Christopher J. Bockisch

Eye position predicts what number you have in mind

Despite the apparent simplicity of picking numbers at random, it is virtually impossible to produce a sequence of truly random numbers. Although numbers seem to pop-up spontaneously in ones mind, their choice is invariably influenced by previously generated numbers [1]. Here, we demonstrate how the eyes and their position give an insight into the nature of the systematic choices made by the brains ‘random number generator’. By measuring a persons vertical and horizontal eye position, we were able to predict with reliable confidence the size of the next number — before it was spoken. Specifically, a leftward and downward change in eye position announced that the next number would be smaller than the last. Correspondingly, if the eyes changed position to the right and upward, it forecast that the next number would be larger. Apart from supporting the old wisdom that it is often the eyes that betray the mind, the findings highlight the intricate links between supposedly abstract thought processes, the bodys actions and the world around us.

Three-dimensional eye position during static roll and pitch in humans

We investigated how three-dimensional (3D) eye position is influenced by static head position relative to gravity, a reflex probably mediated by the otolith organs. In monkeys, the torsional component of eye position is modulated by gravity, but little data is available in humans. Subjects were held in different head/body tilts in roll and pitch for 35 s while we measured 3D eye position with scleral coils, and we used methods that reduced torsion artifacts produced by the eyelids pressing on the contact lens and exit wire. 3D eye positions were described by planar fits to the data (Listings plane), and changes in these planes showed how torsion varied with head position. Similar to findings in monkeys, the eyes counterrolled during roll tilts independent of horizontal and vertical eye position, reaching a maximum torsion of 4.9 degrees. Counterroll was not proportional to the shear force on the macula of the utricles: gain (torsion/sine of the head roll angle) decreased by 50% from near upright to ear down. During pitch forward, torsion increased when subjects looked right, and decreased when they looked left. However, the maximum change of torsion was only -0.06 degrees per degree of horizontal eye position, which is less than reported in monkey. Also in contrast to monkey, we found little change in torsion when subjects were pitched backwards.

Gravity Dependence of Subjective Visual Vertical Variability

The brain integrates sensory input from the otolith organs, the semicircular canals, and the somatosensory and visual systems to determine self-orientation relative to gravity. Only the otoliths directly sense the gravito-inertial force vector and therefore provide the major input for perceiving static head-roll relative to gravity, as measured by the subjective visual vertical (SVV). Intraindividual SVV variability increases with head roll, which suggests that the effectiveness of the otolith signal is roll-angle dependent. We asked whether SVV variability reflects the spatial distribution of the otolithic sensors and the otolith-derived acceleration estimate. Subjects were placed in different roll orientations (0-360 degrees, 15 degrees steps) and asked to align an arrow with perceived vertical. Variability was minimal in upright, increased with head-roll peaking around 120-135 degrees, and decreased to intermediate values at 180 degrees. Otolith-dependent variability was modeled by taking into consideration the nonuniform distribution of the otolith afferents and their nonlinear firing rate. The otolith-derived estimate was combined with an internal bias shifting the estimated gravity-vector toward the body-longitudinal. Assuming an efficient otolith estimator at all roll angles, peak variability of the model matched our data; however, modeled variability in upside-down and upright positions was very similar, which is at odds with our findings. By decreasing the effectiveness of the otolith estimator with increasing roll, simulated variability matched our experimental findings better. We suggest that modulations of SVV precision in the roll plane are related to the properties of the otolith sensors and to central computational mechanisms that are not optimally tuned for roll-angles distant from upright.

Velocity Storage Contribution to Vestibular Self-Motion Perception in Healthy Human Subjects

Self-motion perception after a sudden stop from a sustained rotation in darkness lasts approximately as long as reflexive eye movements. We hypothesized that, after an angular velocity step, self-motion perception and reflexive eye movements are driven by the same vestibular pathways. In 16 healthy subjects (25-71 years of age), perceived rotational velocity (PRV) and the vestibulo-ocular reflex (rVOR) after sudden decelerations (90°/s(2)) from constant-velocity (90°/s) earth-vertical axis rotations were simultaneously measured (PRV reported by hand-lever turning; rVOR recorded by search coils). Subjects were upright (yaw) or 90° left-ear-down (pitch). After both yaw and pitch decelerations, PRV rose rapidly and showed a plateau before decaying. In contrast, slow-phase eye velocity (SPV) decayed immediately after the initial increase. SPV and PRV were fitted with the sum of two exponentials: one time constant accounting for the semicircular canal (SCC) dynamics and one time constant accounting for a central process, known as velocity storage mechanism (VSM). Parameters were constrained by requiring equal SCC time constant and VSM time constant for SPV and PRV. The gains weighting the two exponential functions were free to change. SPV were accurately fitted (variance-accounted-for: 0.85 ± 0.10) and PRV (variance-accounted-for: 0.86 ± 0.07), showing that SPV and PRV curve differences can be explained by a greater relative weight of VSM in PRV compared with SPV (twofold for yaw, threefold for pitch). These results support our hypothesis that self-motion perception after angular velocity steps is be driven by the same central vestibular processes as reflexive eye movements and that no additional mechanisms are required to explain the perceptual dynamics.

Detection and Grading of Endolymphatic Hydrops in Menière Disease Using MR Imaging

BACKGROUND AND PURPOSE: Endolymphatic hydrops has been recognized as the underlying pathophysiology of Menière disease. We used 3T MR imaging to detect and grade endolymphatic hydrops in patients with Menière disease and to correlate MR imaging findings with the clinical severity. MATERIALS AND METHODS: MR images of the inner ear acquired by a 3D inversion recovery sequence 4 hours after intravenous contrast administration were retrospectively analyzed by 2 neuroradiologists blinded to the clinical presentation. Endolymphatic hydrops was classified as none, grade I, or grade II. Interobserver agreement was analyzed, and the presence of endolymphatic hydrops was correlated with the clinical diagnosis and the clinical Menière disease score. RESULTS: Of 53 patients, we identified endolymphatic hydrops in 90% on the clinically affected and in 22% on the clinically silent side. Interobserver agreement on detection and grading of endolymphatic hydrops was 0.97 for cochlear and 0.94 for vestibular hydrops. The average MR imaging grade of endolymphatic hydrops was 1.27 ± 0.66 for 55 clinically affected and 0.65 ± 0.58 for 10 clinically normal ears. The correlation between the presence of endolymphatic hydrops and Menière disease was 0.67. Endolymphatic hydrops was detected in 73% of ears with the clinical diagnosis of possible, 100% of probable, and 95% of definite Menière disease. CONCLUSIONS: MR imaging supports endolymphatic hydrops as a pathophysiologic hallmark of Menière disease. High interobserver agreement on the detection and grading of endolymphatic hydrops and the correlation of MR imaging findings with the clinical score recommend MR imaging as a reliable in vivo technique in patients with Menière disease. The significance of MR imaging detection of endolymphatic hydrops in an additional 22% of asymptomatic ears requires further study.

A New Dynamic Visual Acuity Test to Assess Peripheral Vestibular Function

OBJECTIVE To evaluate a novel test for dynamic visual acuity (DVA) that uses an adaptive algorithm for changing the size of Landolt rings presented during active or passive head impulses, and to compare the results with search-coil head impulse testing. DESIGN Prospective study in healthy individuals and patients with peripheral vestibular deficits. SETTING Tertiary academic center. PARTICIPANTS One hundred neuro-otologically healthy individuals (age range, 19-80 years) and 15 patients with bilateral (n = 5) or unilateral (n = 10) peripheral vestibular loss (age range, 27-72 years). INTERVENTIONS Testing of static visual acuity (SVA), DVA during active and passive horizontal head rotations (optotype presentation at head velocities >100 degrees/s and >150 degrees/s), and quantitative horizontal head impulse testing with scleral search coils. MAIN OUTCOME MEASURE Difference between SVA and DVA, that is, visual acuity loss (VA loss), gain of the high-acceleration vestibulo-ocular reflex. RESULTS Passive head impulses and higher velocities were more effective than active impulses and lower velocities. Using passive head impulses and velocities higher than 150 degrees/s, the DVA test discriminated significantly (P < .001) among patients with bilateral vestibulopathy, those with unilateral vestibulopathy, and normal individuals. The DVA test sensitivity was 100%, specificity was 94%, and accuracy was 95%, with search-coil head impulse testing used as a reference. In healthy individuals, VA loss increased significantly with age (P < .001; R(2) = 0.04). CONCLUSION Dynamic visual acuity testing with Landolt rings that are adaptively changed in size enables detection of peripheral vestibular dysfunction in a fast and simple way.

Visual contribution to postural stability: Interaction between target fixation or tracking and static or dynamic large-field stimulus

Stationary visual information has a stabilizing effect on posture, whereas moving visual information is destabilizing. We compared the influence of a stationary or moving fixation point to the influence of stationary or moving large-field stimulation, as well as the interaction between a fixation point and a large-field stimulus. We recorded body sway in 20 healthy subjects who were fixating a stationary or oscillating dot (vertical or horizontal motion, 1/3 Hz, +/-12 degrees amplitude, distance 96 cm). In addition, a large-field random dot pattern (extension: approximately 80 x 70 degrees) was stationary, moving or absent. Visual fixation of a stationary dot in darkness did not reduce antero-posterior (AP) sway compared to the situation in total darkness, but slightly reduced lateral sway at frequencies below 0.5 Hz. In contrast, fixating a stationary dot on a stationary large-field pattern reduced both AP and lateral body sway at all frequencies (0.1-2 Hz). Ocular tracking of the oscillating dot caused a peak in body sway at 1/3 Hz, i.e. the stimulus frequency, but there was no influence of large-field stimulus at this frequency. A stationary large-field pattern, however, reduced AP and lateral sway at frequencies between 0.1 and 2 Hz when subjects tracked a moving dot, compared to tracking in darkness. Our results demonstrate that a stationary large-field pattern has a stabilizing effect in all conditions, independent of whether the eyes are fixing on a stationary target or tracking a moving target.

Roll-dependent modulation of the subjective visual vertical: contributions of head- and trunk-based signals.

Precision and accuracy of the subjective visual vertical (SVV) modulate in the roll plane. At large roll angles, systematic SVV errors are biased toward the subjects body-longitudinal axis and SVV precision is decreased. To explain this, SVV models typically implement a bias signal, or a prior, in a head-fixed reference frame and assume the sensory input to be optimally tuned along the head-longitudinal axis. We tested the pattern of SVV adjustments both in terms of accuracy and precision in experiments in which the head and the trunk reference frames were not aligned. Twelve subjects were placed on a turntable with the head rolled about 28 degrees counterclockwise relative to the trunk by lateral tilt of the neck to dissociate the orientation of head- and trunk-fixed sensors relative to gravity. Subjects were brought to various positions (roll of head- or trunk-longitudinal axis relative to gravity: 0 degrees , +/-75 degrees ) and aligned an arrow with perceived vertical. Both accuracy and precision of the SVV were significantly (P < 0.05) better when the head-longitudinal axis was aligned with gravity. Comparing absolute SVV errors for clockwise and counterclockwise roll tilts, statistical analysis yielded no significant differences (P > 0.05) when referenced relative to head upright, but differed significantly (P < 0.001) when referenced relative to trunk upright. These findings indicate that the bias signal, which drives the SVV toward the subjects body-longitudinal axis, operates in a head-fixed reference frame. Further analysis of SVV precision supports the hypothesis that head-based graviceptive signals provide the predominant input for internal estimates of visual vertical.

Is Vestibular Self-Motion Perception Controlled by the Velocity Storage? Insights from Patients with Chronic Degeneration of the Vestibulo-Cerebellum

Background The rotational vestibulo-ocular reflex (rVOR) generates compensatory eye movements in response to rotational head accelerations. The velocity-storage mechanism (VSM), which is controlled by the vestibulo-cerebellar nodulus and uvula, determines the rVOR time constant. In healthy subjects, it has been suggested that self-motion perception in response to earth-vertical axis rotations depends on the VSM in a similar way as reflexive eye movements. We aimed at further investigating this hypothesis and speculated that if the rVOR and rotational self-motion perception share a common VSM, alteration in the latter, such as those occurring after a loss of the regulatory control by vestibulo-cerebellar structures, would result in similar reflexive and perceptual response changes. We therefore set out to explore both responses in patients with vestibulo-cerebellar degeneration. Methodology/Principal Findings Reflexive eye movements and perceived rotational velocity were simultaneously recorded in 14 patients with chronic vestibulo-cerebellar degeneration (28–81yrs) and 12 age-matched healthy subjects (30–72yrs) after the sudden deceleration (90°/s2) from constant-velocity (90°/s) rotations about the earth-vertical yaw and pitch axes. rVOR and perceived rotational velocity data were analyzed using a two-exponential model with a direct pathway, representing semicircular canal activity, and an indirect pathway, implementing the VSM. We found that VSM time constants of rVOR and perceived rotational velocity co-varied in cerebellar patients and in healthy controls (Pearson correlation coefficient for yaw 0.95; for pitch 0.93, p<0.01). When constraining model parameters to use the same VSM time constant for rVOR and perceived rotational velocity, moreover, no significant deterioration of the quality of fit was found for both populations (variance-accounted-for >0.8). Conclusions/Significance Our results confirm that self-motion perception in response to rotational velocity-steps may be controlled by the same velocity storage network that controls reflexive eye movements and that no additional, e.g. cortical, mechanisms are required to explain perceptual dynamics.

Enhanced smooth pursuit eye movements in patients with bilateral vestibular deficits.

Patients with bilateral vestibular deficits experience unsteady gait and oscillopsia that can reduce the quality of life, though many patients adapt remarkably well and lead mostly normal lives. One source of adaptation could be the ability of sensory-motor systems to compensate for the vestibular loss by adaptive enhancement of their performance. We studied smooth-pursuit eye movements in five patients and six healthy control subjects using a step-ramp paradigm. Eye movements were measured with scleral search coils. Patients showed open- and closed-loop pursuit gains that were about 9% higher than controls. We suggest that the challenge of living with a deficient vestibular system caused an enhancement in the pursuit system, which contributes to the patients overall compensation.