Xoana G. Troncoso

Microsaccades: a neurophysiological analysis

Microsaccades are the largest and fastest of the fixational eye movements, which are involuntary eye movements produced during attempted visual fixation. In recent years, the interaction between microsaccades, perception and cognition has become one of the most rapidly growing areas of study in visual neuroscience. The neurophysiological consequences of microsaccades have been the focus of less attention, however, as have the oculomotor mechanisms that generate and control microsaccades. Here we review the latest neurophysiological findings concerning microsaccades and discuss their relationships to perception and cognition. We also point out the current gaps in our understanding of the neurobiology of microsaccades and identify the most promising lines of enquiry.

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.

Novel visual illusions related to Vasarely's 'nested squares' show that corner salience varies with corner angle

Vasarelys ‘nested-squares’ illusion shows that 90° corners can be more salient perceptually than straight edges. On the basis of this illusion we have developed a novel visual illusion, the ‘Alternating Brightness Star’, which shows that sharp corners are more salient than shallow corners (an effect we call ‘corner angle salience variation’) and that the same corner can be perceived as either bright or dark depending on the polarity of the angle (ie whether concave or convex: ‘corner angle brightness reversal’). Here we quantify the perception of corner angle salience variation and corner angle brightness reversal effects in twelve naive human subjects, in a two-alternative forced-choice brightness discrimination task. The results show that sharp corners generate stronger percepts than shallow corners, and that corner gradients appear bright or dark depending on whether the corner is concave or convex. Basic computational models of center – surround receptive fields predict the results to some degree, but not fully.

Simultaneous recordings of ocular microtremor and microsaccades with a piezoelectric sensor and a video-oculography system

Our eyes are in continuous motion. Even when we attempt to fix our gaze, we produce so called “fixational eye movements”, which include microsaccades, drift, and ocular microtremor (OMT). Microsaccades, the largest and fastest type of fixational eye movement, shift the retinal image from several dozen to several hundred photoreceptors and have equivalent physical characteristics to saccades, only on a smaller scale (Martinez-Conde, Otero-Millan & Macknik, 2013). OMT occurs simultaneously with drift and is the smallest of the fixational eye movements (∼1 photoreceptor width, >0.5 arcmin), with dominant frequencies ranging from 70 Hz to 103 Hz (Martinez-Conde, Macknik & Hubel, 2004). Due to OMT’s small amplitude and high frequency, the most accurate and stringent way to record it is the piezoelectric transduction method. Thus, OMT studies are far rarer than those focusing on microsaccades or drift. Here we conducted simultaneous recordings of OMT and microsaccades with a piezoelectric device and a commercial infrared video tracking system. We set out to determine whether OMT could help to restore perceptually faded targets during attempted fixation, and we also wondered whether the piezoelectric sensor could affect the characteristics of microsaccades. Our results showed that microsaccades, but not OMT, counteracted perceptual fading. We moreover found that the piezoelectric sensor affected microsaccades in a complex way, and that the oculomotor system adjusted to the stress brought on by the sensor by adjusting the magnitudes of microsaccades.

V1 neurons respond differently to object motion versus motion from eye movements

How 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 V1s potential role in information processing and visual stability during eye movements.

BOLD activation varies parametrically with corner angle throughout human retinotopic cortex

The Alternating Brightness Star (ABS) is an illusion that provides insight into the relationship between brightness perception and corner angle. Recent psychophysical studies of this illusion have shown that corner salience varies parametrically with corner angle, with sharp angles leading to strong illusory percepts and shallow angles leading to weak percepts. It is hypothesized that the illusory effects arise because of an interaction between surface corners and the shape of visual receptive fields: sharp surface corners may create hotspots of high local contrast due to processing by center–surround and other early receptive fields. If this hypothesis is correct, early visual neurons should respond powerfully to sharp corners and curved portions of surface edges. Indeed, the primary role of early visual neurons may be to localize the discontinuities along the edges of surfaces. If so, all early visual areas should show greater BOLD responses to sharp corners than to shallow corners. On the other hand, if corner processing is exclusively constrained to certain areas of the brain, only those specific areas will show greater responses to sharp vs shallow corners. To address this we explored the BOLD correlates of the ABS illusion in the human visual cortex using fMRI. We found that BOLD signal varies parametrically with corner angle throughout the visual cortex, offering the first neurophysiological correlates of the ABS illusion. This finding provides a neurophysiological basis for the previously reported psychophysical data that showed that corner salience varied parametrically with corner angle. We propose that all early visual areas localize discontinuities along the edges of surfaces, and that specific cortical corner-processing circuits further establish the specific nature of those discontinuities, such as their orientation.

Corner salience varies linearly with corner angle during flicker-augmented contrast: a general principle of corner perception based on Vasarely's artworks

When corners are embedded in a luminance gradient, their perceived salience varies linearly with corner angle (Troncoso et al., 2005). Here we hypothesize that this relationship may hold true for all corners, not just corner gradients. To test this hypothesis, we developed a novel variant of the flicker-augmented contrast illusion (Anstis and Ho, 1998) that employs solid (non-gradient) corners of varying angles to modify perceived brightness. We flickered solid corners from dark to light grey (50% luminance over time) against a black or a white background. With this new stimulus, subjects compared the apparent brightness of corners, which did not vary in actual luminance, to non-illusory stimuli that varied in actual luminance. We found that the apparent brightness of corners was linearly related to the sharpness of corner angle. Thus this relationship is not solely an effect of corners embedded in gradients, but may be a general principle of corner perception. These findings may have important repercussions for brain mechanisms underlying the early visual processing of shape and brightness. A large fraction of Vasarelys art showcases the perceptual salience of corners, curvature and terminators. Several of these artworks and their implications for visual processing are discussed.

Fixational Eye Movement Correction of Blink-Induced Gaze Position Errors

Our 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.

Synaptic Correlates of Low-Level Perception in V1.

The computational role of primary visual cortex (V1) in low-level perception remains largely debated. A dominant view assumes the prevalence of higher cortical areas and top-down processes in binding information across the visual field. Here, we investigated the role of long-distance intracortical connections in form and motion processing by measuring, with intracellular recordings, their synaptic impact on neurons in area 17 (V1) of the anesthetized cat. By systematically mapping synaptic responses to stimuli presented in the nonspiking surround of V1 receptive fields, we provide the first quantitative characterization of the lateral functional connectivity kernel of V1 neurons. Our results revealed at the population level two structural-functional biases in the synaptic integration and dynamic association properties of V1 neurons. First, subthreshold responses to oriented stimuli flashed in isolation in the nonspiking surround exhibited a geometric organization around the preferred orientation axis mirroring the psychophysical “association field” for collinear contour perception. Second, apparent motion stimuli, for which horizontal and feedforward synaptic inputs summed in-phase, evoked dominantly facilitatory nonlinear interactions, specifically during centripetal collinear activation along the preferred orientation axis, at saccadic-like speeds. This spatiotemporal integration property, which could constitute the neural correlate of a human perceptual bias in speed detection, suggests that local (orientation) and global (motion) information is already linked within V1. We propose the existence of a “dynamic association field” in V1 neurons, whose spatial extent and anisotropy are transiently updated and reshaped as a function of changes in the retinal flow statistics imposed during natural oculomotor exploration. SIGNIFICANCE STATEMENT The computational role of primary visual cortex in low-level perception remains debated. The expression of this “pop-out” perception is often assumed to require attention-related processes, such as top-down feedback from higher cortical areas. Using intracellular techniques in the anesthetized cat and novel analysis methods, we reveal unexpected structural-functional biases in the synaptic integration and dynamic association properties of V1 neurons. These structural-functional biases provide a substrate, within V1, for contour detection and, more unexpectedly, global motion flow sensitivity at saccadic speed, even in the absence of attentional processes. We argue for the concept of a “dynamic association field” in V1 neurons, whose spatial extent and anisotropy changes with retinal flow statistics, and more generally for a renewed focus on intracortical computation.