Microsaccadic Fixational Eye Movements as an Oculomotor Marker for Concussion

ObjectiveTo identify whether concussion causes abnormalities in fixational eye movements, specifically the generation of microsaccades.BackgroundMicrosaccades are microscopic rapid eye movements that occur normally with attempted fixation. However, changes in microsaccade rate, magnitude, etc have been linked with neurologic and ophthalmic pathologies.Design/MethodsWe collected baseline data for college athletes (n = 116) at Sterling College (Sterling, KS) as they reported for the physical examination before the beginning of the athletic season. None of the athletes had a prior history of concussion. Concussion patients (n = 86) were selected from patients who had an initial visit for concussion at a private concussion clinic. Patients were included if they presented within 50 days of injury. All participants were between 18 and 23 years of age. For each participant we measured the number of saccades generated, the size and speed of the micro saccades, the area covered and the ratio of vertical-to-horizontal direction component of the fixational eye movements, using a 250 Hz video-eye tracker mounted inside a HTC Vive VR headset. Participants were instructed to fixate on a central dot for 140 seconds, in 20-second intervals. We performed a logistic regression with the log-transformed oculomotor characteristics as independent variables and concussion yes/no as dependent variables. Errors are presented as standard error from the mean.ResultsThe average microsaccade magnitude was higher in concussed than in non-concussed participants (1.85 ± 0.12° vs 1.32 ± 0.06°, p < 0.001). Similarly, the fixational eye movements (microsaccades + drifts) of concussed patients tended to cover a more vertical area during fixation periods (vertical-to-horizontal ratio of 3.49 ± 0.94 vs 1.12 ± 0.04, p < 0.005).ConclusionsOculomotor testing, specifically microsaccades is a potential marker for concussion. Concussion patients present larger and more vertical eye movements during fixation.

Reading Specific Small Saccades Predict Individual Phonemic Awareness and Reading Speed

Small fixational eye-movements are a fundamental aspect of vision and thought to reflect fine shifts in covert attention during active viewing. While the perceptual benefits of these small eye movements have been demonstrated during a wide range of experimental tasks including during free viewing, their function during reading remains surprisingly unclear. Previous research demonstrated that readers with increased microsaccade rates displayed longer reading speeds. To what extent increased fixational eye movements are, however, specific to reading and might be indicative of reading skill deficits remains, however, unknown. To address this topic, we compared the eye movement scan paths of 13 neurotypical individuals and 13 subjects diagnosed with developmental dyslexia during short story reading and free viewing of natural scenes. We found that during reading only, dyslexics tended to display small eye movements more frequently compared to neurotypicals, though this effect was not significant at the population level, as it could also occur in slow readers not diagnosed as dyslexics. In line with previous research, neurotypical readers had twice as many regressive compared to progressive microsaccades, which did not occur during free viewing. In contrast, dyslexics showed similar amounts of regressive and progressive small fixational eye movements during both reading and free viewing. We also found that participants with smaller fixational saccades from both neurotypical and dyslexic samples displayed reduced reading speeds and lower scores during independent tests of reading skill. Slower readers also displayed greater variability in the landing points and temporal occurrence of their fixational saccades. Both the rate and spatio-temporal variability of fixational saccades were associated with lower phonemic awareness scores. As none of the observed differences between dyslexics and neurotypical readers occurred during control experiments with free viewing, the reported effects appear to be directly related to reading. In summary, our results highlight the predictive value of small saccades for reading skill, but not necessarily for developmental dyslexia.

Stimulus dependence of theta rhythmic activity in primate V1 and its potential relevance for visual perception

A growing body of psychophysical research reports theta (3-8 Hz) rhythmic fluctuations in visual perception that are often attributed to an attentional sampling mechanism arising from theta rhythmic neural activity in mid- to high-level cortical association areas. However, it remains unclear to what extent such neuronal theta oscillations might already emerge at early sensory cortex like the primary visual cortex (V1), e.g. from the stimulus filter properties of neurons. To address this question, we recorded multi-unit neural activity from V1 of two macaque monkeys viewing a static visual stimulus with variable sizes, orientations and contrasts. We found that among the visually responsive electrode sites, more than 50 % showed a spectral peak at theta frequencies. Theta power varied with varying basic stimulus properties. Within each of these stimulus property domains (e.g. size), there was usually a single stimulus value that induced the strongest theta activity. In addition to these variations in theta power, the peak frequency of theta oscillations increased with increasing stimulus size and also changed depending on the stimulus position in the visual field. Further analysis confirmed that this neural theta rhythm was indeed stimulus-induced and did not arise from small fixational eye movements (microsaccades). When the monkeys performed a detection task of a target embedded in a theta-generating visual stimulus, reaction times also tended to fluctuate at the same theta frequency as the one observed in the neural activity. The present study shows that a highly stimulus-dependent neuronal theta oscillation can be elicited in V1 that appears to influence the temporal dynamics of visual perception.

Functional but not obligatory link between microsaccades and neural modulation by covert spatial attention

Covert spatial attention is associated with spatially specific modulation of neural activity as well as with directional biases in fixational eye-movements known as microsaccades. Recently, this link has been suggested to be obligatory, such that modulation of neural activity by covert spatial attention occurs only when paired with microsaccades toward the attended location. Here we revisited this link between microsaccades and neural modulation by covert spatial attention in humans. We investigated spatial modulation of 8-12 Hz EEG alpha activity and microsaccades in a context with no incentive for overt gaze behaviour: when attention is directed internally within the spatial layout of visual working memory. In line with a common attentional origin, we show that spatial modulations of alpha activity and microsaccades co-vary: alpha lateralisation is stronger in trials with microsaccades toward compared to away from the memorised location of the to-be-attended item and occurs earlier in trials with earlier microsaccades toward this item. Critically, however, trials without attention-driven microsaccades nevertheless showed clear spatial modulation of alpha activity - comparable to the neural modulation observed in trials with attention-driven microsaccades. Thus, directional biases in microsaccades are correlated with neural signatures of covert spatial attention, but they are not a prerequisite for neural modulation by covert spatial attention to be manifest.

Beyond Fixation: detailed characterization of neural selectivity in free-viewing primates

Virtually all vision studies use a fixation point to stabilize gaze, rendering stimuli on video screens fixed to retinal coordinates. This approach requires trained subjects, is limited by the accuracy of fixational eye movements, and ignores the role of eye movements in shaping visual input. To overcome these limitations, we developed a suite of hardware and software tools to study vision during natural behavior in untrained subjects. We show this approach recovers receptive fields and tuning properties of visual neurons from multiple cortical areas of marmoset monkeys. Combined with high-precision eye-tracking, it achieves sufficient resolution to recover the receptive fields of foveal V1 neurons. These findings demonstrate the power of this approach for characterizing neural response while simultaneously studying the dynamics of natural behavior.

The Study of Security Priming on Avoidant Attentional Biases: Combining Microsaccadic Eye-Movement Measurement With a Dot-Probe Task

Microsaccades are small fixational eye movements that have shown to index covert attentional shifts. The present experiment combined microsaccades with performance measures from a dot-probe task to study influences of attachment security priming on the attentional biases of individuals high in attachment avoidance. Security priming is an experimental manipulation aimed at boosting felt security. Using a randomized, mixed design, we measured differences in attentional vigilance toward angry and neutral faces as a function of priming (neutral vs. secure) and attachment avoidance. Individuals high in avoidance habitually tend to withdraw from, or otherwise dismiss, emotionally salient stimuli. Here, we operationalized attentional withdrawal based on both task performance in the dot-probe task and microsaccadic movements. In addition, unlike previous studies where priming salience for the individual participant has been unclear, we used a standardized narrative method for attachment script assessment, securing an indication of how strongly each participant was primed. Dot-probe data significantly captured the link between avoidance and attentional disengagement, though from all facial stimuli (angry and neutral). Although microsaccadic movements did not capture avoidant attentional disengagement, they positively correlated to dot-probe data suggesting measurement convergence. Avoidance was associated with weaker security priming and no overall effect of priming on attention was found, indicating a need for further exploration of suitable priming methods to bypass avoidant deactivation. Our results provide a first indication that, as an implicit looking measure, microsaccadic movements can potentially reveal where early attention is directed at the exact moment of stimulus presentation.