Jorge Otero-Millan

Microsaccadic Efficacy and Contribution to Foveal and Peripheral Vision

Our eyes move constantly, even when we try to fixate our gaze. Fixational eye movements prevent and restore visual loss during fixation, yet the relative impact of each type of fixational eye movement remains controversial. For over five decades, the debate has focused on microsaccades, the fastest and largest fixational eye movements. Some recent studies have concluded that microsaccades counteract visual fading during fixation. Other studies have disputed this idea, contending that microsaccades play no significant role in vision. The disagreement stems from the lack of methods to determine the precise effects of microsaccades on vision versus those of other eye movements, as well as a lack of evidence that microsaccades are relevant to foveal vision. Here we developed a novel generalized method to determine the precise quantified contribution and efficacy of human microsaccades to restoring visibility compared with other eye movements. Our results indicate that microsaccades are the greatest eye movement contributor to the restoration of both foveal and peripheral vision during fixation. Our method to calculate the efficacy and contribution of microsaccades to perception can determine the strength of connection between any two physiological and/or perceptual events, providing a novel and powerful estimate of causal influence; thus, we anticipate wide-ranging applications in neuroscience and beyond.

Microsaccades drive illusory motion in the Enigma illusion

Visual images consisting of repetitive patterns can elicit striking illusory motion percepts. For almost 200 years, artists, psychologists, and neuroscientists have debated whether this type of illusion originates in the eye or in the brain. For more than a decade, the controversy has centered on the powerful illusory motion perceived in the painting Enigma, created by op-artist Isia Leviant. However, no previous study has directly correlated the Enigma illusion to any specific physiological mechanism, and so the debate rages on. Here, we show that microsaccades, a type of miniature eye movement produced during visual fixation, can drive illusory motion in Enigma. We asked subjects to indicate when illusory motion sped up or slowed down during the observation of Enigma while we simultaneously recorded their eye movements with high precision. Before “faster” motion periods, the rate of microsaccades increased. Before “slower/no” motion periods, the rate of microsaccades decreased. These results reveal a direct link between microsaccade production and the perception of illusory motion in Enigma and rule out the hypothesis that the origin of the illusion is purely cortical.

Triggering mechanisms in microsaccade and saccade generation: a novel proposal

Saccades are rapid eye movements that change the line of sight between successive points of fixation. Even as we attempt to fixate our gaze precisely, small rapid eye movements called microsaccades interrupt fixation one or two times each second. Although the neural pathway controlling saccade generation is well understood, the specific mechanism for triggering microsaccades is unknown. Here, we review the evidence suggesting that microsaccades and saccades are generated by the same neural pathway. We also discuss current models of how the saccadic system produces microsaccades. Finally, we propose a new mechanism for triggering both microsaccades and saccades, based on a circuit formed by omnipause and long‐lead burst neurons and driven by activity in the superior colliculus. Our model differs from previous proposals in that it does not require superior colliculus activity to surpass a particular threshold to trigger microsaccades and saccades. Rather, we propose that the reciprocal inhibition between omnipause and long‐lead burst neurons gates each microsaccadic or saccadic event, triggering the eye movement whenever the activity in the long‐lead burst neurons overcomes the inhibition from the omnipause neurons.

The Disturbance of Gaze in Progressive Supranuclear Palsy: Implications for Pathogenesis

Progressive supranuclear palsy (PSP) is a disease of later life that is currently regarded as a form of neurodegenerative tauopathy. Disturbance of gaze is a cardinal clinical feature of PSP that often helps clinicians to establish the diagnosis. Since the neurobiology of gaze control is now well understood, it is possible to use eye movements as investigational tools to understand aspects of the pathogenesis of PSP. In this review, we summarize each disorder of gaze control that occurs in PSP, drawing on our studies of 50 patients, and on reports from other laboratories that have measured the disturbances of eye movements. When these gaze disorders are approached by considering each functional class of eye movements and its neurobiological basis, a distinct pattern of eye movement deficits emerges that provides insight into the pathogenesis of PSP. Although some aspects of all forms of eye movements are affected in PSP, the predominant defects concern vertical saccades (slow and hypometric, both up and down), impaired vergence, and inability to modulate the linear vestibulo-ocular reflex appropriately for viewing distance. These vertical and vergence eye movements habitually work in concert to enable visuomotor skills that are important during locomotion with the hands free. Taken with the prominent early feature of falls, these findings suggest that PSP tauopathy impairs a recently evolved neural system concerned with bipedal locomotion in an erect posture and frequent gaze shifts between the distant environment and proximate hands. This approach provides a conceptual framework that can be used to address the nosological challenge posed by overlapping clinical and neuropathological features of neurodegenerative tauopathies.

An oculomotor continuum from exploration to fixation

During visual exploration, saccadic eye movements scan the scene for objects of interest. During attempted fixation, the eyes are relatively still but often produce microsaccades. Saccadic rates during exploration are higher than those of microsaccades during fixation, reinforcing the classic view that exploration and fixation are two distinct oculomotor behaviors. An alternative model is that fixation and exploration are not dichotomous, but are instead two extremes of a functional continuum. Here, we measured the eye movements of human observers as they either fixed their gaze on a small spot or scanned natural scenes of varying sizes. As scene size diminished, so did saccade rates, until they were continuous with microsaccadic rates during fixation. Other saccadic properties varied as function of image size as well, forming a continuum with microsaccadic parameters during fixation. This saccadic continuum extended to nonrestrictive, ecological viewing conditions that allowed all types of saccades and fixation positions. Eye movement simulations moreover showed that a single model of oculomotor behavior can explain the saccadic continuum from exploration to fixation, for images of all sizes. These findings challenge the view that exploration and fixation are dichotomous, suggesting instead that visual fixation is functionally equivalent to visual exploration on a spatially focused scale.

Highly informative natural scene regions increase microsaccade production during visual scanning.

Classical image statistics, such as contrast, entropy, and the correlation between central and nearby pixel intensities, are thought to guide ocular fixation targeting. However, these statistics are not necessarily task relevant and therefore do not provide a complete picture of the relationship between informativeness and ocular targeting. Moreover, it is not known whether either informativeness or classical image statistics affect microsaccade production; thus, the role of microsaccades in information acquisition is also unknown. The objective quantification of the informativeness of a scene region is a major challenge, because it can vary with both image features and the task of the viewer. Thus, previous definitions of informativeness suffered from subjectivity and inconsistency across studies. Here we developed an objective measure of informativeness based on fixation consistency across human observers, which accounts for both bottom-up and top-down influences in ocular targeting. We then analyzed fixations in more versus less informative image regions in relation to classical statistics. Observers generated more microsaccades on more informative than less informative image regions, and such regions also exhibited low redundancy in their classical statistics. Increased microsaccade production was not explained by increased fixation duration, suggesting that the visual system specifically uses microsaccades to heighten information acquisition from informative regions.

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.

The effects of fixation target size and luminance on microsaccades and square-wave jerks.

A large amount of classic and contemporary vision studies require subjects to fixate a target. Target fixation serves as a normalizing factor across studies, promoting the field’s ability to compare and contrast experiments. Yet, fixation target parameters, including luminance, contrast, size, shape and color, vary across studies, potentially affecting the interpretation of results. Previous research on the effects of fixation target size and luminance on the control of fixation position rendered conflicting results, and no study has examined the effects of fixation target characteristics on square-wave jerks, the most common type of saccadic intrusion. Here we set out to determine the effects of fixation target size and luminance on the characteristics of microsaccades and square-wave jerks, over a large range of stimulus parameters. Human subjects fixated a circular target with varying luminance and size while we recorded their eye movements with an infrared video tracker (EyeLink 1000, SR Research). We detected microsaccades and SWJs automatically with objective algorithms developed previously. Microsaccade rates decreased linearly and microsaccade magnitudes increased linearly with target size. The percent of microsaccades forming part of SWJs decreased, and the time from the end of the initial SWJ saccade to the beginning of the second SWJ saccade (SWJ inter-saccadic interval; ISI) increased with target size. The microsaccadic preference for horizontal direction also decreased moderately with target size . Target luminance did not affect significantly microsaccades or SWJs, however. In the absence of a fixation target, microsaccades became scarcer and larger, while SWJ prevalence decreased and SWJ ISIs increased. Thus, the choice of fixation target can affect experimental outcomes, especially in human factors and in visual and oculomotor studies. These results have implications for previous and future research conducted under fixation conditions, and should encourage forthcoming studies to report the size of fixation targets to aid the interpretation and replication of their results.

Saccades during Attempted Fixation in Parkinsonian Disorders and Recessive Ataxia: From Microsaccades to Square-Wave Jerks

During attempted visual fixation, saccades of a range of sizes occur. These “fixational saccades” include microsaccades, which are not apparent in regular clinical tests, and “saccadic intrusions”, predominantly horizontal saccades that interrupt accurate fixation. Square-wave jerks (SWJs), the most common type of saccadic intrusion, consist of an initial saccade away from the target followed, after a short delay, by a “return saccade” that brings the eye back onto target. SWJs are present in most human subjects, but are prominent by their increased frequency and size in certain parkinsonian disorders and in recessive, hereditary spinocerebellar ataxias. Here we asked whether fixational saccades showed distinctive features in various parkinsonian disorders and in recessive ataxia. Although some saccadic properties differed between patient groups, in all conditions larger saccades were more likely to form SWJs, and the intervals between the first and second saccade of SWJs were similar. These findings support the proposal of a common oculomotor mechanism that generates all fixational saccades, including microsaccades and SWJs. The same mechanism also explains how the return saccade in SWJs is triggered by the position error that occurs when the first saccadic component is large, both in the healthy brain and in neurological disease.

Unsupervised clustering method to detect microsaccades.

Microsaccades, small involuntary eye movements that occur once or twice per second during attempted visual fixation, are relevant to perception, cognition, and oculomotor control and present distinctive characteristics in visual and oculomotor pathologies. Thus, the development of robust and accurate microsaccade-detection techniques is important for basic and clinical neuroscience research. Due to the diminutive size of microsaccades, however, automatic and reliable detection can be difficult. Current challenges in microsaccade detection include reliance on set, arbitrary thresholds and lack of objective validation. Here we describe a novel microsaccade-detecting method, based on unsupervised clustering techniques, that does not require an arbitrary threshold and provides a detection reliability index. We validated the new clustering method using real and simulated eye-movement data. The clustering method reduced detection errors by 62% for binocular data and 78% for monocular data, when compared to standard contemporary microsaccade-detection techniques. Further, the clustering methods reliability index was correlated with the microsaccade-detection error rate, suggesting that the reliability index may be used to determine the comparative precision of eye-tracking devices.