Sven Ohl

Compensatory eye and head movements of patients with homonymous hemianopia in the naturalistic setting of a driving simulation

Homonymous hemianopia (HH) is a frequent deficit resulting from lesions to post-chiasmal brain structures with a significant negative impact on activities of daily living. To address the question how patients with HH may compensate their visual field defect in a naturalistic environment, we performed a driving simulation experiment and quantitatively analyzed both eye and head movements using a head-mounted pupil camera. 14 patients with HH and 14 matched healthy control subjects participated in the study. Based on the detection performance of dynamically moving obstacles, which appeared unexpectedly along the sides of the road track, we divided the patient group into a high- and a low-performance group. Then, we compared parameters of eye and head movements between the two patient groups and the matched healthy control group to identify those which mediate successful detection of potentially hazardous objects. Differences in detection rates could not be explained by demographic variables or the extent of the visual field defect. Instead, high performance of patients with HH in the naturalistic setting of our driving simulation depended on an adapted visual exploratory behavior characterized by a relative increase in the amplitude and a corresponding increase in the peak velocity of saccades, widening horizontally the distribution of eye movements, and by a shift of the overall distribution of saccades into the blind hemifield. The result of the group comparison analyses was confirmed by a subsequent stepwise regression analysis which identified the horizontal spread of eye movements as single factor predicting the detection of hazardous objects.

Driving Simulation in the Clinic: Testing Visual Exploratory Behavior in Daily Life Activities in Patients with Visual Field Defects

Patients suffering from homonymous hemianopia after infarction of the posterior cerebral artery (PCA) report different degrees of constraint in daily life, despite similar visual deficits. We assume this could be due to variable development of compensatory strategies such as altered visual scanning behavior. Scanning compensatory therapy (SCT) is studied as part of the visual training after infarction next to vision restoration therapy. SCT consists of learning to make larger eye movements into the blind field enlarging the visual field of search, which has been proven to be the most useful strategy1, not only in natural search tasks but also in mastering daily life activities2. Nevertheless, in clinical routine it is difficult to identify individual levels and training effects of compensatory behavior, since it requires measurement of eye movements in a head unrestrained condition. Studies demonstrated that unrestrained head movements alter the visual exploratory behavior compared to a head-restrained laboratory condition3. Martin et al.4 and Hayhoe et al.5 showed that behavior demonstrated in a laboratory setting cannot be assigned easily to a natural condition. Hence, our goal was to develop a study set-up which uncovers different compensatory oculomotor strategies quickly in a realistic testing situation: Patients are tested in the clinical environment in a driving simulator. SILAB software (Wuerzburg Institute for Traffic Sciences GmbH (WIVW)) was used to program driving scenarios of varying complexity and recording the drivers performance. The software was combined with a head mounted infrared video pupil tracker, recording head- and eye-movements (EyeSeeCam, University of Munich Hospital, Clinical Neurosciences). The positioning of the patient in the driving simulator and the positioning, adjustment and calibration of the camera is demonstrated. Typical performances of a patient with and without compensatory strategy and a healthy control are illustrated in this pilot study. Different oculomotor behaviors (frequency and amplitude of eye- and head-movements) are evaluated very quickly during the drive itself by dynamic overlay pictures indicating where the subjects gaze is located on the screen, and by analyzing the data. Compensatory gaze behavior in a patient leads to a driving performance comparable to a healthy control, while the performance of a patient without compensatory behavior is significantly worse. The data of eye- and head-movement-behavior as well as driving performance are discussed with respect to different oculomotor strategies and in a broader context with respect to possible training effects throughout the testing session and implications on rehabilitation potential.

Saccadic Eye Movements Impose a Natural Bottleneck on Visual Short-Term Memory.

Visual short-term memory (VSTM) is a crucial repository of information when events unfold rapidly before our eyes, yet it maintains only a fraction of the sensory information encoded by the visual system. Here, we tested the hypothesis that saccadic eye movements provide a natural bottleneck for the transition of fragile content in sensory memory to VSTM. In 4 experiments, we show that saccades, planned and executed after the disappearance of a memory array, markedly bias visual memory performance. First, items that had appeared at the saccade target were more readily remembered than items that had appeared elsewhere, even though the saccade was irrelevant to the memory task (Experiment 1). Second, this influence was strongest for saccades elicited right after the disappearance of the memory array and gradually declined over the course of a second (Experiment 2). Third, the saccade stabilized memory representations: The imposed bias persisted even several seconds after saccade execution (Experiment 3). Finally, the advantage for stimuli congruent with the saccade target occurred even when that stimulus was far less likely to be probed in the memory test than any other stimulus in the array, ruling out a strategic effort of observers to memorize information presented at the saccade target (Experiment 4). Together, these results make a strong case that saccades inadvertently determine the content of VSTM, and highlight the key role of actions for the fundamental building blocks of cognition.

Microsaccades Are Coupled to Heartbeat

During visual fixation, the eye generates microsaccades and slower components of fixational eye movements that are part of the visual processing strategy in humans. Here, we show that ongoing heartbeat is coupled to temporal rate variations in the generation of microsaccades. Using coregistration of eye recording and ECG in humans, we tested the hypothesis that microsaccade onsets are coupled to the relative phase of the R-R intervals in heartbeats. We observed significantly more microsaccades during the early phase after the R peak in the ECG. This form of coupling between heartbeat and eye movements was substantiated by the additional finding of a coupling between heart phase and motion activity in slow fixational eye movements; i.e., retinal image slip caused by physiological drift. Our findings therefore demonstrate a coupling of the oculomotor system and ongoing heartbeat, which provides further evidence for bodily influences on visuomotor functioning. SIGNIFICANCE STATEMENT In the present study, we show that microsaccades are coupled to heartbeat. Moreover, we revealed a strong modulation of slow eye movements around the R peak in the ECG. These results suggest that heartbeat as a basic physiological signal is related to statistical modulations of fixational eye movements, in particular, the generation of microsaccades. Therefore, our findings add a new perspective on the principles underlying the generation of fixational eye movements. Importantly, our study highlights the need to record eye movements when studying the influence of heartbeat in neuroscience to avoid misinterpretation of eye-movement-related artifacts as heart-evoked modulations of neural processing.

Visual Suppression in the Superior Colliculus Around the Time of Microsaccades

Miniature eye movements jitter the retinal image unceasingly, raising the question of how perceptual continuity is achieved during visual fixation. Recent work discovered suppression of visual bursts in the superior colliculus around the time of microsaccades, tiny jerks of the eyes that support visual perception while gaze is fixed. This finding suggests that corollary discharge, supporting visual stability when rapid eye movements drastically shift the retinal image, may also exist for the smallest saccades.

Age-related changes in visual exploratory behavior in a natural scene setting

Diverse cognitive functions decline with increasing age, including the ability to process central and peripheral visual information in a laboratory testing situation (useful visual field of view). To investigate whether and how this influences activities of daily life, we studied age-related changes in visual exploratory behavior in a natural scene setting: a driving simulator paradigm of variable complexity was tested in subjects of varying ages with simultaneous eye- and head-movement recordings via a head-mounted camera. Detection and reaction times were also measured by visual fixation and manual reaction. We considered video computer game experience as a possible influence on performance. Data of 73 participants of varying ages were analyzed, driving two different courses. We analyzed the influence of route difficulty level, age, and eccentricity of test stimuli on oculomotor and driving behavior parameters. No significant age effects were found regarding saccadic parameters. In the older subjects head-movements increasingly contributed to gaze amplitude. More demanding courses and more peripheral stimuli locations induced longer reaction times in all age groups. Deterioration of the functionally useful visual field of view with increasing age was not suggested in our study group. However, video game-experienced subjects revealed larger saccade amplitudes and a broader distribution of fixations on the screen. They reacted faster to peripheral objects suggesting the notion of a general detection task rather than perceiving driving as a central task. As the video game-experienced population consisted of younger subjects, our study indicates that effects due to video game experience can easily be misinterpreted as age effects if not accounted for. We therefore view it as essential to consider video game experience in all testing methods using virtual media.

Setting and changing feature priorities in visual short-term memory.

Many everyday tasks require prioritizing some visual features over competing ones, both during the selection from the rich sensory input and while maintaining information in visual short-term memory (VSTM). Here, we show that observers can change priorities in VSTM when, initially, they attended to a different feature. Observers reported from memory the orientation of one of two spatially interspersed groups of black and white gratings. Using colored pre-cues (presented before stimulus onset) and retro-cues (presented after stimulus offset) predicting the to-be-reported group, we manipulated observers’ feature priorities independently during stimulus encoding and maintenance, respectively. Valid pre-cues reliably increased observers’ performance (reduced guessing, increased report precision) as compared to neutral ones; invalid pre-cues had the opposite effect. Valid retro-cues also consistently improved performance (by reducing random guesses), even if the unexpected group suddenly became relevant (invalid-valid condition). Thus, feature-based attention can reshape priorities in VSTM protecting information that would otherwise be forgotten.

Selective enhancement of orientation tuning before saccades

Saccadic eye movements cause a rapid sweep of the visual image across the retina and bring the saccades target into high-acuity foveal vision. Even before saccade onset, visual processing is selectively prioritized at the saccade target. To determine how this presaccadic attention shift exerts its influence on visual selection, we compare the dynamics of perceptual tuning curves before movement onset at the saccade target and in the opposite hemifield. Participants monitored a 30-Hz sequence of randomly oriented gratings for a target orientation. Combining a reverse correlation technique previously used to study orientation tuning in neurons and general additive mixed modeling, we found that perceptual reports were tuned to the target orientation. The gain of orientation tuning increased markedly within the last 100 ms before saccade onset. In addition, we observed finer orientation tuning right before saccade onset. This increase in gain and tuning occurred at the saccade target location and was not observed at the incongruent location in the opposite hemifield. The present findings suggest, therefore, that presaccadic attention exerts its influence on vision in a spatially and feature-selective manner, enhancing performance and sharpening feature tuning at the future gaze location before the eyes start moving.

Revealing the time course of signals influencing the generation of secondary saccades using Aalen’s additive hazards model

Saccadic eye movements are frequently followed by smaller secondary saccades which are generally assumed to correct for the error in primary saccade landing position. However, secondary saccades can also occur after accurate primary saccades and they are often as small as microsaccades, therefore raising the need to further scrutinize the processes involved in secondary saccade generation. Following up a previous study, we analyzed secondary saccades using rate analysis which allows us to quantify experimental effects as shifts in distributions, therefore going beyond comparisons of mean differences. We use Aalens additive hazards model to delineate the time course of key influences on the secondary saccade rate. In addition to the established effect of primary saccade error, we observed a time-varying influence of under- vs. overshooting - with a higher risk of generating secondary saccades following undershoots. Moreover, increasing target eccentricity influenced the programming of secondary saccades, therefore demonstrating that error-unrelated variables co-determine secondary saccade programs. Our results provide new insights into the generative mechanisms of small saccades during postsaccadic fixation that need to be accounted for by secondary saccade models.

Saccadic adaptation to a systematically varying disturbance

Saccadic adaptation maintains the correct mapping between eye movements and their targets, yet the dynamics of saccadic gain changes in the presence of systematically varying disturbances has not been extensively studied. Here we assessed changes in the gain of saccade amplitudes induced by continuous and periodic postsaccadic visual feedback. Observers made saccades following a sequence of target steps either along the horizontal meridian (Two-way adaptation) or with unconstrained saccade directions (Global adaptation). An intrasaccadic step-following a sinusoidal variation as a function of the trial number (with 3 different frequencies tested in separate blocks)-consistently displaced the target along its vector. The oculomotor system responded to the resulting feedback error by modifying saccade amplitudes in a periodic fashion with similar frequency of variation but lagging the disturbance by a few tens of trials. This periodic response was superimposed on a drift toward stronger hypometria with similar asymptotes and decay rates across stimulus conditions. The magnitude of the periodic response decreased with increasing frequency and was smaller and more delayed for Global than Two-way adaptation. These results suggest that-in addition to the well-characterized return-to-baseline response observed in protocols using constant visual feedback-the oculomotor system attempts to minimize the feedback error by integrating its variation across trials. This process resembles a convolution with an internal response function, whose structure would be determined by coefficients of the learning model. Our protocol reveals this fast learning process in single short experimental sessions, qualifying it for the study of sensorimotor learning in health and disease.