Susana Martinez-Conde

THE ROLE OF FIXATIONAL EYE MOVEMENTS IN VISUAL PERCEPTION

Our eyes continually move even while we fix our gaze on an object. Although these fixational eye movements have a magnitude that should make them visible to us, we are unaware of them. If fixational eye movements are counteracted, our visual perception fades completely as a result of neural adaptation. So, our visual system has a built-in paradox — we must fix our gaze to inspect the minute details of our world, but if we were to fixate perfectly, the entire world would fade from view. Owing to their role in counteracting adaptation, fixational eye movements have been studied to elucidate how the brain makes our environment visible. Moreover, because we are not aware of these eye movements, they have been studied to understand the underpinnings of visual awareness. Recent studies of fixational eye movements have focused on determining how visible perception is encoded by neurons in various visual areas of the brain.

Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys

When viewing a stationary object, we unconsciously make small, involuntary eye movements or ‘microsaccades’. If displacements of the retinal image are prevented, the image quickly fades from perception. To understand how microsaccades sustain perception, we studied their relationship to the firing of cells in primary visual cortex (V1). We tracked eye movements and recorded from V1 cells as macaque monkeys fixated. When an optimally oriented line was centered over a cells receptive field, activity increased after microsaccades. Moreover, microsaccades were better correlated with bursts of spikes than with either single spikes or instantaneous firing rate. These findings may help explain maintenance of perception during normal visual fixation.

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.

Task difficulty modulates the activity of specific neuronal populations in primary visual cortex

Spatial attention enhances our ability to detect stimuli at restricted regions of the visual field. This enhancement is thought to depend on the difficulty of the task being performed, but the underlying neuronal mechanisms for this dependency remain largely unknown. We found that task difficulty modulates neuronal firing rate at the earliest stages of cortical visual processing (area V1) in monkey (Macaca mulatta). These modulations were spatially specific: increasing task difficulty enhanced V1 neuronal firing rate at the focus of attention and suppressed it in regions surrounding the focus. Moreover, we found that response enhancement and suppression are mediated by distinct populations of neurons that differ in direction selectivity, spike width, interspike-interval distribution and contrast sensitivity. Our results provide strong support for center-surround models of spatial attention and suggest that task difficulty modulates the activity of specific populations of neurons in the primary visual cortex.

Fixational eye movements in normal and pathological vision

Most of our visual experience is driven by the eye movements we produce while we fixate our gaze. In a sense, our visual system thus has a built-in contradiction: when we direct our gaze at an object of interest, our eyes are never still. Therefore the perception, physiology, and computational modeling of fixational eye movements is critical to our understanding of vision in general, and also to the understanding of the neural computations that work to overcome neural adaptation in normal subjects as well as in clinical patients. Moreover, because we are not aware of our fixational eye movements, they can also help us understand the underpinnings of visual awareness. Research in the field of fixational eye movements faded in importance for several decades during the late 20th century. However, new electrophysiological and psychophysical data have now rejuvenated the field. The last decade has brought significant advances to our understanding of the neuronal and perceptual effects of fixational eye movements, with crucial implications for neural coding, visual awareness, and perception in normal and pathological vision. This chapter will review the type of neural activity generated by fixational eye movements at different levels in the visual system, as well as the importance of fixational eye movements for visual perception in normal vision and in visual disease. Special attention will be given to microsaccades, the fastest and largest type of fixational eye movement.

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.

The role of feedback in visual masking and visual processing

This paper reviews the potential role of feedback in visual masking, for and against. Our analysis reveals constraints for feedback mecha- nisms that limit their potential role in visual masking, and in all other general brain functions. We propose a feedforward model of visual masking, and provide a hypothesis to explain the role of feedback in visual masking and visual processing in general. We review the anato-my and physiology of feedback mechanisms, and propose that the massive ratio of feedback versus feedforward connections in the visual system may be explained solely by the critical need for top-down attentional modulation. We discuss the merits of visual masking as a tool to discover the neural correlates of consciousness, especially as compared to other popular illusions, such as binocular rivalry. Finally, we propose a new set of neurophysiological standards needed to establish whether any given neuron or brain circuit may be the neural substrate of awareness.

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.

Saccadic velocity as an arousal index in naturalistic tasks.

Experimental evidence indicates that saccadic metrics vary with task difficulty and time-on-task in naturalistic scenarios. We explore historical and recent findings on the correlation of saccadic velocity with task parameters in clinical, military, and everyday situations, and its potential role in ergonomics. We moreover discuss the hypothesis that changes in saccadic velocity indicate variations in sympathetic nervous system activation; that is, variations in arousal.

Dichoptic Visual Masking Reveals that Early Binocular Neurons Exhibit Weak Interocular Suppression: Implications for Binocular Vision and Visual Awareness

Visual masking effects are illusions in which a target is rendered invisible by a mask, which can either overlap or not overlap the target spatially and/or temporally. These illusions provide a powerful tool to study visibility and consciousness, object grouping, brightness perception, and much more. As such, the physiological mechanisms underlying the perception of masking are critically important to our understanding of visibility. Several models that require cortical circuits have been proposed previously to explain the mysterious spatial and timing effects associated with visual masking. Here we describe single-unit physiological experiments from the awake monkey that show that visual masking occurs in at least two separate and independent circuits, one that is binocular and one that is monocular (possibly even subcortical), without feedback from higher-level visual brain areas. These and other results together fail to support models of masking that require circuits found only in the cortex, but support our proposed model that suggests that simple ubiquitous lateral inhibition may itself be the fundamental mechanism that explains visual masking across multiple levels in the brain. We also show that area V1 neurons are dichoptic in terms of excitation, but monoptic in terms of inhibition. That is, responses within area V1 binocular neurons reveal that excitation to monocular targets is inhibited strongly only by masks presented to the same eye, and not by masks presented to the opposite eye. These results lead us to redefine the model for the first stage of binocular processing in the visual system, and may be crucial to interpreting the effects of other similar binocular and dichoptic stimulation paradigms, such as the binocular rivalry family of illusions.