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Distortion of Perceived Visual Space after Eccentric Gaze Holding

Previous studies have shown that rebound nystagmus can be a behavioral probe into the adaptive properties of the gaze-holding mechanism, showing that after prolonged eccentric gaze holding and upon return to central gaze the eye tends to drift towards the previously held position. It is not known whether perception of visual space is also affected by similar adaptation mechanisms. The current study seeks to elucidate if eccentric gaze holding changes the perception of space in a relative spatial judgment task. To measure their spatial bias, twelve subjects were asked to report which among two short vertical lines flashed to the left or to the right of the display was closer to a third central line. Perception was assessed after holding eccentric gaze at 40 degrees towards the left or right and compared with control trials without eccentric gaze holding. Subjects showed a significant difference in spatial bias between the leftward and rightward gaze holding conditions (p = 0.04), suggesting that the visual space changes differently with respect to the side where gaze was held. While we did not observe an overall bias (p = 0.327) under no gaze holding we did observe a significant correlation between handedness and spatial bias (r2 = 0.4, p = 0.04). We conclude that gaze holding temporarily distorts the perception of space in a mechanism that may be related to the adaptation of the gaze holding mechanism.

perception↗

Oblique Eccentric Gaze Holding Evokes Larger Horizontal than Vertical Rebound Nystagmus

Rebound nystagmus (RN) has been used to probe the adaptation mechanisms of the gaze holding system. This type of nystagmus is invoked upon returning to central gaze after prolonged fixation at an eccentric point and it is thought to reflect a set-point adaptation of the neural integrator circuit. Previous studies have only observed horizontal RN after horizontal eccentric gaze holding, reflecting adaptation of the horizontal neural integrator. The current study seeks to elucidate how eccentric gaze at oblique target locations, where there are equal horizontal and vertical components, affects the characteristics of the resulting RN. For a given trial, subjects were instructed to fixate a central flashing target for 5 seconds, then fixate an eccentric continuous target for 30 seconds at one of six possible locations (4 oblique and 2 horizontal targets), and finally fixate centrally at a flashing target for 15 seconds where RN is assessed. Binocular eye-tracking data were collected at 250 Hz. Slow-phase velocity (SPV) or the slow drift part of the nystagmus was used to quantify the magnitude of RN. Subjects showed elevated SPV in the horizontal component (2.3 deg/s), but less in the vertical component (1.4 deg/s) after oblique eccentric gaze holding, reflecting an oblique RN. The smaller vertical RN may reflect a different behavior of the horizontal and vertical neural integrators which are anatomically separated. Under the current paradigm, oblique gaze holding would appear to have a smaller effect on adaptation of the vertical integrator than in the horizontal integrator. Further investigation is needed to establish the reference frame of this distinction between the horizontal and vertical integrator circuits.

gaze holding↗

Modification of Eccentric Gaze-Holding

Clear vision and accurate localization of objects in the environment are prerequisites for reliable performance of motor tasks. Space flight confronts the crewmember with a stimulus rearrangement that requires adaptation to function effectively with the new requirements of altered spatial orientation and motor coordination. Adaptation and motor learning driven by the effects of cerebellar disorders may share some of the same demands that face our astronauts. One measure of spatial localization shared by the astronauts and those suffering from cerebellar disorders that is easily quantified, and for which a neurobiological substrate has been identified, is the control of the angle of gaze (the "line of sight"). The disturbances of gaze control that have been documented to occur in astronauts and cosmonauts, both in-flight and postflight, can be directly related to changes in the extrinsic gravitational environment and intrinsic proprioceptive mechanisms thus, lending themselves to description by simple non-linear statistical models. Because of the necessity of developing robust normal response populations and normative populations against which abnormal responses can be evaluated, the basic models can be formulated using normal, non-astronaut test subjects and subsequently extended using centrifugation techniques to alter the gravitational and proprioceptive environment of these subjects. Further tests and extensions of the models can be made by studying abnormalities of gaze control in patients with cerebellar disease. A series of investigations were conducted in which a total of 62 subjects were tested to: (1) Define eccentric gaze-holding parameters in a normative population, and (2) explore the effects of linear acceleration on gaze-holding parameters. For these studies gaze-holding was evaluated with the subjects seated upright (the normative values), rolled 45 degrees to both the left and right, or pitched back 30 and 90 degrees. In a separate study the further effects of acceleration on gaze stability was examined during centrifugation (+2 G (sub x) and +2 G (sub z) using a total of 23 subjects. In all of our investigations eccentric gaze-holding was established by having the subjects acquire an eccentric target (+/-30 degrees horizontal, +/- 15 degrees vertical) that was flashed for 750 msec in an otherwise dark room. Subjects were instructed to hold gaze on the remembered position of the flashed target for 20 sec. Immediately following the 20 sec period, subjects were cued to return to the remembered center position and to hold gaze there for an additional 20 sec. Following this 20 sec period the center target was briefly flashed and the subject made any corrective eye movement back to the true center position. Conventionally, the ability to hold eccentric gaze is estimated by fitting the natural log of centripetal eye drifts by linear regression and calculating the time constant (G) of these slow phases of "gaze-evoked nystagmus". However, because our normative subjects sometimes showed essentially no drift (tau (sub c) = m), statistical estimation and inference on the effect of target direction was performed on values of the decay constant theta = 1/(tau (sub c)) which we found was well modeled by a gamma distribution. Subjects showed substantial variance of their eye drifts, which were centrifugal in approximately 20 % of cases, and > 40% for down gaze. Using the ensuing estimated gamma distributions, we were able to conclude that rightward and leftward gaze holding were not significantly different, but that upward gaze holding was significantly worse than downward (p<0.05). We also concluded that vertical gaze holding was significantly worse than horizontal (p<0.05). In the case of left and right roll, we found that both had a similar improvement to horizontal gaze holding (p<0.05), but didn't have a significant effect on vertical gaze holding. For pitch tilts, both tilt angles significantly decreased gaze-holding ility in all directions (p<0.05). Finally, we found that hyper-g centrifugation significantly decreased gaze holding ability in the vertical plane. The main findings of this study are as follows: (1) vertical gaze-holding is less stable than horizontal, (2) gaze-holding to upward targets is less stable than to downward targets, (3) tilt affects gaze holding, and (4) hyper-g affects gaze holding. This difference between horizontal and vertical gaze-holding may be ascribed to separate components of the velocity-to-position neural integrator for eye movements, and to differences in orbital mechanics. The differences between upward and downward gaze-holding may be ascribed to an inherent vertical imbalance in the vestibular system. Because whole body tilt and hyper-g affects gaze-holding, it is implied that the otolith organs have direct connections to the neural integrator and further studies of astronaut gaze-holding are warranted. Our statistical method for representing the range of normal eccentric gaze stability can be readily applied to normals who maybe exposed to environments which may modify the central integrator and require monitoring, and to evaluate patients with gaze-evoked nystagmus by comparing to the above established normative criteria.

Reschke, M. F.↗

Dose-Dependent Sensorimotor Impairment in Human Ocular Tracking After Acute Low-Dose Alcohol Administration

Changes in oculomotor behaviours are often used as metrics of sensorimotor disruption due to ethanol (EtOH); however, previous studies have focused on deficits at blood-alcohol concentrations (BACs) above about 0.04%.We investigated the dose dependence of the impairment in oculomotor and ocular behaviours caused by EtOH administration across a range of ultra-low BACs (≤0.035%).We took repeated measures of oculomotor and ocular performance from sixteen participants, both pre- and post-EtOH administration. To assess the neurological impacts across a wide range of brain areas and pathways, our protocol measured 21 largely independent performance metrics extracted from a range of behavioural responses ranging from ocular tracking of radial step-ramp stimuli, to eccentric gaze holding, to pupillary responses evoked by light flashes. Our results show significant impairment of pursuit and visual motion processing at 0.015% BAC, reflecting degraded neural processing within extrastriate cortical pathways. However, catch-up saccades largely compensate for the tracking displacement shortfall caused by low pursuit gain, although there still is significant residual retinal slip and thus degraded dynamic acuity. Furthermore, although saccades are more frequent, their dynamics are more sluggish (i.e. show lower peak velocities) starting at BAC levels as low as 0.035%. Small effects in eccentric gaze holding and no effect in pupillary response dynamics were observed at levels below 0.07%, showing the higher sensitivity of the pursuit response to very low levels of blood alcohol, under the conditions of our study.

visual motion processing↗

Studies of the Ability to Hold the Eye in Eccentric Gaze: Measurements in Normal Subjects with the Head Erect

We studied the ability to hold the eyes in eccentric horizontal or vertical gaze angles in 68 normal humans, age range 19-56. Subjects attempted to sustain visual fixation of a briefly flashed target located 30 in the horizontal plane and 15 in the vertical plane in a dark environment. Conventionally, the ability to hold eccentric gaze is estimated by fitting centripetal eye drifts by exponential curves and calculating the time constant (t(sub c)) of these slow phases of gazeevoked nystagmus. Although the distribution of time-constant measurements (t(sub c)) in our normal subjects was extremely skewed due to occasional test runs that exhibited near-perfect stability (large t(sub c) values), we found that log10(tc) was approximately normally distributed within classes of target direction. Therefore, statistical estimation and inference on the effect of target direction was performed on values of z identical with log10t(sub c). Subjects showed considerable variation in their eyedrift performance over repeated trials; nonetheless, statistically significant differences emerged: values of tc were significantly higher for gaze elicited to targets in the horizontal plane than for the vertical plane (P less than 10(exp -5), suggesting eccentric gazeholding is more stable in the horizontal than in the vertical plane. Furthermore, centrifugal eye drifts were observed in 13.3, 16.0 and 55.6% of cases for horizontal, upgaze and downgaze tests, respectively. Fifth percentile values of the time constant were estimated to be 10.2 sec, 3.3 sec and 3.8 sec for horizontal, upward and downward gaze, respectively. The difference between horizontal and vertical gazeholding may be ascribed to separate components of the velocity position neural integrator for eye movements, and to differences in orbital mechanics. Our statistical method for representing the range of normal eccentric gaze stability can be readily applied in a clinical setting to patients who were exposed to environments that may have modified their central integrators and thus require monitoring. Patients with gaze-evoked nystagmus can be flagged by comparing to the above established normative criteria.

Reschke, Millard F.↗

How Eye Drift Adapts to the History of Eye Positions

Oculomotor behavior is a powerful tool to probe brain function and disease. Previous studies have shown how fixational drift velocities depend on eccentricity (Bertolini et al., 2013; Romano et al., 2017) and how fixational drift can adapt after prolonged eccentric fixation (Otero-Millan et al., 2019). Here, eighteen subjects completed two experiments where we measured drift velocity while fixating a briefly flashed target, to remove retinal slip cues. In the first experiment, we measured their baseline relationship between fixational drift velocity and eye position. In the second experiment, we investigated the adaptation of that relationship after prolonged fixation at a very eccentric position. This adaptation usually manifests by the presence of rebound nystagmus (RN) upon returning to central gaze. Our results replicate the finding that drift increases at central fixation in the direction consistent with rebound nystagmus, that is, towards the previously held eccentric position, highlighting that drift velocity depends on the history of eye positions. When examining the entire relationship between drift velocity and eye position we find a mostly linear relationship but with increased slope relative to the baseline condition. However, the adaptation of the integrator cannot be modeled by a simple change in leakiness, as that would not result in increased drift at central gaze. Other mechanisms of adaptation such as shifts in the position or velocity set-points for gaze holding could be present but are indistinguishable with the current data.

eye movement↗