Dominik Straumann

Listing's law for eye, head and arm movements and their synergistic control

SummaryWe have recorded eye, head, and upper arm rotations in five healthy human subjects using the three-dimensional search coil technique. Our measurements show that the coordination of eye and head movements during gaze shifts within ± 25 deg relative to the forward direction is organized by restricting the rotatory trajectories of the two systems to almost parallel planes. These so-called “Listing planes” for eye-in-space and head-in-space rotations are workspace-oriented, not body-fixed. Eye and head trajectories in their respective planes are closely related in direction and amplitude. For pointing or grasping, the rotatory trajectories of the arm are also restricted to a workspace-oriented Listing plane. During visually guided movements, arm follows gaze, and the nine-dimensional rotatory configuration space for eye-head-arm-synergies (three degrees of freedom for each system) is reduced to a two-dimensional plane in the space of quaternion vectors.

Static Roll and Pitch in the Monkey: Shift and Rotation of Listing's Plane

In three rhesus monkeys three-dimensional eye positions were measured with the dual search coil technique. Recordings of spontaneous eye movements were made in the light and in the dark, with the monkeys in different static roll or pitch positions. Eye positions were expressed as rotation vectors. In all static positions eye rotation vectors were confined to a plane, i.e. Listings plane was conserved. Tilt about the roll axis shifted the plane along this axis, i.e. a constant torsional component was added to all eye positions. Tilt about the pitch axis changed the pitch angle of Listings plane.

Caloric and search-coil head-impulse testing in patients after vestibular neuritis.

The objective of this study was to compare results of quantitative head-impulse testing using search coils with eye-movement responses to caloric irrigation in patients with unilateral vestibular hypofunction after vestibular neuritis. The study population consisted of an acute group (<3 days; N = 10; 5 male, 5 female; 26-89 years old) and a chronic group (>2 months; N = 14; 8 male, 6 female; 26-78 years old) of patients with unilateral vestibular hypofunction after vestibular neuritis. The testing battery included: (1) simultaneous measurement of eye and head rotations with search coils in a magnetic coil frame during passive Halmagyi-Curthoys head-impulse testing and (2) electronystagmography during bilateral monaural 44 degrees C-warm and 30 degrees C-cold caloric irrigation. The main outcome measures were (1) the gain of the horizontal vestibulo-ocular reflex during search-coil head-impulse testing and (2) the amount of canal paresis during caloric irrigation. All acute and chronic patients had a unilateral gain reduction during search-coil head-impulse testing. A pathological canal paresis factor was present in 100% of the acute patients but in only 64% of the chronic patients. The clinically suspected unilateral vestibular hypofunction resulting from vestibular neuritis was validated in all acute patients by both search-coil head-impulse and caloric testing. Hence, either of these tests is sufficient for diagnosis in the acute phase of vestibular neuritis. Chronic patients, however, were reliably identified only by search-coil head-impulse testing, which suggests that the low-frequency function of the labyrinths often becomes symmetrical, leading to a normal canal paresis factor.

Deficits in torsional and vertical rapid eye movements and shift of Listing's plane after uni- and bilateral lesions of the rostral interstitial nucleus of the medial longitudinal fasciculus

The rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF) contains burst neurons whose activity precedes rapid eye movements with a vertical and/or torsional component. To ascertain their causal role in the generation of conjugate eye movements, we placed uni- and bilateral kainic acid lesions in that region. Unilateral inactivation of the riMLF leads to a loss of all rapid eye movements with an ipsitorsional component (ipsitorsional is defined as movement of the upper pole of the ipsilateral eye in a temporal direction). Vertical eye movements are impaired in an asymmetric way, with downward movements slowed and upward movements little affected. Listings plane is shifted in the contratorsional direction, i.e., we find a constant torsional offset for all eye positions. With bilateral lesions one observes a total loss of all vertical and torsional eye movements, while Listings plane retains its shape and position. These results show that burst neurons in the riMLF play a decisive role in generating rapid eye movements with a vertical and torsional component.

Gravity dependence of ocular drift in patients with cerebellar downbeat nystagmus

Downbeat nystagmus is a frequent ocular motor sign in patients with lesions of the vestibulocerebellum. The upward drift in downbeat nystagmus is a combination of a gaze‐evoked drift, due to an impaired vertical neural integrator, and a velocity bias. Using a three‐dimensional turntable, we analyzed the influence of gravity on these two mechanisms. Patients with cerebellar downbeat nystagmus (n = 6) and healthy subjects (n = 12) were placed in various whole‐body positions along the roll, pitch, and oblique vertical planes of the head. Ocular drift was monitored with scleral search coils. Although there was no gravity dependence of the vertical gaze‐evoked drift, the vertical velocity bias consisted of two components: a gravity‐dependent component that sinusoidally modulated as a function of body position along the pitch plane, and a gravity‐independent component that was directed upward. The combination of the two components led to an overall drift that was minimal in supine and maximal in prone position. In healthy subjects, only the gravity‐dependent component was present, but in a scaled‐down manner. Our results suggest that the intact vestibulocerebellum minimizes an overacting otolith‐ocular reflex elicited by pitch tilt and cancels an inherent upward ocular drift that is independent of gravity‐modulated otolith signals.

Single motor unit activity in human extraocular muscles during the vestibulo‐ocular reflex

•  While the eye movements have been well characterized during the vestibulo‐ocular reflex, the corresponding motor unit activity in human eye muscles is not well understood. •  The present study describes the first single motor unit recordings during the vestibulo‐ocular reflex in human eye muscles. •  Simultaneous needle and surface recordings identified the inferior oblique as the eye muscle of origin of the ocular vestibular evoked myogenic potential (oVEMP), thus validating the physiological basis of this clinical test of otolith function. •  The results demonstrate short‐latency vestibulo‐ocular projections from the otoliths to individual eye muscles. •  Single motor unit activity of eye muscles provides a window into neural activity of the ocular motor nuclei in humans.

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.

Translation, cross-cultural adaptation and reliability of the German version of the dizziness handicap inventory

Objective: To translate the Dizziness Handicap Inventory into German (DHI-G) and investigate reliability, assess the association between selected items of the University of California Los Angeles Dizziness Questionnaire and the DHI-G, and compare the scores of patients and healthy participants. Study Design: Cross-sectional design. Setting: Tertiary center for vertigo, dizziness, or balance disorders. Patients: One hundred forty-one patients with vertigo, dizziness, and unsteadiness associated with a vestibular disorder, with a mean age (standard deviation) of 51.5 (13.2) years, and 52 healthy individuals participated. Interventions: Fourteen patients participated in the cognitive debriefing; 127 patients completed the questionnaires once or twice within 1 week. Main Outcome Measures: The DHI-G assesses disability caused by dizziness and unsteadiness; the items of the University of California Los Angeles Dizziness Questionnaire assess dizziness and impact on everyday activities. Internal consistency was estimated using Cronbach &agr;, reproducibility by calculating Bland-Altman limits of agreement and intraclass correlation coefficients. Associations were estimated by Spearman correlation coefficients. Results: Patients filled out the DHI-G without problem and found that their self-perceived disabilities were mostly included. Cronbach &agr; values for the DHI-G and the functional, physical, and emotional subscales were 0.90, 0.80, 0.71, and 0.82, respectively. The limits of agreement were ±12.4 points for the total scale (maximum, 100 points). Intraclass correlation coefficients ranged from 0.90 to 0.95. The DHI-G correlated moderately with the question assessing functional disability (0.56) and fairly with the questions quantifying dizziness (0.43, 0.35). The DHI-G discriminated significantly between healthy participants and patients. Conclusion: The DHI-G demonstrated good reliability and is recommended as a measure of disability in patients with dizziness and unsteadiness.

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.

Pathomechanism of mammalian downbeat nystagmus due to cerebellar lesion: a simple hypothesis

Most of the various hypotheses on the pathomechanism of the slight ocular upward drift in normal mammals and on the prominent downbeat nystagmus following cerebellar lesions assume an inherent vertical asymmetry in the central vestibulo-ocular pathways. In this paper we propose that this vertical asymmetry is simply based on the anatomical orientation of the six semicircular canals in the head which is right-left symmetrical but lacks symmetry in the cranio-caudal direction. Presuming that each semicircular canal elicits eye movements in a direction roughly in its anatomical plane, vectorial addition of the tonic resting activity of all six canals leads to a cancellation of horizontal and torsional eye movement components but leaves an important vertical (slow phase) upward component. This peripheral vestibular bias is centrally cancelled by floccular and parafloccular inhibitory pathways which are related to the smooth pursuit system, but becomes disinhibited in the presence of posterior cerebellar lesions.