Eye Speed Research Articles

A sensory-motor decoder that transforms neural responses in extrastriate area MT into smooth pursuit eye movements.

Visual motion drives smooth pursuit eye movements through a sensory-motor decoder that uses multiple parallel neural pathways to transform the population response in extrastriate area MT into movement. We evaluated the decoder by challenging pursuit in monkeys with reduced motion reliability created by reducing coherence of motion in patches of dots. Our strategy was to determine how reduced dot coherence changes the population response in MT. We then predicted the properties of a decoder that transforms the MT population response into dot coherence-induced deficits in the initiation of pursuit and steady-state tracking. During pursuit initiation, decreased dot coherence reduces MT population response amplitude without changing the preferred speed at its peak. The successful decoder reproduces the measured eye movements by multiplication of 1) the estimate of target speed from the peak of the population response with 2) visual-motor gain based on the amplitude of the population response. During steady-state tracking, the decoder that worked for pursuit initiation failed to reproduce the paradox that steady-state eye speeds do not accelerate to the target speed despite persistent image motion. It predicted eye acceleration to target speed even when monkeys' eye speeds were steady at well below the target speed. To account for the effect of dot coherence on steady-state eye speed, we postulate that the decoder uses sensory-motor gain to modulate the eye velocity positive feedback that normally sustains perfect steady-state tracking. Then, poor steady-state tracking persists because of balance between eye deceleration caused by low positive feedback gain and acceleration driven by MT.NEW & NOTEWORTHY By challenging a sensory-motor system with degraded sensory stimuli, we reveal how the sensory-motor decoder transforms the population response in extrastriate area MT into commands for the initiation and steady-state behavior of smooth pursuit eye movements. Conclusions are based on measuring population responses in MT for multiple target speeds and different levels of motion reliability and evaluating a decoder with a biologically motivated architecture to determine the decoder properties that create the measured eye movements.

Ocular following responses of the marmoset monkey are dependent on postsaccadic delay, spatiotemporal frequency, and saccade direction.

Ocular following is a short-latency, reflexive eye movement that tracks wide-field visual motion. It has been studied extensively in humans and macaques and is an appealing behavior for studying sensory-motor transformations in the brain because of its rapidity and rigidity. We explored ocular following in the marmoset, an emerging model in neuroscience because their lissencephalic brain allows direct access to most cortical areas for imaging and electrophysiological recordings. In three experiments, we tested ocular following responses in three adult marmosets. First, we varied the delay between saccade end and stimulus motion onset, from 10 to 300 ms. As in other species, tracking had shorter onset latencies and higher eye speeds with shorter postsaccadic delays. Second, using sine-wave grating stimuli, we explored the dependence of eye speed on spatiotemporal frequency. The highest eye speed was evoked at ∼16 Hz and ∼0.16 cycles per degree (cpd); however, the highest gain was elicited at ∼1.6 Hz and ∼1.2 cpd. The highest eye speed for each spatial frequency was observed at a different temporal frequency, but this interdependence was not consistent with complete speed tuning of the ocular following response. Finally, we found the highest eye speeds when saccade and stimulus motion directions were identical, although latencies were unaffected by direction difference. Our results showed qualitatively similar ocular following in marmosets, humans, and macaques, despite over an order of magnitude variation in body and eye size across species. This characterization will help future studies examining the neural basis of sensory-motor transformations.NEW & NOTEWORTHY Previous ocular following studies focused on humans and macaques. We examined the properties of ocular following responses in marmosets in three experiments, in which postsaccadic delay, spatial-temporal frequency of stimuli, and congruence of saccade and motion directions were manipulated. We have demonstrated short-latency ocular following in marmosets and discuss the similarities across three species that vary markedly in eye and head size. Our findings will help future studies examining the neural mechanism of sensory-motor transformations.

Retinal error signals and fluctuations in eye velocity influence oculomotor behavior in subsequent trials.

The oculomotor system makes use of an integration of previous stimulus velocities (the prior) and current sensory inputs to adjust initial eye speeds. The present study extended this research by investigating the roles of different retinal or extra-retinal signals for this process. To test for this, participants viewed movement sequences that all ended with the same test trial. Earlier in the sequence, the prior was manipulated by presenting targets that either had different velocities, different starting positions, or target movements designed to elicit differential oculomotor behavior (tracked with or without additional corrective saccades). Additionally, these prior targets could vary in terms of contrast to manipulate reliability. When the velocity of prior trials differed from test trials, the reliability-weighted integration of prior information was replicated. When the prior trials differed in starting position, significant effects on subsequent oculomotor behavior were only observed for the reliable target. Although there were also differences in eye velocity across the different manipulations, they could not explain the observed reliability-weighted integration. When comparing the same physical prior trials but tracked with additional corrective saccades, the eye velocity in the test trial also differed systematically (slower for forward saccades, and faster for backward saccades). The direction of the observed effect contradicts the expectations based on perceived speed and eye velocity, but can be predicted by a combination of retinal velocity and position error signals. Together, these results suggest that general fluctuations in eye velocity as well as retinal error signals are related to oculomotor behavior in subsequent trials.

Visual task complexity and eye movement patterns influence measures of human neurovascular coupling

Human neurovascular coupling research conventionally aims to selectively activate the posterior circulation using a visual task. Different research groups use divergent visual tasks ranging in complexity and eye movement patterns with potential confounding effects. To understand the role of task complexity and eye movement patterns in neurovascular coupling, we performed a series of experiments with visual tasks ranging in complexity, eye speed, and eye movement amplitude. Greater task complexity significantly reduced selectivity for the posterior circulation. Greater task amplitude (i.e. larger eye movements) increased selectivity. These findings are important when interpreting and designing neurovascular coupling investigations.

Different mechanisms for modulation of the initiation and steady-state of smooth pursuit eye movements.

Smooth pursuit eye movements are used by primates to track moving objects. They are initiated by sensory estimates of target speed represented in the middle temporal (MT) area of extrastriate visual cortex and then supported by motor feedback to maintain steady-state eye speed at target speed. Here, we show that reducing the coherence in a patch of dots for a tracking target degrades the eye speed both at the initiation of pursuit and during steady-state tracking, when eye speed reaches an asymptote well below target speed. The deficits are quantitatively different between the motor-supported steady-state of pursuit and the sensory-driven initiation of pursuit, suggesting separate mechanisms. The deficit in visually guided pursuit initiation could not explain the deficit in steady-state tracking. Pulses of target speed during steady-state tracking revealed lower sensitivities to image motion across the retina for lower values of dot coherence. However, sensitivity was not zero, implying that visual motion should still be driving eye velocity toward target velocity. When we changed dot coherence from 100% to lower values during accurate steady-state pursuit, we observed larger eye decelerations for lower coherences, as expected if motor feedback was reduced in gain. A simple pursuit model accounts for our data based on separate modulation of the strength of visual-motor transmission and motor feedback. We suggest that reduced dot coherence allows us to observe evidence for separate modulations of the gain of visual-motor transmission during pursuit initiation and of the motor corollary discharges that comprise eye velocity memory and support steady-state tracking.NEW & NOTEWORTHY We exploit low-coherence patches of dots to control the initiation and steady state of smooth pursuit eye movements and show that these two phases of movement are modulated separately by the reliability of visual motion signals. We conclude that the neural circuit for pursuit includes separate modulation of the strength of visual-motor transmission for movement initiation and of eye velocity positive feedback to support steady-state tracking.

Vestibular Testing: Patient Perceptions, Morbidity, and Opportunity Costs.

To characterize patient tolerance and nonmonetary cost burdens of vestibular testing. Rigorously acquired data are essential for patient counseling and to determine if proposed additions/modifications to current protocols improve quality, experience, and efficiencies of care. Prospective observational study. Tertiary center. 130 adults (67% women, mean age 55 yr), referred to audiology clinic for vestibular testing. Surveys administered to patients and audiologists immediately and 1 week following videonystagmography (VNG) with caloric and/or rotary chair (RC) testing. Symptoms, visual analog scale ratings of dizziness, distress, and nausea during testing; test completion; and opportunity costs (time, missed work). Seventy-five patients (58%) experienced undesirable symptoms during testing, including nausea (50%), vomiting (5%), and headaches (12%). Distress and nausea ratings during testing were low (<3/10), with RC ratings lower than VNG. Nineteen patients (15%) discontinued testing early, rating distress and nausea two to three times higher than those who completed testing (p < 0.05). Greater dizziness was associated with younger age and female sex, not migraine and total eye speed. Women had increased distress. Test times were 71 [23] and 26 [13] minutes for VNG with calorics and RC, respectively. Testing required 48% to miss work (range 2-120 h) and 78% obtained assistance to/from testing. Posttest symptoms included drowsiness/fatigue (44%), nausea (31%), and headache (33%). This work provides baseline patient tolerance data for vestibular testing. While eliciting distress ratings comparable to other in-office otolaryngology procedures, there are high frequencies of undesirable symptoms, posttest morbidity, and opportunity costs.

Eye movements during path integration.

Self‐motion induces spontaneous eye movements which serve the purpose of stabilizing the visual image on the retina. Previous studies have mainly focused on their reflexive nature and how the perceptual system disentangles visual flow components caused by eye movements and self‐motion. Here, we investigated the role of eye movements in distance reproduction (path integration). We used bimodal (visual‐auditory)‐simulated self‐motion: visual optic flow was paired with an auditory stimulus whose frequency was scaled with simulated speed. The task of the subjects in each trial was, first, to observe the simulated self‐motion over a certain distance (Encoding phase) and, second, to actively reproduce the observed distance using only visual, only auditory, or bimodal feedback (Reproduction phase). We found that eye positions and eye speeds were strongly correlated between the Encoding and the Reproduction phases. This was the case even when reproduction relied solely on auditory information and thus no visual stimulus was presented. We believe that these correlations are indicative of a contribution of eye movements to path integration.

Encoding of Reward and Decoding Movement from the Frontal Eye Field during Smooth Pursuit Eye Movements.

Expectation of reward potentiates sensorimotor transformations to drive vigorous movements. One of the main challenges in studying reward is to determine how representations of reward interact with the computations that drive behavior. We recorded activity in smooth pursuit neurons in the frontal eye field (FEF) of two male rhesus monkeys while controlling the eye speed by manipulating either reward size or target speed. The neurons encoded the different reward conditions more strongly than the different target speed conditions. This pattern could not be explained by differences in the eye speed, since the eye speed sensitivity of the neurons was also larger for the reward conditions. Pooling the responses by the preferred direction of the neurons attenuated the reward modulation and led to a tighter association between neural activity and behavior. Therefore, a plausible decoder such as the population vector could explain how the FEF both drives behavior and encodes reward beyond behavior.SIGNIFICANCE STATEMENT Motor areas combine sensory and reward information to drive movement. To disambiguate these sources, we manipulated the speed of smooth pursuit eye movements by controlling either the size of the reward or the speed of the visual motion signals. We found that the relationship between activity in frontal eye field and eye kinematics varied: the eye speed sensitivity was larger for the different reward conditions than for the different target speed conditions. Decoders that pooled signals by the preferred direction of the neurons attenuated the reward modulations. These decoders may indicate how reward can be both encoded beyond eye kinematics at the single neuron level and drive movement at the population level.

Total caloric eye speed in patients with vestibular migraine

PurposeVestibular migraine is a common cause of dizziness that lacks a known objective test. This study examined total eye speed on caloric testing as a diagnostic marker for vestibular migraine. Materials and methodsRetrospective chart review of patients seen in a tertiary otologic practice between 2004 and 2016 who had undergone caloric testing with water irrigation and had a diagnosis of vestibular migraine (n=34). A group of patients with benign paroxysmal positional vertigo (n=10) were used as a control group. Patients were grouped into quartiles based on total eye speed. ResultsOnly patients in the lowest quartile (total eye speed<79) had a diagnosis of vestibular migraine. All other quartiles included a mix of control and vestibular migraine patients. ConclusionLow total eye speed may be suggestive of a diagnosis of vestibular migraine, but most patients with vestibular migraine do not have low total eye speed.

Control of the strength of visual-motor transmission as the mechanism of rapid adaptation of priors for Bayesian inference in smooth pursuit eye movements.

Bayesian inference provides a cogent account of how the brain combines sensory information with "priors" based on past experience to guide many behaviors, including smooth pursuit eye movements. We now demonstrate very rapid adaptation of the pursuit system's priors for target direction and speed. We go on to leverage that adaptation to outline possible neural mechanisms that could cause pursuit to show features consistent with Bayesian inference. Adaptation of the prior causes changes in the eye speed and direction at the initiation of pursuit. The adaptation appears after a single trial and accumulates over repeated exposure to a given history of target speeds and directions. The influence of the priors depends on the reliability of visual motion signals: priors are more effective against the visual motion signals provided by low-contrast vs. high-contrast targets. Adaptation of the direction prior generalizes to eye speed and vice versa, suggesting that both priors could be controlled by a single neural mechanism. We conclude that the pursuit system can learn the statistics of visual motion rapidly and use those statistics to guide future behavior. Furthermore, a model that adjusts the gain of visual-motor transmission predicts the effects of recent experience on pursuit direction and speed, as well as the specifics of the generalization between the priors for speed and direction. We suggest that Bayesian inference in pursuit behavior is implemented by distinctly non-Bayesian internal mechanisms that use the smooth eye movement region of the frontal eye fields to control of the gain of visual-motor transmission.NEW & NOTEWORTHY Bayesian inference can account for the interaction between sensory data and past experience in many behaviors. Here, we show, using smooth pursuit eye movements, that the priors based on past experience can be adapted over a very short time frame. We also show that a single model based on direction-specific adaptation of the strength of visual-motor transmission can explain the implementation and adaptation of priors for both target direction and target speed.

Evidence that smooth pursuit velocity, not eye position, modulates alpha and beta oscillations in human middle temporal cortex.

Suppression of 5-25 Hz oscillations have been observed in MT+ during pursuit eye movements, suggesting oscillations that play a role in oculomotor control and/or the integration of extraretinal signals during pursuit. The amplitude of these rhythms appears to covary with head-centered eye position, but an alternative is that they depend on a velocity signal that lags the movement of the eyes. To investigate, we explored how alpha and beta amplitude changes related to ongoing eye movement depended on pursuit at different eccentricities. The results revealed largely identical patterns of modulation in the alpha and beta amplitude, irrespective of the eccentricity at which the pursuit eye movement was performed. The signals we measured therefore do not depend on head-centered position. A second experiment was designed to investigate whether the alpha and beta oscillations depended on the direction of pursuit, as opposed to just speed. We found no evidence that alpha or beta oscillations depended on direction, but there was a significant effect of eye speed on the magnitude of the beta suppression. This suggests distinct functional roles for alpha and beta suppression in pursuit behavior.

Saccade-induced image motion cannot account for post-saccadic enhancement of visual processing in primate MST.

Primates use saccadic eye movements to make gaze changes. In many visual areas, including the dorsal medial superior temporal area (MSTd) of macaques, neural responses to visual stimuli are reduced during saccades but enhanced afterwards. How does this enhancement arise—from an internal mechanism associated with saccade generation or through visual mechanisms activated by the saccade sweeping the image of the visual scene across the retina? Spontaneous activity in MSTd is elevated even after saccades made in darkness, suggesting a central mechanism for post-saccadic enhancement. However, based on the timing of this effect, it may arise from a different mechanism than occurs in normal vision. Like neural responses in MSTd, initial ocular following eye speed is enhanced after saccades, with evidence suggesting both internal and visually mediated mechanisms. Here we recorded from visual neurons in MSTd and measured responses to motion stimuli presented soon after saccades and soon after simulated saccades—saccade-like displacements of the background image during fixation. We found that neural responses in MSTd were enhanced when preceded by real saccades but not when preceded by simulated saccades. Furthermore, we also observed enhancement following real saccades made across a blank screen that generated no motion signal within the recorded neurons' receptive fields. We conclude that in MSTd the mechanism leading to post-saccadic enhancement has internal origins.

5.2: Simulation of Color Breakup Perception using Eye‐Tracking Data

Color breakup (CBU) is an artifact caused by a field‐sequential color system. A proper understanding of the CBU‐perception mechanism is essential in order to develop high‐quality displays. This paper reports on the development of a precise simulator of CBU perception due to saccades using eye‐tracking data. In experiments conducted, actual eye speeds were measured through subjective experiments of CBU evaluation. The results indicate that the simulated CBU images based on eye‐tracking measurements realize higher reproducibility on human perception than the conventional approach.

Smooth pursuit preparation modulates neuronal responses in visual areas MT and MST

Primates are able to track small moving visual targets using smooth pursuit eye movements. Target motion for smooth pursuit is signaled by neurons in visual cortical areas MT and MST. In this study, we trained monkeys to either initiate or withhold smooth pursuit in the presence of a moving target to test whether this decision was reflected in the relative strength of "go" and "no-go" processes. We found that the gain of the motor response depended strongly on whether monkeys were instructed to initiate or withhold pursuit, thus demonstrating voluntary control of pursuit initiation. We found that the amplitude of the neuronal response to moving targets in areas MT and MST was also significantly lower on no-go trials (by 2.1 spikes/s on average). The magnitude of the neural response reduction was small compared with the behavioral gain reduction. There were no significant differences in neuronal direction selectivity, spatial selectivity, or response reliability related to pursuit initiation or the absence thereof. Variability in eye speed was negatively correlated with firing rate variability after target motion onset during go trials but not during no-go trials, suggesting that MT and MST activity represents an error signal for a negative feedback controller. We speculate that modulation of the visual motion signals in areas MT and MST may be one of the first visual cortical events in the initiation of smooth pursuit and that the small early response modulation may be amplified to produce an all-or-none motor response by downstream areas.

A unified signal of attentional control.

A unified signal of attentional control.

Motion sensitivity and caloric responsiveness in vestibular migraine and Meniere's disease

We examined whether scores on a motion sensitivity questionnaire (MSQ) could distinguish between vestibular migraine (VM) and Meniere's disease (MD). As a secondary goal, we examined whether scores on the MSQ correlated with results from caloric testing. This study administered a telephone questionnaire to subjects who met clinical criteria for vestibular migraine, Meniere's disease, and controls. A MSQ was administered to 20 subjects meeting American Academy of Otolaryngology (AAO) criteria for MD, 30 subjects meeting Neuhauser criteria for both probable vestibular migraine (pVM) and definite vestibular migraine (dVM), and 22 controls. The average score on the MSQ was 5.9 for VM, 4.25 for MD, and 0.4 for controls. Both the VM and MD scored significantly higher than the controls (P = 0.0001), but results were not statistically different from each other (P = 0.17). However, the average score for subjects with dVM was 7.1, which was significantly higher than subjects with pVM whose average score was 4.2 (P = 0.045) and higher than subjects with MD (P = 0.048). When each question of the MSQ was analyzed, motion sensitivity to riding in a car was found to be significantly different between VM (average score 1.1) and MD (average score 0.5), with P value of 0.048. Scores of MSQ did not correlate with the total eye speed (TES) on caloric testing. Subjects with VM and MD had elevated levels of motion sensitivity compared to controls. Subjects with VM had more motion sensitivity to riding in a car than those with MD, but their TES was not different. 3b.

The Interaction of Bayesian Priors and Sensory Data and Its Neural Circuit Implementation in Visually Guided Movement

Sensory-motor behavior results from a complex interaction of noisy sensory data with priors based on recent experience. By varying the stimulus form and contrast for the initiation of smooth pursuit eye movements in monkeys, we show that visual motion inputs compete with two independent priors: one prior biases eye speed toward zero; the other prior attracts eye direction according to the past several days' history of target directions. The priors bias the speed and direction of the initiation of pursuit for the weak sensory data provided by the motion of a low-contrast sine wave grating. However, the priors have relatively little effect on pursuit speed and direction when the visual stimulus arises from the coherent motion of a high-contrast patch of dots. For any given stimulus form, the mean and variance of eye speed covary in the initiation of pursuit, as expected for signal-dependent noise. This relationship suggests that pursuit implements a trade-off between movement accuracy and variation, reducing both when the sensory signals are noisy. The tradeoff is implemented as a competition of sensory data and priors that follows the rules of Bayesian estimation. Computer simulations show that the priors can be understood as direction-specific control of the strength of visual-motor transmission, and can be implemented in a neural-network model that makes testable predictions about the population response in the smooth eye movement region of the frontal eye fields.

Dramatic impairment of prediction due to frontal lobe degeneration

Prediction is essential for motor function in everyday life. For instance, predictive mechanisms improve the perception of a moving target by increasing eye speed anticipatively, thus reducing motion blur on the retina. Subregions of the frontal lobes play a key role in eye movements in general and in smooth pursuit in particular, but their precise function is not firmly established. Here, the role of frontal lobes in the timing of predictive action is demonstrated by studying predictive smooth pursuit during transient blanking of a moving target in mild frontotemporal lobar degeneration (FTLD) and Alzheimer's disease (AD) patients. While control subjects and AD patients predictively reaccelerated their eyes before the predicted time of target reappearance, FTLD patients did not. The difference was so dramatic (classification accuracy >90%) that it could even lead to the definition of a new biomarker. In contrast, anticipatory eye movements triggered by the disappearance of the fixation point were still present before target motion onset in FTLD patients and visually guided pursuit was normal in both patient groups compared with controls. Therefore, FTLD patients were only impaired when the predicted timing of an external event was required to elicit an action. These results argue in favor of a role of the frontal lobes in predictive movement timing.

Refractive lens exchange for a multifocal intraocular lens with a surface-embedded near section in mild to moderate anisometropic amblyopic patients

To evaluate visual and refractive outcomes in amblyopic patients who had bilateral implantation of a multifocal intraocular lens (IOL) with a surface-embedded near section. Cathedral Eye Clinic, Belfast, Northern Ireland, United Kingdom. Comparative case series. Anisometropic amblyopic patients having bilateral implantation of Lentis Mplus multifocal IOLs were examined for distance and near visual acuities, contrast sensitivity, defocus curves, extent of crowding, reading speed, stereoacuity, and Quality of Vision (QoV) questionnaire scores preoperatively and at 3-month intervals during 12 months. A +3.00 diopter (D) reading addition IOL was used in all eyes. Twenty-eight eyes (14 patients) (mean age 59.4 years) were included. In the nonamblyopic eye, the mean uncorrected distance visual acuity (UDVA) was 0.16 logMAR ± 0.17 (SD), the mean corrected distance visual acuity (CDVA) was 0.02 ± 0.07 logMAR, and the mean near acuity was M 0.5 (Jaeger [J] 2 = logRAD 0.1) or better. In the amblyopic eye, the means were 0.30 ± 0.14 logMAR, 0.21 ± 0.11 logMAR, and M 0.8 (J4 = logRAD 0.3) or better, respectively. Bilateral reading speeds (mean 137.73 ± 28.7 words per minute [wpm]) surpassed unilateral nonamblyopic eye speeds (mean 130.6 ± 29.4 wpm). The mean QoV scores improved from 7.78 ± 10.23 preoperatively to 1.92 ± 5.21 at 12 months. No glare or halos were reported; 1 patient had mild starburst symptoms at 1 year. Patients rated distance and near vision as excellent. Anisometropic amblyopic patients may benefit from bilateral implantation of the multifocal IOL; no unwanted side effects were detected.

Visual Stimulation Tests: Testing Methods, Interpretation and Pitfalls

An eye tracking test (ETT), saccade, optokinetic nystagmus (OKN) test and optokinetic-after nystagmus (OKAN) test are the visual stimulation tests most commonly performed. In this article, I will examine the methods, interpretation of the results and pitfalls of those tests. The function of smooth pursuit is evaluated in an ETT. Smooth pursuit is very susceptible to central nervous system damage. Because smooth pursuit is easily affected by the age and arousal, these conditions should be considered in evaluating the results of an ETT. In saccade, the latent time, maximal eye speed and accuracy are evaluated. Saccade may be occasionally the only test that can detect the failure of the central nervous system. OKN is divided into two types by the instructions to the examinees. When examinees are instructed to look at the stripes so as to count them, one by one, OKN is Schau-Nystagmus. When examinees are instructed to stare vacantly in front of them, OKN is Stier-Nystagmus. Schau-Nystagmus differs significantly from Steir-Nystagmus in terms of the speed and form of nystagmus. It is important to clarify the instructions given to the patient. In a qualitative analysis of OKN, nystagmus are superimposed over the stripes with a computer and pursuit movements and catching movements of the target are separately examined. OKN is able to be evaluated in detail in a qualitative analysis, whereas the optokinetic pattern test (OKP) is a clinically convenient method for visually detecting slow and fast phase asymmetry of OKN. OKAN has been thought to be concerned with the velocity storage mechanism. Therefore OKAN test is significant in the study of the function of the peripheral and central vestibular system.