Stephen L. Macknik

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.

Neuronal correlates of visibility and invisibility in the primate visual system.

A brief visual target stimulus may be rendered invisible if it is immediately preceded or followed by another stimulus. This class of illusions, known as visual masking, may allow insights into the neural mechanisms that underlie visual perception. We have therefore explored the temporal characteristics of masking illusions in humans, and compared them with corresponding neuronal responses in the primary visual cortex of awake and anesthetized monkeys. Stimulus parameters that in humans produce forward masking (in which the mask precedes the target) suppress the transient on-response to the target in monkey visual cortex. Those that produce backward masking (in which the mask comes after the target) inhibit the transient after-discharge, the excitatory response that occurs just after the disappearance of the target. These results suggest that, for targets that can be masked (those of short duration), the transient neuronal responses associated with onset and turning off of the target may be important in its visibility.

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.

The function of bursts of spikes during visual fixation in the awake primate lateral geniculate nucleus and primary visual cortex

When images are stabilized on the retina, visual perception fades. During voluntary visual fixation, however, constantly occurring small eye movements, including microsaccades, prevent this fading. We previously showed that microsaccades generated bursty firing in the primary visual cortex (area V-1) in the presence of stationary stimuli. Here we examine the neural activity generated by microsaccades in the lateral geniculate nucleus (LGN), and in the area V-1 of the awake monkey, for various functionally relevant stimulus parameters. During visual fixation, microsaccades drove LGN neurons by moving their receptive fields across a stationary stimulus, offering a likely explanation of how microsaccades block fading during normal fixation. Bursts of spikes in the LGN and area V-1 were associated more closely than lone spikes with preceding microsaccades, suggesting that bursts are more reliable than are lone spikes as neural signals for visibility. In area V-1, microsaccade-generated activity, and the number of spikes per burst, was maximal when the bar stimulus centered over a receptive field matched the cells optimal orientation. This suggested burst size as a neural code for stimuli optimality (and not solely stimuli visibility). As expected, burst size did not vary with stimulus orientation in the LGN. To address the effectiveness of microsaccades in generating neural activity, we compared activity correlated with microsaccades to activity correlated with flashing bars. Onset responses to flashes were about 7 times larger than the responses to the same stimulus moved across the cells receptive fields by microsaccades, perhaps because of the relative abruptness of flashes.

The impact of microsaccades on vision: towards a unified theory of saccadic function

When we attempt to fix our gaze, our eyes nevertheless produce so-called fixational eye movements, which include microsaccades, drift and tremor. Fixational eye movements thwart neural adaptation to unchanging stimuli and thus prevent and reverse perceptual fading during fixation. Over the past 10 years, microsaccade research has become one of the most active fields in visual, oculomotor and even cognitive neuroscience. The similarities and differences between microsaccades and saccades have been a most intriguing area of study, and the results of this research are leading us towards a unified theory of saccadic and microsaccadic function.

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.

Attention and awareness in stage magic: turning tricks into research

Just as vision scientists study visual art and illusions to elucidate the workings of the visual system, so too can cognitive scientists study cognitive illusions to elucidate the underpinnings of cognition. Magic shows are a manifestation of accomplished magic performers deep intuition for and understanding of human attention and awareness. By studying magicians and their techniques, neuroscientists can learn powerful methods to manipulate attention and awareness in the laboratory. Such methods could be exploited to directly study the behavioural and neural basis of consciousness itself, for instance through the use of brain imaging and other neural recording techniques.

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.

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.