Intersaccadic Interval Research Articles

Fast feature- and category-related parafoveal previewing support free visual exploration.

While humans typically saccade every ∼250 ms in natural settings, studies on vision tend to prevent or restrict eye movements. As it takes ∼50 ms to initiate and execute a saccade, this leaves only ∼200 ms to identify the fixated object and select the next saccade goal. How much detail can be derived about parafoveal objects in this short time interval, during which foveal processing and saccade planning both occur? Here, we had male and female human participants freely explore a set of natural images while we recorded magnetoencephalography and eye movements. Using multivariate pattern analysis, we demonstrate that future parafoveal images could be decoded at the feature and category level with peak decoding at ∼110 ms and ∼165 ms respectively, while the decoding of fixated objects at the feature and category level peaked at ∼100 ms and ∼145 ms. The decoding of features and categories was contingent on the objects being saccade goals. In sum, we provide insight on the neuronal mechanism of pre-saccadic attention by demonstrating that feature and category specific information of foveal and parafoveal objects can be extracted in succession within a ∼200 ms intersaccadic interval. These findings rule out strict serial or parallel processing accounts but are consistent with a pipeline mechanism in which foveal and parafoveal objects are processed in parallel but at different levels in the visual hierarchy.Significance Statement We provide neural evidence that future parafoveal saccade goals are processed surprisingly quickly at the feature and the category level before we saccade to them. Specifically, using multivariate pattern analysis applied to magnetoencephalography and eye-tracking data, we found that information about the colour and the category of parafoveal objects emerged at ∼110 ms and ∼165 ms respectively, with the same information about foveal objects emerging ∼100 ms and ∼145 ms. Our findings provide novel insight into the neuronal dynamics of parafoveal previewing during free visual exploration. The dynamics rule out strict serial or parallel processing, but are consistent with a pipelining mechanism in which foveal and parafoveal objects are processed in parallel but at different levels in the visual hierarchy.

Oculomotor randomness is higher in autistic children and increases with the severity of symptoms.

A variety of studies have suggested that at least some children with autism spectrum disorder (ASD) view the world differently. Differences in gaze patterns as measured by eye tracking have been demonstrated during visual exploration of images and natural viewing of movies with social content. Here we analyzed the temporal randomness of saccades and blinks during natural viewing of movies, inspired by a recent measure of "randomness" applied to micro-movements of the hand and head in ASD (Torres et al., 2013; Torres & Denisova, 2016). We analyzed a large eye-tracking dataset of 189 ASD and 41 typically developing (TD) children (1-11 years old) who watched three movie clips with social content, each repeated twice. We found that oculomotor measures of randomness, obtained from gamma parameters of inter-saccade intervals (ISI) and blink duration distributions, were significantly higher in the ASD group compared with the TD group and were correlated with the ADOS comparison score, reflecting increased "randomness" in more severe cases. Moreover, these measures of randomness decreased with age, as well as with higher cognitive scores in both groups and were consistent across repeated viewing of each movie clip. Highly "random" eye movements in ASD children could be associated with high "neural variability" or noise, poor sensory-motor control, or weak engagement with the movies. These findings could contribute to the future development of oculomotor biomarkers as part of an integrative diagnostic tool for ASD.

Tracking a moving visual target in the rhesus monkey: influence of the occurrence frequency of the target path.

Following previous studies documenting the ability to generate anticipatory responses, we tested whether the repeated motion of a visual target along the same path affected its oculomotor tracking. In six rhesus monkeys, we evaluated how the frequency of a target path influenced the onset, accuracy, and velocity of eye movements. Three hundred milliseconds after its extinction, a central target reappeared and immediately moved toward the periphery in four possible (oblique) directions and at a constant speed (20°/s or 40°/s). During each daily session, the frequency of one motion direction was either uncertain (25% of trials) or certain (100% of trials). Our results show no reduction of saccade latency between the two sessions. No express saccades were observed in either session. A slow eye movement started after target onset (presaccadic glissade) and its velocity was larger during the "certain" sessions only with the 40°/s target. No anticipatory eye movement was observed. Longer intersaccadic intervals were found during the "certain" sessions but the postsaccadic pursuit velocity exhibited no change. No correlation was found between the accuracy and precision of saccades (interceptive or catch-up) and the postsaccadic pursuit velocity. Repeatedly tracking a target that moves always along the same path does not favor the generation of anticipatory eye movements, saccadic or slow. Their occurrence is not spontaneous but seems to require preliminary training. Finally, for both sessions, the lack of correlation between the saccade-related and pursuit-related kinematic parameters is consistent with separate control of saccadic and slow eye movements.NEW & NOTEWORTHY Following previous studies documenting anticipatory movements, we investigated how the frequency of occurrence of a target path influenced the generation of tracking eye movements. When present, the effects were small. The limited performance that we found suggests that anticipatory responses require preliminary training, in which case, they should not be considered as a behavioral marker of the primates' ability to extrapolate but the outcome of learning and remembering past experience.

Opsoclonus and ocular flutter: evaluation and management.

Opsoclonus and ocular flutter are saccadic intrusions characterized by spontaneous, back-to-back, fast eye movements (saccades) that oscillate about the midline of central visual fixation without intervening inter-saccadic intervals. When this type of movement occurs exclusively in the horizontal plane, it is called ocular flutter. When it occurs in multiple planes (i.e. horizontal, vertical, and torsional) it is called opsoclonus. The most common etiologic categories are parainfectious and paraneoplastic diseases. Less common are toxic-metabolic, traumatic, or idiopathic origins. The mechanism of these movements relates to dysfunction of brainstem and cerebellar machinery involved in the generation of saccades. In this review, we discuss the characteristics of opsoclonus and ocular flutter, describe approaches to clinical evaluation and management of the patient with opsoclonus and ocular flutter, and review approaches to therapeutic intervention. Recent publications demonstrated eye position-dependent opsoclonus present only in left gaze, which may be related to dysfunction of frontal eye fields or structures in the cerebellar vermis. Opsoclonus and ocular flutter originate from a broad array of neuropathologies and have value from both a neuroanatomic and etiologic perspective.

Opsoclonus Induced by Head-Shaking in Vestibular Migraine.

Opsoclonus refers to saccadic oscillations without an intersaccadic interval occurring in multiple planes. Opsoclonus mostly indicates dysfunction of the brainstem or cerebellum. We report opsoclonus induced by horizontal head-shaking without other signs of brainstem or cerebellar dysfunction in two patients with vestibular migraine (VM). The development of opsoclonus after horizontal head-shaking indicates unstable or hyperactive neural circuits between the excitatory and inhibitory saccadic premotor burst neurons in these patients with VM.

Multiple step saccades are generated by internal real-time saccadic error correction.

Multiple step saccades (MSSs) are an atypical form of saccade that consists of a series of small-amplitude saccades. It has been argued that the mechanism for generating MSS is due to the automatic saccadic plan. This argument was based on the observation that trials with MSS had shorter saccadic latency than trials without MSS in the reactive saccades. However, the validity of this argument has never been verified by other saccadic tasks. Alternatively, we and other researchers have speculated that the function of MSS is the same as that of the corrective saccade (CS), i.e., to correct saccadic errors. Thus, we propose that the function of the MSS is also to rectify saccadic errors and generated by forward internal models. The objective of the present study is to examine whether the automatic theory is universally applicable for the generation of MSSs in various saccadic tasks and to seek other possible mechanisms, such as error correction by forward internal models. Fifty young healthy subjects (YHSs) and fifty elderly healthy subjects (EHSs) were recruited in the present study. The task paradigms were prosaccade (PS), anti-saccade (AS) and memory-guided saccade (MGS) tasks. Saccadic latency in trials with MSS was shorter than without MSS in the PS task but similar in the AS and MGS tasks. The intersaccadic intervals (ISI) were similar among the three tasks in both YHSs and EHSs. Our results indicate that the automatic theory is not a universal mechanism. Instead, the forward internal model for saccadic error correction might be an important mechanism.

Binocular, accommodative and oculomotor alterations in multiple sclerosis

AbstractMultiple sclerosis (MS) is an acquired demyelinating and inflammatory neurodegenerative disease affecting the central nervous system (CNS). Clinical and subclinical ocular disturbances occur in almost all patients with MS. Among them, oculomotor, accommodative and binocular alterations have been reported in MS. Our research group has conducted a complete analysis of the visual and oculomotor function in several researches with MS patients conducted in the last 4 years, obtaining a characterization of some visual aspects of the patient with MS. Concerning the binocular function, several alterations have been detected in MS patients, with divergence at near distance and stereopsis the most affected parameters. Likewise, MS patients with previous optic neuritis present worse binocular vision. Symptomatology compatible with convergence insufficiency measured with the CISS (Convergence Insufficiency Symptom Survey) is frequently reported by MS patients, but not supported by signs that show clear trend to esophoria at near. This discrepancy between the signs and symptoms could be due to the peculiarities of the CISS questionnaire, including items that are also related to the cognitive function and other ocular abnormalities.Oculomotor alterations have been reported also in patients with multiple sclerosis (MS), especially saccadic dysfunctions. The indirect analysis of horizontal saccades with the Developmental Eye Movement (DEM) and King‐Devick tests shows that are affected by MS, with more level of alteration if there has been a previous episode of optic neuritis. Similar findings have been also reported by other authors using objective eye tracking or video‐oculographic systems. Specifically, the most reported saccadic alterations in advanced MS and clinically isolated syndrome (CIS) are saccadic dysmetry (41.7%) and impaired smooth pursuit (42.3%), which relates to prolonged saccadic latency, no matter if they have suffered or not optic neuritis or internuclear ophthalmoplegia (INO). An increase in saccadic latency has been even found in children with MS. Saccadic initiation time (SI time) and average inter‐saccadic intervals (ISI) are also higher in patients with MS. Furthermore, the first cause of acquired pendular nystagmus is MS.Finally, macular sensitivity measured by microperimetry has been found to be altered in MS patients, especially in eyes with previous optic neuritis. Likewise, a fixational instability characterized also my microperimetry is present in MS patients with optic neuritis, with more increase of the vertical axis of the fixation area than of the horizontal. The ratio of the disease also affects the patient fixation pattern.

The integrated optokinetic nystagmus inter-saccadic interval scales statistical different in a group of vertigo patients depended on the stimulation velocity, but not for healthy subjects

The integrated optokinetic nystagmus inter-saccadic interval scales statistical different in a group of vertigo patients depended on the stimulation velocity, but not for healthy subjects

The integrated optokinetic nystagmus inter-saccadic interval scales statistical different in a group of vertigo patients depended on the stimulation velocity, but not for healthy subjects

Optokinetic nystagmus is rhythmic eye movements, back and forth, with a slow and fast phase, when the eyes are presented for full-field visual stimulus. OKN was recorded in 10 healthy subjects and 10 patients suffering from vertigo, for four conditions: stripes moving 30 o/s left and right and 60 o/s left and right. The aim of the present study was to analyze if the optokinetic stimulation intensity, stripes moving with angular velocity of 30 and 60 o/s, below and above the normal threshold for smooth pursuit function, influences the scaling properties of the integrated optokinetic nystagmus inter-saccadic intervals in a group of patients suffering from vertigo and a group of healthy subjects. Calculating the scaling, the spread over time, for the integrated optokinetic nystagmus inter-saccadic intervals, the time intervals between the onsets of consecutive fast components, shows lower Hurst exponent for velocity stimulation of 30o/s compared to 60o/s for both patients and health subjects, but only reach statistical significance for the group of patients. This result is a novel finding.

Visual and motor signatures of locomotion dynamically shape a population code for feature detection in Drosophila.

Natural vision is dynamic: as an animal moves, its visual input changes dramatically. How can the visual system reliably extract local features from an input dominated by self-generated signals? In Drosophila, diverse local visual features are represented by a group of projection neurons with distinct tuning properties. Here, we describe a connectome-based volumetric imaging strategy to measure visually evoked neural activity across this population. We show that local visual features are jointly represented across the population, and a shared gain factor improves trial-to-trial coding fidelity. A subset of these neurons, tuned to small objects, is modulated by two independent signals associated with self-movement, a motor-related signal, and a visual motion signal associated with rotation of the animal. These two inputs adjust the sensitivity of these feature detectors across the locomotor cycle, selectively reducing their gain during saccades and restoring it during intersaccadic intervals. This work reveals a strategy for reliable feature detection during locomotion.

Rapid Automatized Picture Naming in an Outpatient Concussion Center: Quantitative Eye Movements during the Mobile Universal Lexicon Evaluation System (MULES) Test

Number and picture rapid automatized naming (RAN) tests are useful sideline diagnostic tools. The main outcome measure of these RAN tests is the completion time, which is prolonged with a concussion, yet yields no information about eye movement behavior. We investigated eye movements during a digitized Mobile Universal Lexicon Evaluation System (MULES) test of rapid picture naming. A total of 23 participants with a history of concussion and 50 control participants performed MULES testing with simultaneous eye tracking. The test times were longer in participants with a concussion (32.4 s [95% CI 30.4, 35.8] vs. 26.9 s [95% CI 25.9, 28.0], t=6.1). The participants with a concussion made more saccades per picture than the controls (3.6 [95% CI 3.3, 4.1] vs. 2.7 [95% CI 2.5, 3.0]), and this increase was correlated with longer MULES times (r = 0.46, p = 0.026). The inter-saccadic intervals (ISI) did not differ between the groups, nor did they correlate with the test times. Following a concussion, eye movement behavior differs during number versus picture RAN performance. Prior studies have shown that ISI prolongation is the key finding for a number-based RAN test, whereas this study shows a primary finding of an increased saccade number per picture with a picture-based RAN test. Number-based and picture-based RAN tests may be complimentary in concussion detection, as they may detect different injury effects or compensatory strategies.

An investigation into the measurement properties of the King-Devick Eye Tracking system

Objectives Eye tracking has been gaining increasing attention as a possible assessment and monitoring tool for concussion. The King-Devick test (K-DT) was expanded to include an infrared video-oculography-based eye tracker (K-D ET). Therefore, the aim was to provide evidence on the reliability of the K-D ET system under an exercise condition. Methods Participants (N = 61; 26 male, 35 female; age range 19-25) were allocated to an exercise or sedentary group. Both groups completed a baseline K-D ET measurement and then either two 10-min exercise or sedentary interventions with repeated K-D ET measurements between interventions. Results The test-retest reliability of the K-D ET ranged from good to excellent for the different variables measured. The mean ± SD of the differences for the total number of saccades was 1.04 ± 4.01 and there was an observable difference (p = 0.005) in the trial number. There were no observable differences for the intervention (p = 0.768), gender (p = 0.121) and trial (p = 0.777) for average saccade’s velocity. The mean ± SD of the difference of the total fixations before and after intervention across both trials was 1.04 ± 3.63 and there was an observable difference in the trial number (p = 0.025). The mean ± SD of the differences for the Inter-Saccadic Interval and the fixation polyarea before and after intervention across both trials were 1.86 ± 22.99 msec and 0.51 ± 59.11 mm2 and no observable differences for the intervention, gender and trial. Conclusion The results provide evidence on the reliability of the K-D ET, and the eye-tracking components and demonstrate the relationship between completion time and other variables of the K-D ET system. This is vital as the use of the K-DT may be increasing and the combination of the K-DT and eye tracking as one single package highlights the need to specifically measure the reliability of this combined unit.

King-Devick Test Performance and Cognitive Dysfunction after Concussion: A Pilot Eye Movement Study.

(1) Background: The King-Devick (KD) rapid number naming test is sensitive for concussion diagnosis, with increased test time from baseline as the outcome measure. Eye tracking during KD performance in concussed individuals shows an association between inter-saccadic interval (ISI) (the time between saccades) prolongation and prolonged testing time. This pilot study retrospectively assesses the relation between ISI prolongation during KD testing and cognitive performance in persistently-symptomatic individuals post-concussion. (2) Results: Fourteen participants (median age 34 years; 6 women) with prior neuropsychological assessment and KD testing with eye tracking were included. KD test times (72.6 ± 20.7 s) and median ISI (379.1 ± 199.1 msec) were prolonged compared to published normative values. Greater ISI prolongation was associated with lower scores for processing speed (WAIS-IV Coding, r = 0.72, p = 0.0017), attention/working memory (Trails Making A, r = −0.65, p = 0.006) (Digit Span Forward, r = 0.57, p = −0.017) (Digit Span Backward, r= −0.55, p = 0.021) (Digit Span Total, r = −0.74, p = 0.001), and executive function (Stroop Color Word Interference, r = −0.8, p = 0.0003). (3) Conclusions: This pilot study provides preliminary evidence suggesting that cognitive dysfunction may be associated with prolonged ISI and KD test times in concussion.

Temporal Patterns of Spontaneous Fixational Eye Movements: The Influence of Basal Ganglia.

Spontaneity is a unique feature of the nervous system. One of the fundamentally critical and recognized forms of spontaneous motor activity is witnessed in the visuomotor system. Microsaccades, the miniature spontaneous eye movements, are critical for the visual perception. We hypothesized that microsaccades follow specific temporal patterns that are modulated by the basal ganglia output. We used high-resolution video-oculography to capture microsaccades in 48 subjects (31 healthy and 17 with Parkinson's disease) when subjects were asked to hold their gaze on a straight-ahead target projected on white background. We analyzed spontaneous discharge patterns of microsaccades. The first analysis considering coefficient of variation in intersaccadic interval distribution demonstrated that microsaccades in Parkinson's disease are more dispersed than the control group. The second analysis scrutinized microsaccades' temporal variability and revealed 3 distinct occurrence patterns: regular rhythmic, clustered, and randomly occurring following a Poisson-like process. The regular pattern was relatively more common in Parkinson's disease. Subthalamic DBS modulated this temporal pattern. The amount of change in the temporal variability depended on the DBS-induced volume of tissue activation and its overlap with the subthalamic nucleus. The third analysis determined the autocorrelations of microsaccades within 2-second time windows. We found that Parkinson's disease altered local temporal organization in microsaccade generation, and DBS had a modulatory effect. The microsaccades occur in 3 temporal patterns. The basal ganglia are one of the modulators of the microsaccade spontaneity.

Ocular Flutter in Parainfectious Meningoencephalitis: A Case Report

Ocular flutter is a rare, horizontal eye movement disorder characterized by intermittent bursts of conjugate horizontal saccades without intersaccadic intervals. It can occur in various clinical conditions such as metabolic dysfunction, infection and paraneoplastic syndrome. Herein, a 50-year-old male showed ocular flutter in parainfectious meningoencephalitis and immunoglobulin therapy led to an improvement of symptoms. This case can improve the understanding of the pathological mechanisms of ocular flutter.

Involuntary "Voluntary" Nystagmus.

Voluntary nystagmus is a common phenomenon in the general population and is believed to be under voluntary control. Some patients have an eye movement disorder indistinguishable from voluntary nystagmus and yet have no control over these movements. Four patients with involuntary eye movements consisting of spontaneous or induced bursts of saccadic eye movements with no intersaccadic interval are described. All eye movements were typical of "voluntary nystagmus," yet they denied any control over the movements. In none of the patients was there any evidence of psychopathology or secondary gain. Two types of patients with involuntary eye movements that were indistinguishable from voluntary nystagmus are presented. One group of 2 patients had clear neurological disease, whereas another 2 had no evidence of any neurological pathology. The patterns seen in these patients suggest that there is a spectrum of oculomotor saccadic instabilities that includes voluntary nystagmus on one extreme and ocular flutter on the other. In between these 2 are both normal and abnormal patients with eye movements indistinguishable from ocular flutter/voluntary nystagmus that may or may not be induced by convergence. It is suggested that involuntary "voluntary nystagmus" is a real condition and that psychopathology should be ruled in rather than simply assumed.

Spontaneous grouping of saccade timing in the presence of task-irrelevant objects.

Sequential movements are often grouped into several chunks, as evidenced by the modulation of the timing of each elemental movement. Even during synchronized tapping with a metronome, we sometimes feel subjective accent for every few taps. To examine whether motor segmentation emerges during synchronized movements, we trained monkeys to generate a series of predictive saccades synchronized with visual stimuli which sequentially appeared for a fixed interval (400 or 600 ms) at six circularly arranged landmark locations. We found two types of motor segmentations that featured periodic modulation of saccade timing. First, the intersaccadic interval (ISI) depended on the target location and saccade direction, indicating that particular combinations of saccades were integrated into motor chunks. Second, when a task-irrelevant rectangular contour surrounding three landmarks ("inducer") was presented, the ISI significantly modulated depending on the relative target location to the inducer. All patterns of individual differences seen in monkeys were also observed in humans. Importantly, the effects of the inducer greatly decreased or disappeared when the animals were trained to generate only reactive saccades (latency >100 ms), indicating that the motor segmentation may depend on the internal rhythms. Thus, our results demonstrate two types of motor segmentation during synchronized movements: one is related to the hierarchical organization of sequential movements and the other is related to the spontaneous grouping of rhythmic events. This experimental paradigm can be used to investigate the underlying neural mechanism of temporal grouping during rhythm production.

How sandbag-able are concussion sideline assessments? A close look at eye movements to uncover strategies

ABSTRACT Background: Sideline diagnostic tests for concussion are vulnerable to volitional poor performance (“sandbagging”) on baseline assessments, motivated by desire to subvert concussion detection and potential removal from play. We investigated eye movements during sandbagging versus best effort on the King-Devick (KD) test, a rapid automatized naming (RAN) task. Methods: Participants performed KD testing during oculography following instructions to sandbag or give best effort. Results: Twenty healthy participants without concussion history were included (mean age 27 ± 8 years). Sandbagging resulted in longer test times (89.6 ± 39.2 s vs 48.2 ± 8.5 s, p < .001), longer inter-saccadic intervals (459.5 ± 125.4 ms vs 311.2 ± 79.1 ms, p < .001) and greater numbers of saccades (171.4 ± 47 vs 138 ± 24.2, p < .001) and reverse saccades (wrong direction for reading) (21.2% vs 11.3%, p < .001). Sandbagging was detectable using a logistic model with KD times as the only predictor, though more robustly detectable using eye movement metrics. Conclusions: KD sandbagging results in eye movement differences that are detectable by eye movement recordings and suggest an invalid test score. Objective eye movement recording during the KD test shows promise for distinguishing between best effort and post-injury performance, as well as for identifying sandbagging red flags.

Ocular Flutter in Hyperosmolar Hyperglycemic State during Treatment of Malignant Cerebral Edema

Ocular flutter (OF) is a rare eye movement disorder with horizontal saccadic oscillations without inter-saccadic intervals. The OF can occur in various clinical settings. A 83-year-old female showed the OF in hyperosmolar hyperglycemic state (HHS) following malignant cerebral infarction. The pathophysiology of the OF is still unclear, but this case provides a new information that the OF can occur in the context of toxic-metabolic state such as HHS.

Isolated opsoclonus heralding neuromyelitis optica spectrum disorder

Opsoclonus is an ocular motility disorder characterized by spontaneous, arrhythmic conjugate saccades of varying amplitude occurring in all directions of gaze without normal intersaccadic interval. Etiological spectrum of opsoclonus encompasses paraneoplastic and neoplastic conditions, infectious and para-infectious encephalitis, autoimmune, metabolic and toxic encephalopathies, drugs, motor neuron diseases, multiple sclerosis and rarely neuromyelitis optica spectrum disorder (NMOSD). Opsoclonus has never been reported as a presenting manifestation heralding NMOSD. We herein report a previously healthy 37-year-old Asian Indian woman who presented with oscillopsia and opsoclonus, followed, 12 h later, by right-sided hemiparesis, right-sided appendicular ataxia, and left-sided lower motor neuron type facial palsy and dysarthria. Brain magnetic resonance imaging revealed hyperintense lesions in brainstem and thalamus in T2-weighted and fluid attenuated inversion recovery-weighted images, quite suggestive of NMOSD. Serum and cerebrospinal fluid samples were positive for anti-aquaporin-4 antibodies, which clinched the diagnosis of seropositive NMOSD. After completion of a course of intravenous methylprednisolone 1 g/day for 5 days, her opsoclonus disappeared completely. There was significant improvement in her speech and weakness within the first week of therapy and no objective deficit after day 20 of admission. After one-and-a-half-year follow-up, the patient was maintaining well on rituximab as secondary prophylaxis without any further attack. Our case highlights that isolated opsoclonus can be the presenting feature of NMOSD.