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Unsupervised clustering method to detect microsaccadesMicrosaccades, 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 method's 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.
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Fixational eye movements and binocular visionDuring attempted visual fixation, small involuntary eye movements-called fixational eye movements-continuously change of our gaze's position. Disagreement between the left and right eye positions during such motions can produce diplopia (double vision). Thus, the ability to properly coordinate the two eyes during gaze fixation is critical for stable perception. For the last 50 years, researchers have studied the binocular characteristics of fixational eye movements. Here we review classical and recent studies on the binocular coordination (i.e., degree of conjugacy) of each fixational eye movement type: microsaccades, drift and tremor, and its perceptual contribution to increasing or reducing binocular disparity. We also discuss how amblyopia and other visual pathologies affect the binocular coordination of fixational eye movements.
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Different fixational eye movements mediate the prevention and the reversal of visual fadingFixational eye movements (FEMs; including microsaccades, drift and tremor) are thought to improve visibility during fixation by thwarting neural adaptation to unchanging stimuli, but how the different FEM types influence this process is a matter of debate. Attempts to answer this question have been hampered by the failure to distinguish between the prevention of fading (where fading is blocked before it happens in the first place) and the reversal of fading (where vision is restored after fading has already occurred). Because fading during fixation is a detriment to clear vision, the prevention of fading, which avoids visual degradation before it happens, is a more desirable scenario than improving visibility after fading has occurred. Yet previous studies have not examined the role of FEMs in the prevention of fading, but have focused on visual restoration instead. Here we set out to determine the differential contributions and efficacies of microsaccades and drift to preventing fading in human vision. Our results indicate that both microsaccades and drift mediate the prevention of visual fading. We also found that drift is a potentially larger contributor to preventing fading than microsaccades, although microsaccades are more effective than drift. Microsaccades moreover prevented foveal and peripheral fading in an equivalent fashion, and their efficacy was independent of their size, number, and direction. Our data also suggest that faster drift may prevent fading better than slower drift. These findings may help to reconcile the long-standing controversy concerning the comparative roles of microsaccades and drift in visibility during fixation.
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Fixational Eye Movement Correction of Blink-Induced Gaze Position ErrorsOur eyes move continuously. Even when we attempt to fix our gaze, we produce "fixational" eye movements including microsaccades, drift and tremor. The potential role of microsaccades versus drifts in the control of eye position has been debated for decades and remains in question today. Here we set out to determine the corrective functions of microsaccades and drifts on gaze-position errors due to blinks in non-human primates (Macaca mulatta) and humans. Our results show that blinks contribute to the instability of gaze during fixation, and that microsaccades, but not drifts, correct fixation errors introduced by blinks. These findings provide new insights about eye position control during fixation, and indicate a more general role of microsaccades in fixation correction than thought previously.
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Marvels of illusion: illusion and perception in the art of Salvador DaliThe surrealist movement aimed to blur the distinction between the real and the imagined. Such lack of a border between demonstrable truth and fantasy is perhaps most apparent in the art of Spanish painter Salvador Dali (1904-1989). Dali included numerous illusions in his artworks, with the intent to challenge the viewers' perceptions of reality and to enable them to see beyond the surface. The "Marvels of Illusion" exhibit, shown at The Dali Museum in St. Petersburg, FL., from June 14 to October 12, 2014, showcased Dali paintings, prints and sculptures centered on illusory themes. Here, we review the significance of illusions in Dali's art, focusing on the pieces displayed at the "Marvels of Illusion" exhibit.
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V1 neurons respond differently to object motion versus motion from eye movementsHow does the visual system differentiate self-generated motion from motion in the external world? Humans can discern object motion from identical retinal image displacements induced by eye movements, but the brain mechanisms underlying this ability are unknown. Here we exploit the frequent production of microsaccades during ocular fixation in the primate to compare primary visual cortical responses to self-generated motion (real microsaccades) versus motion in the external world (object motion mimicking microsaccades). Real and simulated microsaccades were randomly interleaved in the same viewing condition, thereby producing equivalent oculomotor and behavioural engagement. Our results show that real microsaccades generate biphasic neural responses, consisting of a rapid increase in the firing rate followed by a slow and smaller-amplitude suppression that drops below baseline. Simulated microsaccades generate solely excitatory responses. These findings indicate that V1 neurons can respond differently to internally and externally generated motion, and expand V1's potential role in information processing and visual stability during eye movements.
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Simultaneous Recordings of Human Microsaccades and Drifts with a Contemporary Video Eye Tracker and the Search Coil TechniqueHuman eyes move continuously, even during visual fixation. These "fixational eye movements" (FEMs) include microsaccades, intersaccadic drift and oculomotor tremor. Research in human FEMs has grown considerably in the last decade, facilitated by the manufacture of noninvasive, high-resolution/speed video-oculography eye trackers. Due to the small magnitude of FEMs, obtaining reliable data can be challenging, however, and depends critically on the sensitivity and precision of the eye tracking system. Yet, no study has conducted an in-depth comparison of human FEM recordings obtained with the search coil (considered the gold standard for measuring microsaccades and drift) and with contemporary, state-of-the art video trackers. Here we measured human microsaccades and drift simultaneously with the search coil and a popular state-of-the-art video tracker. We found that 95% of microsaccades detected with the search coil were also detected with the video tracker, and 95% of microsaccades detected with video tracking were also detected with the search coil, indicating substantial agreement between the two systems. Peak/mean velocities and main sequence slopes of microsaccades detected with video tracking were significantly higher than those of the same microsaccades detected with the search coil, however. Ocular drift was significantly correlated between the two systems, but drift speeds were higher with video tracking than with the search coil. Overall, our combined results suggest that contemporary video tracking now approaches the search coil for measuring FEMs.
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Making the covert overt: Eye-movements reveal the misdirection of gaze and attentionThe methods of magicians are gaining widespread popularity in cognitive science as a powerful tool for increasing the ecological validity of experiments on attention and perception. In a series of eyetracking experiments, participants watched videos of a magic trick, wherein a coin placed beneath a napkin disappears, reappearing under a different napkin. Appropriately deployed attention would allow participants to detect the "secret" event that underlies the illusion (a moving coin), as it happens in full view and is visible for approximately 550 ms. Nevertheless, we observed high rates of inattentional blindness. Unlike prior research, eye-movements during the critical event showed different patterns for participants, depending on whether they saw the moving coin. By adding a distractor task to the magical presentation, we were able to use it to study the timecourse of divided attention via the measurement of microsaccades. We observed that both the onset and direction of microsaccades index task complexity and the locus of covert attention. Meeting abstract presented at VSS 2016
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Abnormal Capillary Vasodynamics Contribute to Ictal Neurodegeneration in EpilepsySeizure-driven brain damage in epilepsy accumulates over time, especially in the hippocampus, which can lead to sclerosis, cognitive decline, and death. Excitotoxicity is the prevalent model to explain ictal neurodegeneration. Current labeling technologies cannot distinguish between excitotoxicity and hypoxia, however, because they share common molecular mechanisms. This leaves open the possibility that undetected ischemic hypoxia, due to ictal blood flow restriction, could contribute to neurodegeneration previously ascribed to excitotoxicity. We tested this possibility with Confocal Laser Endomicroscopy (CLE) and novel stereological analyses in several models of epileptic mice. We found a higher number and magnitude of NG2+ mural-cell mediated capillary constrictions in the hippocampus of epileptic mice than in that of normal mice, in addition to spatial coupling between capillary constrictions and oxidative stressed neurons and neurodegeneration. These results reveal a role for hypoxia driven by capillary blood flow restriction in ictal neurodegeneration.
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Unchanging visions: the effects and limitations of ocular stillnessScientists have pondered the perceptual effects of ocular motion, and those of its counterpart, ocular stillness, for over 200 years. The unremitting 'trembling of the eye' that occurs even during gaze fixation was first noted by Jurin in 1738. In 1794, Erasmus Darwin documented that gaze fixation produces perceptual fading, a phenomenon rediscovered in 1804 by Ignaz Paul Vital Troxler. Studies in the twentieth century established that Jurin's 'eye trembling' consisted of three main types of 'fixational' eye movements, now called microsaccades (or fixational saccades), drifts and tremor. Yet, owing to the constant and minute nature of these motions, the study of their perceptual and physiological consequences has met significant technological challenges. Studies starting in the 1950s and continuing in the present have attempted to study vision during retinal stabilization-a technique that consists on shifting any and all visual stimuli presented to the eye in such a way as to nullify all concurrent eye movements-providing a tantalizing glimpse of vision in the absence of change. No research to date has achieved perfect retinal stabilization, however, and so other work has devised substitute ways to counteract eye motion, such as by studying the perception of afterimages or of the entoptic images formed by retinal vessels, which are completely stable with respect to the eye. Yet other research has taken the alternative tack to control eye motion by behavioural instruction to fix one's gaze or to keep one's gaze still, during concurrent physiological and/or psychophysical measurements. Here, we review the existing data-from historical and contemporary studies that have aimed to nullify or minimize eye motion-on the perceptual and physiological consequences of perfect versus imperfect fixation. We also discuss the accuracy, quality and stability of ocular fixation, and the bottom-up and top-down influences that affect fixation behaviour.This article is part of the themed issue 'Movement suppression: brain mechanisms for stopping and stillness'.
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Microsaccade Characteristics in Neurological and Ophthalmic DiseaseMicrosaccade research has recently reached a critical mass of studies that allows, for the first time, a comprehensive review of how microsaccadic dynamics change in neurological and ophthalmic disease. We discuss the various pathological conditions that affect microsaccades, their impact on microsaccadic and other fixational eye movement dynamics, and the incipient studies that point to microsaccadic features as potential indicators of differential and early diagnoses of multiple clinical conditions, from movement disorders to attention-deficit hyperactivity disorder to amblyopia. We propose that the objective assessment of fixational eye movement parameters may help refine differential diagnostics in neurological disease and assist in the evaluation of ongoing therapy regimes. In addition, determining the effects of ophthalmic disease on fixational eye movement features may help evaluate visual impairment in an objective manner, particularly in young patients or those experiencing communication difficulties.
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Modeling the Triggering of Saccades, Microsaccades, and Saccadic IntrusionsWhen we explore a static visual scene, our eyes move in a sequence of fast eye movements called saccades, which are separated by fixation periods of relative eye stability. Based on uncertain sensory and cognitive inputs, the oculomotor system must decide, at every moment, whether to initiate a saccade or to remain in the fixation state. Even when we attempt to maintain our gaze on a small spot, small saccades, called microsaccades, intrude on fixation once or twice per second. Because microsaccades occur at the boundary of the decision to maintain fixation versus starting a saccade, they offer a unique opportunity to study the mechanisms that control saccadic triggering. Abnormal saccadic intrusions can occur during attempted fixation in patients with neurodegenerative disorders. We have implemented a model of the triggering mechanism of saccades, based on known anatomy and physiology, that successfully simulates the generation of saccades of any size-including microsaccades in healthy observers, and the saccadic intrusions that interrupt attempted fixation in parkinsonian patients. The model suggests that noisy neuronal activity in the superior colliculus controls the state of a mutually inhibitory network in the brain stem formed by burst neurons and omnipause neurons. When the neuronal activity is centered at the rostral pole, the system remains at a state of fixation. When activity is perturbed away from this center, a saccade is triggered. This perturbation can be produced either by the intent to move one's gaze or by random fluctuations in activity.
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Long-term all-optical interrogation of cortical neurons in awake-behaving nonhuman primatesWhereas optogenetic techniques have proven successful in their ability to manipulate neuronal populations-with high spatial and temporal fidelity-in species ranging from insects to rodents, significant obstacles remain in their application to nonhuman primates (NHPs). Robust optogenetics-activated behavior and long-term monitoring of target neurons have been challenging in NHPs. Here, we present a method for all-optical interrogation (AOI), integrating optical stimulation and simultaneous two-photon (2P) imaging of neuronal populations in the primary visual cortex (V1) of awake rhesus macaques. A red-shifted channel-rhodopsin transgene (ChR1/VChR1 [C1V1]) and genetically encoded calcium indicators (genetically encoded calmodulin protein [GCaMP]5 or GCaMP6s) were delivered by adeno-associated viruses (AAVs) and subsequently expressed in V1 neuronal populations for months. We achieved optogenetic stimulation using both single-photon (1P) activation of neuronal populations and 2P activation of single cells, while simultaneously recording 2P calcium imaging in awake NHPs. Optogenetic manipulations of V1 neuronal populations produced reliable artificial visual percepts. Together, our advances show the feasibility of precise and stable AOI of cortical neurons in awake NHPs, which may lead to broad applications in high-level cognition and preclinical testing studies.
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Area V1 responses to illusory corner-folds in Vasarely’s nested squares and the Alternating Brightness Star illusionsVasarely's nested squares illusion shows that the corners of concentric squares, arranged in a gradient of increasing or decreasing luminance, generate illusory "corner-folds," which appear more salient (either brighter or darker) than the adjacent flat (non- corner) regions of each individual square. The Alternating Brightness Star (ABS) illusion, based on Vasarely's classic nested squares, further shows that the strength of these corner-folds depends on corner angle. Previous psychophysical studies showed the relationship between corner angle and perceived contrast in the ABS illusion to be linear, with sharp angles looking higher in contrast, and shallow angles lower in contrast. Center-surround difference-of-Gaussians (DOG) modeling did not replicate this linear relationship, however, suggesting that a full neural explanation of the nested squares and ABS illusions might be found in the visual cortex, rather than at subcortical stages. Here we recorded the responses from single area V1 neurons in the awake primate, during the presentation of visual stimuli containing illusory corner-folds of various angles. Our results showed stronger neural responses for illusory corner-folds made from sharper than from shallower corners, consistent with predictions from the previous psychophysical work. The relationship between corner angle and strength of the neuronal responses, albeit parametric, was apparently non-linear. This finding was in line with the previous DOG data, but not with the psychophysical data. Our combined results suggest that, whereas corner-fold illusions likely originate from center-surround retinogeniculate processes, their complete neural explanation may be found in extrastriate visual cortical areas.
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Analysis of Perceptual Expertise in Radiology – Current Knowledge and a New PerspectiveRadiologists rely principally on visual inspection to detect, describe, and classify findings in medical images. As most interpretive errors in radiology are perceptual in nature, understanding the path to radiologic expertise during image analysis is essential to educate future generations of radiologists. We review the perceptual tasks and challenges in radiologic diagnosis, discuss models of radiologic image perception, consider the application of perceptual learning methods in medical training, and suggest a new approach to understanding perceptional expertise. Specific principled enhancements to educational practices in radiology promise to deepen perceptual expertise among radiologists with the goal of improving training and reducing medical error.
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Microsaccades reflect the dynamics of misdirected attention in magicThe methods of magicians provide powerful tools for enhancing the ecological validity of laboratory studies of attention. The current research borrows a technique from magic to explore the relationship between microsaccades and covert attention under near-natural viewing conditions. We monitored participants' eye movements as they viewed a magic trick where a coin placed beneath a napkin vanishes and reappears beneath another napkin. Many participants fail to see the coin move from one location to the other the first time around, thanks to the magician's misdirection. However, previous research was unable to distinguish whether or not participants were fooled based on their eye movements. Here, we set out to determine if microsaccades may provide a window into the efficacy of the magician's misdirection. In a multi-trial setting, participants monitored the location of the coin (which changed positions in half of the trials), while engaging in a delayed match-to-sample task at a different spatial location. Microsaccades onset times varied with task difficulty, and microsaccade directions indexed the locus of covert attention. Our combined results indicate that microsaccades may be a useful metric of covert attentional processes in applied and ecologically valid settings.
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The Storytelling Brain: How Neuroscience Stories Help Bridge the Gap between Research and SocietyActive communication between researchers and society is necessary for the scientific community's involvement in developing science-based policies. This need is recognized by governmental and funding agencies that compel scientists to increase their public engagement and disseminate research findings in an accessible fashion. Storytelling techniques can help convey science by engaging people's imagination and emotions. Yet, many researchers are uncertain about how to approach scientific storytelling, or feel they lack the tools to undertake it. Here we explore some of the techniques intrinsic to crafting scientific narratives, as well as the reasons why scientific storytelling may be an optimal way of communicating research to nonspecialists. We also point out current communication gaps between science and society, particularly in the context of neurodiverse audiences and those that include neurological and psychiatric patients. Present shortcomings may turn into areas of synergy with the potential to link neuroscience education, research, and advocacy.
