Saccadic facilitation by modulation of microsaccades in natural backgrounds.
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ABSTRACT:
SUBMITTER: Sinn P
PROVIDER: S-EPMC3089726 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:When 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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Project description: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.
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Project description:The fundamental role of the visual system is to guide behavior in natural environments. To optimize information transmission, many animals have evolved a non-homogeneous retina and serially sample visual scenes by saccadic eye movements. Such eye movements, however, introduce high-speed retinal motion and decouple external and internal reference frames. Until now, these processes have only been studied with unnatural stimuli, eye movement behavior, and tasks. These experiments confound retinotopic and geotopic coordinate systems and may probe a non-representative functional range. Here we develop a real-time, gaze-contingent display with precise spatiotemporal control over high-definition natural movies. In an active condition, human observers freely watched nature documentaries and indicated the location of periodic narrow-band contrast increments relative to their gaze position. In a passive condition under central fixation, the same retinal input was replayed to each observer by updating the video's screen position. Comparison of visual sensitivity between conditions revealed three mechanisms that the visual system has adapted to compensate for peri-saccadic vision changes. Under natural conditions we show that reduced visual sensitivity during eye movements can be explained simply by the high retinal speed during a saccade without recourse to an extra-retinal mechanism of active suppression; we give evidence for enhanced sensitivity immediately after an eye movement indicative of visual receptive fields remapping in anticipation of forthcoming spatial structure; and we demonstrate that perceptual decisions can be made in world rather than retinal coordinates.
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Project description:The interest in saccadic IOR is funneled by the hypothesis that it serves a clear functional purpose in the selection of fixation points: the facilitation of foraging. In this study, we arrive at a different interpretation of saccadic IOR. First, we find that return saccades are performed much more often than expected from the statistical properties of saccades and saccade pairs. Second, we find that fixation durations before a saccade are modulated by the relative angle of the saccade, but return saccades show no sign of an additional temporal inhibition. Thus, we do not find temporal saccadic inhibition of return. Interestingly, we find that return locations are more salient, according to empirically measured saliency (locations that are fixated by many observers) as well as stimulus dependent saliency (defined by image features), than regular fixation locations. These results and the finding that return saccades increase the match of individual trajectories with a grand total priority map evidences the return saccades being part of a fixation selection strategy that trades off exploration and exploitation.
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Project description:Recent evidence suggests that microsaccades are causally linked to the attention-related modulation of neurons-specifically, that microsaccades toward the attended location are required for the subsequent changes in firing rate. These findings have raised questions about whether attention-related modulation is due to different states of attention as traditionally assumed or might instead be a secondary effect of microsaccades. Here, in two rhesus macaques, we tested the relationship between microsaccades and attention-related modulation in the superior colliculus (SC), a brain structure crucial for allocating attention. We found that attention-related modulation emerged even in the absence of microsaccades, was already present prior to microsaccades toward the cued stimulus, and persisted through the suppression of activity that accompanied all microsaccades. Nonetheless, consistent with previous findings, we also found significant attention-related modulation when microsaccades were directed toward, rather than away from, the cued location. Thus, despite the clear links between microsaccades and attention, microsaccades are not necessary for attention-related modulation, at least not in the SC. They do, however, provide an additional marker for the state of attention, especially at times when attention is shifting from one location to another.
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Project description:Saccadic eye movements play a central role in primate vision. Yet, relatively little is known about their effects on the neural processing of visual inputs. Here we examine this question in primary visual cortex (V1) using receptive-field-based models, combined with an experimental design that leaves the retinal stimulus unaffected by saccades. This approach allows us to analyse V1 stimulus processing during saccades with unprecedented detail, revealing robust perisaccadic modulation. In particular, saccades produce biphasic firing rate changes that are composed of divisive gain suppression followed by an additive rate increase. Microsaccades produce similar, though smaller, modulations. We furthermore demonstrate that this modulation is likely inherited from the LGN, and is driven largely by extra-retinal signals. These results establish a foundation for integrating saccades into existing models of visual cortical stimulus processing, and highlight the importance of studying visual neuron function in the context of eye movements.
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Project description:Despite strong evidence to the contrary in the literature, microsaccades are overwhelmingly described as involuntary eye movements. Here we show in both human subjects and monkeys that individual microsaccades of any direction can easily be triggered: (1) on demand, based on an arbitrary instruction, (2) without any special training, (3) without visual guidance by a stimulus, and (4) in a spatially and temporally accurate manner. Subjects voluntarily generated instructed "memory-guided" microsaccades readily, and similarly to how they made normal visually-guided ones. In two monkeys, we also observed midbrain superior colliculus neurons that exhibit movement-related activity bursts exclusively for memory-guided microsaccades, but not for similarly-sized visually-guided movements. Our results demonstrate behavioral and neural evidence for voluntary control over individual microsaccades, supporting recently discovered functional contributions of individual microsaccade generation to visual performance alterations and covert visual selection, as well as observations that microsaccades optimize eye position during high acuity visually-guided behavior.
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Project description:Saccadic peak velocity increases in a stereotyped manner with the amplitude of eye movements. This relationship, known as the main sequence, has classically been considered to be fixed, although several recent studies have demonstrated that velocity can be modulated to some extent by external incentives. However, the ability to voluntarily control saccadic velocity and its association with motivation has yet to be investigated. Here, in three separate experimental paradigms, we measured the effects of incentivisation on saccadic velocity, reaction time and preparatory pupillary changes in 53 young healthy participants. In addition, the ability to voluntarily modulate saccadic velocity with and without incentivisation was assessed. Participants varied in their ability to increase and decrease the velocity of their saccades when instructed to do so. This effect correlated with motivation level across participants, and was further modulated by addition of monetary reward and avoidance of loss. The findings show that a degree of voluntary control of saccadic velocity is possible in some individuals, and that the ability to modulate peak velocity is associated with intrinsic levels of motivation.
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Project description:To investigate mechanisms by which reward modulates target selection, we studied the behavioral effects of perturbing dopaminergic activity within the frontal eye field (FEF) of monkeys performing a saccadic choice task and simulated the effects using a plausible cortical network. We found that manipulation of FEF activity either by blocking D1 receptors (D1Rs) or by stimulating D2 receptors (D2Rs) increased the tendency to choose targets in the response field of the affected site. However, the D1R manipulation decreased the tendency to repeat choices on subsequent trials, whereas the D2R manipulation increased that tendency. Moreover, the amount of shift in target selection resulting from the two manipulations correlated in opposite ways with the baseline stochasticity of choice behavior. Our network simulation results suggest that D1Rs influence target selection mainly through their effects on the strength of inputs to the FEF and on recurrent connectivity, whereas D2Rs influence the excitability of FEF output neurons. Altogether, these results reveal dissociable dopaminergic mechanisms influencing target selection and suggest how reward can influence adaptive choice behavior via prefrontal dopamine.
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Project description:The lateralisation of 8-12 Hz alpha activity is a canonical signature of human spatial cognition that is typically studied under strict fixation requirements. Yet, even during attempted fixation, the brain produces small involuntary eye movements known as microsaccades. Here we report how spontaneous microsaccades - made in the absence of incentives to look elsewhere - can themselves drive transient lateralisation of EEG alpha power according to microsaccade direction. This transient lateralisation of posterior alpha power occurs similarly following start and return microsaccades and is, at least for start microsaccades, driven by increased alpha power ipsilateral to microsaccade direction. This reveals new links between spontaneous microsaccades and human electrophysiological brain activity. It highlights how microsaccades are an important factor to consider in studies relating alpha activity - including spontaneous fluctuations in alpha activity - to spatial cognition, such as studies on visual attention, anticipation, and working memory.
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