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.

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.

Distinctive features of saccadic intrusions and microsaccades in progressive supranuclear palsy.

The eyes do not stay perfectly still during attempted fixation; fixational eye movements and saccadic intrusions (SIs) continuously change the position of gaze. The most common type of SI, square-wave jerks (SWJs), consists of saccade pairs that appear purely horizontal on clinical inspection: the first saccade moves the eye away from the fixation target, and after a short interval, the second saccade brings it back toward the target. SWJs are prevalent in certain neurological disorders, including progressive supranuclear palsy (PSP). Here, we developed an objective method to identify SWJs. We found that SWJs are more frequent, larger, and more markedly horizontal in PSP patients than in healthy human subjects. Furthermore, the loss of a vertical component in fixational saccades and SWJs was the eye movement feature that best distinguished PSP patients from controls. We moreover determined that, in PSP patients and controls, the larger the saccade the more likely it was part of a SWJ. Furthermore, saccades produced by PSP patients had equivalent properties whether they were part of a SWJ or not, suggesting that normal fixational saccades (microsaccades) are rare in PSP. We propose that fixational saccades and SIs are generated by the same neural circuit and that, both in PSP patients and in controls, SWJs result from a coupling mechanism that generates a second corrective saccade shortly after a large fixation saccade. Because of brainstem and/or cerebellum impairment, fixational saccades in PSP are abnormally large and thus more likely to trigger a corrective saccade, giving rise to SWJs.

Horizontal connectivity in V1: Prediction of coherence in contour and motion integration.

This study demonstrates the functional importance of the Surround context relayed laterally in V1 by the horizontal connectivity, in controlling the latency and the gain of the cortical response to the feedforward visual drive. We report here four main findings: 1) a centripetal apparent motion sequence results in a shortening of the spiking latency of V1 cells, when the orientation of the local inducer and the global motion axis are both co-aligned with the RF orientation preference; 2) this contextual effects grows with visual flow speed, peaking at 150-250°/s when it matches the propagation speed of horizontal connectivity (0.15-0.25 mm/ms); 3) For this speed range, the axial sensitivity of V1 cells is tilted by 90° to become co-aligned with the orientation preference axis; 4) the strength of modulation by the surround context correlates with the spatiotemporal coherence of the apparent motion flow. Our results suggest an internally-generated binding process, linking local (orientation /position) and global (motion/direction) features as early as V1. This long-range diffusion process constitutes a plausible substrate in V1 of the human psychophysical bias in speed estimation for collinear motion. Since it is demonstrated in the anesthetized cat, this novel form of contextual control of the cortical gain and phase is a built-in property in V1, whose expression does not require behavioral attention and top-down control from higher cortical areas. We propose that horizontal connectivity participates in the propagation of an internal "prediction" wave, shaped by visual experience, which links contour co-alignment and global axial motion at an apparent speed in the range of saccade-like eye movements.

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.

Microsaccades counteract visual fading during fixation.

Our eyes move continually, even while we fixate our gaze on an object. If fixational eye movements are counteracted, our perception of stationary objects fades completely, due to neural adaptation. Some studies have suggested that fixational microsaccades refresh retinal images, thereby preventing adaptation and fading. However, other studies disagree, and so the role of microsaccades remains unclear. Here, we correlate visibility during fixation to the occurrence of microsaccades. We asked subjects to indicate when Troxler fading of a peripheral target occurs, while simultaneously recording their eye movements with high precision. We found that before a fading period, the probability, rate, and magnitude of microsaccades decreased. Before transitions toward visibility, the probability, rate, and magnitude of microsaccades increased. These results reveal a direct link between suppression of microsaccades and fading and suggest a causal relationship between microsaccade production and target visibility during fixation.

Area V1 responses to illusory corner-folds in Vasarely's nested squares and the Alternating Brightness Star illusions.

Vasarely'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.

Microsaccades counteract perceptual filling-in.

Artificial scotomas positioned within peripheral dynamic noise fade perceptually during visual fixation (that is, the surrounding dynamic noise appears to fill-in the scotoma). Because the scotomas' edges are continuously refreshed by the dynamic noise background, this filling-in effect cannot be explained by low-level adaptation mechanisms (such as those that may underlie classical Troxler fading). We recently showed that microsaccades counteract Troxler fading and drive first-order visibility during fixation (S. Martinez-Conde, S. L. Macknik, X. G. Troncoso, & T. A. Dyar, 2006). Here we set out to determine whether microsaccades may counteract the perceptual filling-in of artificial scotomas and thus drive second-order visibility. If so, microsaccades may not only counteract low-level adaptation but also play a role in higher perceptual processes. We asked subjects to indicate, via button press/release, whether an artificial scotoma presented on a dynamic noise background was visible or invisible at any given time. The subjects' eye movements were simultaneously measured with a high precision video system. We found that increases in microsaccade production counteracted the perception of filling-in, driving the visibility of the artificial scotoma. Conversely, decreased microsaccades allowed perceptual filling-in to take place. Our results show that microsaccades do not solely overcome low-level adaptation mechanisms but they also contribute to maintaining second-order visibility during fixation.

Saccades and microsaccades during visual fixation, exploration, and search: foundations for a common saccadic generator.

Microsaccades are known to occur during prolonged visual fixation, but it is a matter of controversy whether they also happen during free-viewing. Here we set out to determine: 1) whether microsaccades occur during free visual exploration and visual search, 2) whether microsaccade dynamics vary as a function of visual stimulation and viewing task, and 3) whether saccades and microsaccades share characteristics that might argue in favor of a common saccade-microsaccade oculomotor generator. Human subjects viewed naturalistic stimuli while performing various viewing tasks, including visual exploration, visual search, and prolonged visual fixation. Their eye movements were simultaneously recorded with high precision. Our results show that microsaccades are produced during the fixation periods that occur during visual exploration and visual search. Microsaccade dynamics during free-viewing moreover varied as a function of visual stimulation and viewing task, with increasingly demanding tasks resulting in increased microsaccade production. Moreover, saccades and microsaccades had comparable spatiotemporal characteristics, including the presence of equivalent refractory periods between all pair-wise combinations of saccades and microsaccades. Thus our results indicate a microsaccade-saccade continuum and support the hypothesis of a common oculomotor generator for saccades and 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 V1's potential role in information processing and visual stability during eye movements.

Characteristics of Spontaneous Square-Wave Jerks in the Healthy Macaque Monkey during Visual Fixation.

Saccadic intrusions (SIs), predominantly horizontal saccades that interrupt accurate fixation, include square-wave jerks (SWJs; the most common type of SI), which consist of an initial saccade away from the fixation 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. SWJs have been also documented in monkeys with tectal and cerebellar etiologies, but no studies to date have investigated the occurrence of SWJs in healthy nonhuman primates. Here we set out to determine the characteristics of SWJs in healthy rhesus macaques (Macaca mulatta) during attempted fixation of a small visual target. Our results indicate that SWJs are common in healthy nonhuman primates. We moreover found primate SWJs to share many characteristics with human SWJs, including the relationship between the size of a saccade and its likelihood to be part of a SWJ. One main discrepancy between monkey and human SWJs was that monkey SWJs tended to be more vertical than horizontal, whereas human SWJs have a strong horizontal preference. Yet, our combined data indicate that primate and human SWJs play a similar role in fixation correction, suggesting that they share a comparable coupling mechanism at the oculomotor generation level. These findings constrain the potential brain areas and mechanisms underlying the generation of fixational saccades in human and nonhuman primates.

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.

Effect of stimulus width on simultaneous contrast.

Perceived brightness of a stimulus depends on the background against which the stimulus is set, a phenomenon known as simultaneous contrast. For instance, the same gray stimulus can look light against a black background or dark against a white background. Here we quantified the perceptual strength of simultaneous contrast as a function of stimulus width. Previous studies have reported that wider stimuli result in weaker simultaneous contrast, whereas narrower stimuli result in stronger simultaneous contrast. However, no previous research has quantified this relationship. Our results show a logarithmic relationship between stimulus width and perceived brightness. This relationship is well matched by the normalized output of a Difference-of-Gaussians (DOG) filter applied to stimuli of varied widths.

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.

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 Vasarely's art showcases the perceptual salience of corners, curvature and terminators. Several of these artworks and their implications for visual processing are discussed.

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.

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.

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

Vasarely's 'nested-squares' illusion shows that 90 degrees 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.