Scott H. Seidman

Tilt perception during dynamic linear acceleration

Abstract Head tilt is a rotation of the head relative to gravity, as exemplified by head roll or pitch from the natural upright orientation. Tilt stimulates both the otolith organs, owing to shifts in gravitational orientation, and the semicircular canals in response to head rotation, which in turn drive a variety of behavioral and perceptual responses. Studies of tilt perception typically have not adequately isolated otolith and canal inputs or their dynamic contributions. True tilt cannot readily dissociate otolith from canal influences. Alternatively, centrifugation generates centripetal accelerations that simulate tilt, but still entails a rotatory (canal) stimulus during important periods of the stimulus profiles. We reevaluated the perception of head tilt in humans, but limited the stimulus to linear forces alone, thus isolating the influence of otolith inputs. This was accomplished by employing a centrifugation technique with a variable-radius spinning sled. This allowed us to accelerate the sled to a constant angular velocity (128°/s), with the subject centered, and then apply dynamic centripetal accelerations after all rotatory perceptions were extinguished. These stimuli were presented in the subjects’ naso-occipital axis by translating the subjects 50 cm eccentrically either forward or backward. Centripetal accelerations were thus induced (0.25 g), which combined with gravity to yield a dynamically shifting gravitoinertial force simulating pitch-tilt, but without actually rotating the head. A magnitude-estimation task was employed to characterize the dynamic perception of pitch-tilt. Tilt perception responded sluggishly to linear acceleration, typically reaching a peak after 10–30 s. Tilt perception also displayed an adaptation phenomenon. Adaptation was manifested as a per-stimulus decline in perceived tilt during prolonged stimulation and a reversal aftereffect upon return to zero acceleration (i.e., recentering the subject). We conclude that otolith inputs can produce tilt perception in the absence of canal stimulation, and that this perception is subject to an adaptation phenomenon and low-pass filtering of its otolith input.

Evaluation of a video tracking device for measurement of horizontal and vertical eye rotations during locomotion

We have evaluated a video-based method for measuring binocular horizontal and vertical eye movements of human subjects by comparing it with the magnetic search coil technique. This video tracking system (VTS) uses multiple infrared light sources and small video cameras to simultaneously measure the positions of reflected corneal images and the center of the pupil. The system has a linear range of approximately +/- 40 degrees horizontally and +/- 30 degrees vertically, a sampling rate of 120 Hz (180 Hz with the head fixed), and system noise with standard deviation of < 0.04 degree. The binocular eye-tracking system is light-weight (190 g), being mounted on goggles that, with the eyes in primary position, permit a field of view of 60 degrees horizontally and vertically. The VTS is insensitive to translations of the tracker relative to the eyes. By placing the video preprocessing unit on a cart, eye movements may be recorded while subjects walk through distances up to 100 feet. In comparison with the magnetic search coil technique, the VTS generally provides reliable measurements of horizontal and vertical eye position; eye velocity is noisier than corresponding coil signals, but superior to electro-oculography.

Characteristics of the VOR in Response to Linear Acceleration

Abstract: The primate linear VOR (LVOR) includes two forms. First, eye‐movement responses to translation [e.g., horizontal responses to interaural (IA) motion] help maintain binocular fixation on targets, and therefore a stable bifoveal image. The translational LVOR is strongly modulated by fixation distance, and operates with high‐pass dynamics (>1 Hz). Second, other LVOR responses occur that cannot be compensatory for translation and instead seem compensatory for head tilt. This reflects an otolith response ambiguity‐that is, an inability to distinguish head translation from head tilt relative to gravity. Thus, ocular torsion is appropriately compensatory for head roll‐tilt, but also occurs during IA translation, since both stimuli entail IA acceleration. Unlike the IA‐horizontal response, IA torsion behaves with low‐pass dynamics (with respect to “tilt”), and is uninfluenced by fixation distance. Interestingly, roll‐tilt, like IA translation, also produces both horizontal (a translational reflex) and torsional (a tilt reflex) responses, further emphasizing the ambiguity problem. Early data from subjects following unilateral labyrinthectomy, which demonstrates a general immediate decline in translational LVOR responses, are also presented, followed by only modest recovery over several months. Interestingly, the usual high‐pass dynamics of these reflexes shift to an even higher cutoff. Both eyes respond roughly equally, suggesting that unilateral otolith input generates a binocularly symmetric LVOR.

Dynamic properties of the human vestibulo-ocular reflex during head rotations in roll

We investigated the dynamic properties of the human vestibulo-ocular reflex (VOR) during roll head rotations in three human subjects using the magnetic search coil technique. In the first of two experiments, we quantify the behavior of the ocular motor plant in the torsional plane. The subjects eye was mechanically displaced into intorsion, extorsion or abduction, and the dynamic course of return of the eye to its resting position was measured. The mean predominant time constants of return were 210 msec from intorsion, 83 msec from extorsion, and 217 msec from abduction, although there was considerable variability of results from different trials and subjects. In the second experiment, we quantify the efficacy of velocity-to-position integration of the vestibular signal. Position-step stimuli were used to test the torsional or horizontal VOR, being applied with subjects heads erect or supine. After a torsional position-step, the eye drifted back to its resting position, but after a horizontal position-step the eye held its new horizontal position. To interpret these responses we used a simple model of the VOR with parameters of the ocular motor plant set to values determined during Exp 1. The time constant of the velocity-to-position neural integrator was smaller (typically 2 sec) in the torsional plane than in the horizontal plane (> 20 sec). No disconjugacy of torsional eye movements was observed. Thus, the dynamic properties of the VOR in roll differ significantly from those of the VOR in yaw, reflecting different visual demands placed on this reflex in these two planes.

The human torsional vestibulo-ocular reflex during rotation about an earth-vertical axis

Using the magnetic search coil technique, we have measured the gain and time constant (Tvor) of the torsional vestibulo-ocular reflex (VOR) in 4 subjects who were rotated about an earth-vertical axis with their necks extended and faces supine. Following a 1-min period of rotation in darkness at 50 degrees/s, the post-rotational response to a velocity off-step had a group mean gain of 0.43 and Tvor of 3.7 s. Following a 1-min period of rotation in the light at 50 degrees/s, the post-rotational response in darkness had a group mean gain of 0.29 and Tvor of 4.1 s. Following rotation in darkness with the neck flexed and head prone, the post-rotational response, measured in two subjects, had a mean gain of 0.39 and Tvor of 5.7 s. Similar results were obtained with 100 degrees/s stimuli. In all subjects, the gain and Tvor of the torsional VOR were smaller than corresponding values for their horizontal VOR; these smaller values can be related to the different visual demands made of the torsional VOR.

Canal-otolith interactions in the squirrel monkey vestibulo-ocular reflex and the influence of fixation distance.

Abstract Natural head movements include angular and linear components of motion. Two classes of vestibulo-ocular reflex (VOR), mediated by the semicircular canals and otoliths (the angular and linear VOR, or AVOR and LVOR, respectively), compensate for head movements and help maintain binocular fixation on targets in space. In this study, AVOR/LVOR interactions were quantified during complex head motion over a broad range of fixation distances at a fixed stimulus frequency of 4.0 Hz. Binocular eye movements were recorded (search-coil technique) in squirrel monkeys while fixation distance (assessed by vergence) was varied using brief presentations of earth-fixed targets at various distances. Stimuli consisted of rotations around an earth-vertical axis and therefore always activated the AVOR. Horizontal and vertical AVORs were assessed when the head was centered over the axis of rotation and oriented upright (UP) and right-side-down (RD), respectively. AVOR gains increased slightly with increasing vergence in darkness, as expected given the small anterior position of the eyes in the head. Combined AVOR/LVOR responses were recorded when subjects were displaced eccentrically from the rotation axis. Eccentric rotations activated the AVOR just as when the head was centered, but added a translational stimulus which generated an LVOR component in response to interaural (IA) or dorsoventral (DV) tangential accelerations, depending on whether the head was UP or RD, respectively. When the head was eccentric and facing nose-out, the AVOR and LVOR produced ocular responses in the same plane and direction (coplanar and synergistic), and response magnitudes increased with increasing vergence. With the head facing nose-in, AVOR and LVOR response components were oppositely directed (coplanar and antagonistic). The AVOR dominated the response when fixation distance was far, and phase was compensatory for head rotation. As fixation distance decreased toward the rotation axis, responses declined to near zero, and when fixation distance approached even closer, the LVOR component dominated and response phase inverted. The same pattern was observed for both horizontal (head UP) and vertical (head RD) responses. The LVOR was recorded directly by rotating subjects eccentrically but in the nose-up (NU) orientation. The AVOR then generated torsional responses to head roll, coexistent with either horizontal or vertical LVOR responses to tangential acceleration when the subject was oriented head-out or right-side-out, respectively. Only the LVOR response components were modulated by vergence. A vectorial analysis of AVOR, LVOR, and combined responses supports the conclusion that AVOR and LVOR response components combine linearly during complex head motion.

Behavior of human horizontal vestibulo-ocular reflex in response to high-acceleration stimuli

We studied the horizontal vestibulo-ocular reflex (VOR) during transient, high-acceleration (1900-7100 degrees/s2) head rotations in 4 human subjects. Such stimuli perturbed the angle of gaze and caused illusory movement of a viewed target (oscillopsia). The disturbance of gaze could be attributed to the latency of the VOR (which ranged from 6-15 ms) and inadequate compensatory eye rotations (median VOR gain ranged from 0.61-0.83).

The stability of human eye orientation during visual fixation

Using the magnetic search coil technique, gaze stability in the horizontal, vertical and torsional planes was measured binocularly in human subjects during visual fixation. Horizontal and vertical eye rotations exhibited a mixture of slow drifts and resetting microsaccades yielding an average standard deviation of 0.11 and 0.10 deg, respectively. In contrast, torsional rotations showed unsystematic smooth drifts with fewer saccades yielding an average standard deviation of 0.18 deg. The lower precision of gaze control in the torsional plane may reflect (i) a discrepancy between the encoding of retinal images in two dimensions but of ocular motor control signals in three dimensions, and (ii) the visual consequences of ocular drifts in the torsional plane, which differ from those in the horizontal and vertical planes.

Canal-otolith interactions driving vertical and horizontal eye movements in the squirrel monkey

The vestibulo-ocular reflex (VOR) was studied in three squirrel monkeys subjected to rotations with the head either centered over, or displaced eccentrically from, the axis of rotation. This was done for several different head orientations relative to gravity in order to determine how canal-mediated angular (aVOR) and otolithmediated linear (lVOR) components of the VOR are combined to generate eye movement responses in three-dimensional space. The aVOR was stimulated in isolation by rotating the head about the axis of rotation in the upright (UP), right-side down (RD), or nose-up (NU) orientations. Horizontal and vertical aVOR responses were compensatory for head rotation over the frequency range 0.25–4.0 Hz, with mean gains near 0.9. The horizontal aVOR was relatively constant across the frequency range, while vertical aVOR gains increased with increasing stimulation frequency. In the NU orientation, compensatory torsional aVOR responses were of relatively low gain (0.54) compared with horizontal and vertical responses, and gains remained constant over the frequency range. When the head was displaced eccentrically, rotation provided the same angular stimuli but added linear stimulus components, due to the centripetal and tangential accelerations acting on the head. By manipulating the orientation of the head relative to gravity and relative to the axis of rotation, the lVOR response could be combined with, or isolated from, the aVOR response. Eccentric rotation in the UP and RD orientations generated aVOR and lVOR responses which acted in the same head plane. Horizontal aVOR-lVOR interactions were recorded when the head was in the UP orientation and facing toward (“nose-in”) or away from (“nose-out”) the rotation axis. Similarly, vertical responses were recorded with the head RD and in the nose-out or nose-in positions. For both horizontal and vertical responses, gains were dependent on both the frequency of stimulation and the directions and relative amplitudes of the angular and linear motion components. When subjects were positioned nose-out, the angular and linear stimuli produced synergistic interactions, with the lVOR driving the eyes in the same direction as the aVOR. Gains increased with increasing frequency, consistent with an addition of broad-band aVOR and high-pass lVOR components. When subjects were nose-in, angular and linear stimuli generated eye movements in opposing directions, and gains declined with increasing frequency, consistent with a subtraction of the lVOR from the aVOR. This response pattern was identical for horizontal and vertical eye movements. aVOR and lVOR interactions were also assessed when the two components acted in orthogonal response planes. By rotating the monkeys into the NU orientation, the aVOR acted primarily in the roll plane, generating torsional ocular responses, while the translational (lVOR) component generated horizontal or vertical ocular responses, depending on whether the head was oriented such that linear accelerations acted along the interaural or dorsoventral axes, respectively. Horizontal and vertical lVOR responses were negligible at 0.25 Hz and increased dramatically with increasing frequency. Comparison of the combined responses (UP and RD orientations) with the isolated aVOR (head-centered) and lVOR (NU orientation) responses, indicates that these VOR components sum in a linear fashion during complex head motion.

A Neurobiological Approach to Acquired Nystagmus

Abstract: The development of animal and mathematical models for several forms of acquired nystagmus has led to more comprehensive knowledge of these disorders. In the best understood forms, such as periodic alternating nystagmus, our range of knowledge includes an animal model, the neurotransmitters involved, and effective treatment. For some other forms, such as downbeat nystagmus, we have an animal model, but reliable treatment is lacking. In other cases, exemplified by acquired pendular nystagmus, we have only a provisional hypothesis for pathogenesis to account for the oscillations, without an animal model, but effective treatment is possible in some patients. The present trend of studying all aspects of the neurobiology of nystagmus, from molecules to behavior, seems to be the best approach to extend our knowledge and to identify new treatments, but much remains to be done.