Spatial localization during open-loop smooth pursuit.

Introduction: Numerous previous studies have shown that eye movements induce errors in the localization of briefly flashed stimuli. Remarkably, the error pattern is indicative of the underlying eye movement and the exact experimental condition. For smooth pursuit eye movements (SPEM) and the slow phase of the optokinetic nystagmus (OKN), perceived stimulus locations are shifted in the direction of the ongoing eye movement, with a hemifield asymmetry observed only during SPEM. During the slow phases of the optokinetic afternystagmus (OKAN), however, the error pattern can be described as a perceptual expansion of space. Different from SPEM and OKN, the OKAN is an open-loop eye movement. Methods: Visually guided smooth pursuit can be transformed into an open-loop eye movement by briefly blanking the pursuit target (gap). Here, we examined flash localization during open-loop pursuit and asked, whether localization is also prone to errors and whether these are similar to those found during SPEM or during OKAN. Human subjects tracked a pursuit target. In half of the trials, the target was extinguished for 300 ms (gap) during the steady-state, inducing open-loop pursuit. Flashes were presented during this gap or during steady-state (closed-loop) pursuit. Results: In both conditions, perceived flash locations were shifted in the direction of the eye movement. The overall error pattern was very similar with error size being slightly smaller in the gap condition. The differences between errors in the open- and closed-loop conditions were largest in the central visual field and smallest in the periphery. Discussion: We discuss the findings in light of the neural substrates driving the different forms of eye movements.

Antisaccades in Parkinson's Disease: A Meta-Analysis.

The usefulness of eye-tracking tasks as potential biomarkers for motor or cognitive disease burden in Parkinson's disease (PD) has been subject of debate for many years. Several studies suggest that the performance in the antisaccade task may be altered in patients with PD and associated with motor disease severity or executive dysfunction. In this meta-analysis, random effects models were used to synthesize the existing evidence on antisaccade error rates and latency in PD. Furthermore, meta-regressions were performed to assess the role of motor and cognitive disease severity, dopaminergic medication and methodological factors. Additionally, the impact of acute levodopa administration and activation of deep brain stimulation was evaluated in two separate sub-analyses.This meta-analysis confirms that antisaccade latency and error rate are significantly increased in PD. Disease duration, Unified Parkinson's disease rating scale score and Hoehn and Yahr stage mediate the effect of PD on antisaccade latency with higher motor burden being associated with increased antisaccade latency.Acute administration of levodopa had no significant effects on antisaccade performance in a small number of eligible studies. Deep brain stimulation in the subthalamic nucleus, on the other hand, may alter the speed accuracy trade-off supporting an increase of impulsivity following deep brain stimulation in PD.According to the results of the meta-analysis, antisaccade latency may provide a potential marker for disease severity and progression in PD which needs further confirmation in longitudinal studies.

Perisaccadic encoding of temporal information in macaque area V4.

The accurate processing of temporal information is of critical importance in everyday life. Yet, psychophysical studies in humans have shown that the perception of time is distorted around saccadic eye movements. The neural correlates of this misperception are still poorly understood. Behavioral and neural evidence suggest that it is tightly linked to other known perisaccadic modulations of visual perception. To further our understanding of how temporal processing is affected by saccades, we studied the representations of brief visual time intervals during fixation and saccades in area V4 of two awake macaques. We presented random sequences of vertical bar stimuli and extracted neural responses to double-pulse stimulation at varying interstimulus intervals. Our results show that temporal information about very brief intervals of as brief as 20 ms is reliably represented in the multiunit activity in area V4. Response latencies were not systematically modulated by the saccade. However, a general increase in perisaccadic activity altered the ratio of response amplitudes within stimulus pairs compared with fixation. In line with previous studies showing that the perception of brief time intervals is partly based on response levels, this may be seen as a possible correlate of the perisaccadic misperception of time.NEW & NOTEWORTHY We investigated for the first time how temporal information on very brief timescales is represented in area V4 around the time of saccadic eye movements. Overall, the responses showed an unexpectedly precise representation of time intervals. Our finding of a perisaccadic modulation of relative response amplitudes introduces a new possible correlate of saccade-related perceptual distortions of time.

Nonretinocentric localization of successively presented flashes during smooth pursuit eye movements.

Keeping track of objects in our environment across body and eye movements is essential for perceptual stability and localization of external objects. As of yet, it is largely unknown how this perceptual stability is achieved. A common behavioral approach to investigate potential neuronal mechanisms underlying spatial vision has been the presentation of one brief visual stimulus across eye movements. Here, we adopted this approach and aimed to determine the reference frame of the perceptual localization of two successively presented flashes during fixation and smooth pursuit eye movements (SPEMs). To this end, eccentric flashes with a stimulus onset asynchrony of zero or ± 200 ms had to be localized with respect to each other during fixation and SPEMs. The results were used to evaluate different models predicting the reference frame in which the spatial information is represented. First, we were able to reproduce the well-known effect of relative mislocalization during fixation. Second, smooth pursuit led to a characteristic relative mislocalization, different from that during fixation. A model assuming that relative localization takes place in a nonretinocentric reference frame described our data best. This suggests that the relative localization judgment is performed at a stage of visual processing in which retinal and nonretinal information is available.

Quantitative comparison of a mobile and a stationary video-based eye-tracker.

Vision represents the most important sense of primates. To understand visual processing, various different methods are employed-for example, electrophysiology, psychophysics, or eye-tracking. For the latter method, researchers have recently begun to step outside the artificial environments of laboratory setups toward the more natural conditions we usually face in the real world. To get a better understanding of the advantages and limitations of modern mobile eye-trackers, we quantitatively compared one of the most advanced mobile eye-trackers available, the EyeSeeCam, with a commonly used laboratory eye-tracker, the EyeLink II, serving as a gold standard. We aimed to investigate whether or not fully mobile eye-trackers are capable of providing data that would be adequate for direct comparisons with data recorded by stationary eye-trackers. Therefore, we recorded three different, commonly used eye movements-fixations, saccades, and smooth-pursuit eye movements-with both eye-trackers, in successive standardized paradigms in a laboratory setting with eight human subjects. Despite major technical differences between the devices, most eye movement parameters were not statistically different between the two systems. Differences could only be found in overall gaze accuracy and for time-critical parameters such as saccade duration, for which a higher sample frequency is especially useful. Although the stationary EyeLink II system proved to be superior, especially on a single-subject or even a single-trial basis, the ESC showed similar performance for the averaged parameters across both trials and subjects. We concluded that modern mobile eye-trackers are well-suited to providing reliable oculomotor data at the required spatial and temporal resolutions.

Neural correlate of spatial (mis-)localization during smooth eye movements.

The dependence of neuronal discharge on the position of the eyes in the orbit is a functional characteristic of many visual cortical areas of the macaque. It has been suggested that these eye-position signals provide relevant information for a coordinate transformation of visual signals into a non-eye-centered frame of reference. This transformation could be an integral part for achieving visual perceptual stability across eye movements. Previous studies demonstrated close to veridical eye-position decoding during stable fixation as well as characteristic erroneous decoding across saccadic eye-movements. Here we aimed to decode eye position during smooth pursuit. We recorded neural activity in macaque area VIP during steady fixation, saccades and smooth-pursuit and investigated the temporal and spatial accuracy of eye position as decoded from the neuronal discharges. Confirming previous results, the activity of the majority of neurons depended linearly on horizontal and vertical eye position. The application of a previously introduced computational approach (isofrequency decoding) allowed eye position decoding with considerable accuracy during steady fixation. We applied the same decoder on the activity of the same neurons during smooth-pursuit. On average, the decoded signal was leading the current eye position. A model combining this constant lead of the decoded eye position with a previously described attentional bias ahead of the pursuit target describes the asymmetric mislocalization pattern for briefly flashed stimuli during smooth pursuit eye movements as found in human behavioral studies.

Eye movements of patients with schizophrenia in a natural environment.

Alterations of eye movements in schizophrenia patients have been widely described for laboratory settings. For example, gain during smooth tracking is reduced, and fixation patterns differ between patients and healthy controls. The question remains, whether such results are related to the specifics of the experimental environment, or whether they transfer to natural settings. Twenty ICD-10 diagnosed schizophrenia patients and 20 healthy age-matched controls participated in the study, each performing four different oculomotor tasks corresponding to natural everyday behavior in an indoor environment: (I) fixating stationary targets, (II) sitting in a hallway with free gaze, (III) walking down the hallway, and (IV) visually tracking a target on the floor while walking straight-ahead. In all conditions, eye movements were continuously recorded binocularly by a mobile lightweight eye tracker (EyeSeeCam). When patients looked at predefined targets, they showed more fixations with reduced durations than controls. The opposite was true when participants were sitting in a hallway with free gaze. During visual tracking, patients showed a significantly greater root-mean-square error (representing the mean deviation from optimal) of retinal target velocity. Different from previous results on smooth-pursuit eye movements obtained in laboratory settings, no such difference was found for velocity gain. Taken together, we have identified significant differences in fundamental oculomotor parameters between schizophrenia patients and healthy controls during natural behavior in a real environment. Moreover, our data provide evidence that in natural settings, patients overcome some impairments, which might be present only in laboratory studies, by as of now unknown compensatory mechanisms or strategies.

Effects of aging on eye movements in the real world.

The effects of aging on eye movements are well studied in the laboratory. Increased saccade latencies or decreased smooth-pursuit gain are well established findings. The question remains whether these findings are influenced by the rather untypical environment of a laboratory; that is, whether or not they transfer to the real world. We measured 34 healthy participants between the age of 25 and 85 during two everyday tasks in the real world: (I) walking down a hallway with free gaze, (II) visual tracking of an earth-fixed object while walking straight-ahead. Eye movements were recorded with a mobile light-weight eye tracker, the EyeSeeCam (ESC). We find that age significantly influences saccade parameters. With increasing age, saccade frequency, amplitude, peak velocity, and mean velocity are reduced and the velocity/amplitude distribution as well as the velocity profile become less skewed. In contrast to laboratory results on smooth pursuit, we did not find a significant effect of age on tracking eye-movements in the real world. Taken together, age-related eye-movement changes as measured in the laboratory only partly resemble those in the real world. It is well-conceivable that in the real world additional sensory cues, such as head-movement or vestibular signals, may partially compensate for age-related effects, which, according to this view, would be specific to early motion processing. In any case, our results highlight the importance of validity for natural situations when studying the impact of aging on real-life performance.

Validation of mobile eye-tracking as novel and efficient means for differentiating progressive supranuclear palsy from Parkinson's disease.

BACKGROUND: The decreased ability to carry out vertical saccades is a key symptom of Progressive Supranuclear Palsy (PSP). Objective measurement devices can help to reliably detect subtle eye movement disturbances to improve sensitivity and specificity of the clinical diagnosis. The present study aims at transferring findings from restricted stationary video-oculography (VOG) to a wearable head-mounted device, which can be readily applied in clinical practice. METHODS: We investigated the eye movements in 10 possible or probable PSP patients, 11 Parkinson's disease (PD) patients, and 10 age-matched healthy controls (HCs) using a mobile, gaze-driven video camera setup (EyeSeeCam). Ocular movements were analyzed during a standardized fixation protocol and in an unrestricted real-life scenario while walking along a corridor. RESULTS: The EyeSeeCam detected prominent impairment of both saccade velocity and amplitude in PSP patients, differentiating them from PD and HCs. Differences were particularly evident for saccades in the vertical plane, and stronger for saccades than for other eye movements. Differences were more pronounced during the standardized protocol than in the real-life scenario. CONCLUSIONS: Combined analysis of saccade velocity and saccade amplitude during the fixation protocol with the EyeSeeCam provides a simple, rapid (<20 s), and reliable tool to differentiate clinically established PSP patients from PD and HCs. As such, our findings prepare the ground for using wearable eye-tracking in patients with uncertain diagnoses.