms: (1) when fixating on the center, or (2) when fixating on the corner of the TSLO imaging raster. Fixational saccade amplitude in recent concussion patients (≤ 21 days) was significantly greater, on average, in the concussion group (mean = 1.03°; SD = 0.36°) compared with the controls (mean = 0.82°; SD = 0.31°), when fixating on the center of the imaging raster (t = 2.87, df = 82, p = 0.005). These fixational saccades followed the main sequence and therefore also had greater peak velocity (t = 2.86, df = 82, p = 0.006) and peak acceleration (t = 2.80, df = 82, p = 0.006). These metrics significantly differentiated concussed from controls (AUC = 0.67–0.68, minimum p = 0.005). No group differences were seen for the drift metrics in either task or for any of the FEMs metrics in the corner-of-raster fixation task. Fixational saccade amplitudes were significantly different in the concussion group, but only when fixating on the center of the raster. This task specificity suggests that task optimization may improve differentiation and warrants further study. FEMs measured in the acute-to-subacute period of concussion recovery may provide a quick (<3 minutes), objective, sensitive, and accurate ocular dysfunction assessment. Future work should assess the impact of age, mechanism of injury, and post-concussion recovery on FEM alterations following concussion.     

Arousal thresholds during human tonic and phasic REM sleep

The goal of the present study was to investigate arousal thresholds (ATs) in tonic and phasic episodes of rapid eye movement (REM) sleep, and to compare the frequency spectrum of these sub‐states of REM to non‐REM (NREM) stages of sleep. We found the two REM stages to differ with regard to behavioural responses to external acoustic stimuli. The AT in tonic REM was indifferent from that in sleep stage 2, and ATs in phasic REM were similar to those in slow‐wave sleep (stage 4). NREM and REM stages of similar behavioural thresholds were distinctly different with regard to their frequency pattern. These data provide further evidence that REM sleep should not be regarded a uniform state. Regarding electroencephalogram frequency spectra, we found that the two REM stages were more similar to each other than to NREM stages with similar responsivity. Ocular activity such as ponto‐geniculo‐occipital‐like waves and microsaccades are discussed as likely modulators of behavioural responsiveness and cortical processing of auditory information in the two REM sub‐states.