The Effect of Target Distance and Stimulus Frequency on Horizontal Eye Movements Induced by Linear Acceleration on a Parallel Swing

Telford, Laura, Scott H. Seidman, and Gary D. Paige. Dynamics of squirrel monkey linear vestibuloocular reflex and interactions with fixation distance. J. Neurophysiol. 78: 1775–1790, 1997. Horizontal, vertical, and torsional eye movements were recorded using the magnetic search-coil technique during linear accelerations along the interaural (IA) and dorsoventral (DV) head axes. Four squirrel monkeys were translated sinusoidally over a range of frequencies (0.5–4.0 Hz) and amplitudes (0.1–0.7 g peak acceleration). The linear vestibuloocular reflex (LVOR) was recorded in darkness after brief presentations of visual targets at various distances from the subject. With subjects positioned upright or nose-up relative to gravity, IA translations generated conjugate horizontal (IA horizontal) eye movements, whereas DV translations with the head nose-up or right-side down generated conjugate vertical (DV vertical) responses. Both were compensatory for linear head motion and are thus translational LVOR responses. In concert with geometric requirements, both IA-horizontal and DV-vertical response sensitivities (in deg eye rotation/cm head translation) were related linearly to reciprocal fixation distance as measured by vergence (in m−1, or meter-angles, MA). The relationship was characterized by linear regressions, yielding sensitivity slopes (in deg⋅cm−1⋅MA−1) and intercepts (sensitivity at 0 vergence). Sensitivity slopes were greatest at 4.0 Hz, but were only slightly more than half the ideal required to maintain fixation. Slopes declined with decreasing frequency, becoming negligible at 0.5 Hz. Small responses were observed when vergence was zero (intercept), although no response is required. Like sensitivity slope, the intercept was largest at 4.0 Hz and declined with decreasing frequency. Phase lead was near zero (compensatory) at 4.0 Hz, but increased as frequency declined. Changes in head orientation, motion axis (IA vs. DV), and acceleration amplitude produced slight and sporadic changes in LVOR parameters. Translational LVOR response characteristics are consistent with high-pass filtering within LVOR pathways. Along with horizontal eye movements, IA translation generated small torsional responses. In contrast to the translational LVORs, IA-torsional responses were not systematically modulated by vergence angle. The IA-torsional LVOR is not compensatory for translation because it cannot maintain image stability. Rather, it likely compensates for the effective head tilt simulated by translation. When analyzed in terms of effective head tilt, torsional responses were greatest at the lowest frequency and declined as frequency increased, consistent with low-pass filtering of otolith input. It is unlikely that IA-torsional responses compensate for actual head tilt, however, because they were similar for both upright and nose-up head orientations. The IA-torsional and -horizontal LVORs seem to respond only to linear acceleration along the IA head axis, and the DV-vertical LVOR to acceleration along the head's DV axis, regardless of gravity.

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Linear Acceleration and Horizontal Eye Movements in Man

Acta Oto-Laryngologica ◽

10.3109/00016489109131401 ◽

1991 ◽

Vol 111 (sup481) ◽

pp. 277-281 ◽

Cited By ~ 5

Author(s):

Mark Shelhamer ◽

Laurence R. Young

Keyword(s):

Eye Movements ◽

Linear Acceleration

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Eye Movements Induced by Linear Acceleration are Modified by Visualisation of Imaginary Targets

Acta Oto-Laryngologica ◽

10.3109/00016488909139063 ◽

1989 ◽

Vol 108 (sup468) ◽

pp. 289-293 ◽

Cited By ~ 27

Author(s):

J. J. Skipper ◽

G. R. Barnes

Keyword(s):

Eye Movements ◽

Linear Acceleration

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Neural Processing of Gravito-Inertial Cues in Humans. I. Influence of the Semicircular Canals Following Post-Rotatory Tilt

Journal of Neurophysiology ◽

10.1152/jn.2000.84.4.2001 ◽

2000 ◽

Vol 84 (4) ◽

pp. 2001-2015 ◽

Cited By ~ 45

Author(s):

L. H. Zupan ◽

R. J. Peterka ◽

D. M. Merfeld

Keyword(s):

Eye Movements ◽

Information Integration ◽

Constant Velocity ◽

Gravitational Force ◽

Inertial Force ◽

Semicircular Canals ◽

Linear Acceleration ◽

Head Orientation ◽

Otolith Organs ◽

Sensory Cues

Sensory systems often provide ambiguous information. Integration of various sensory cues is required for the CNS to resolve sensory ambiguity and elicit appropriate responses. The vestibular system includes two types of sensors: the semicircular canals, which measure head rotation, and the otolith organs, which measure gravito-inertial force (GIF), the sum of gravitational force and inertial force due to linear acceleration. According to Einstein's equivalence principle, gravitational force is indistinguishable from inertial force due to linear acceleration. As a consequence, otolith measurements must be supplemented with other sensory information for the CNS to distinguish tilt from translation. The GIF resolution hypothesis states that the CNS estimates gravity and linear acceleration, so that the difference between estimates of gravity and linear acceleration matches the measured GIF. Both otolith and semicircular canal cues influence this estimation of gravity and linear acceleration. The GIF resolution hypothesis predicts that inaccurate estimates of both gravity and linear acceleration can occur due to central interactions of sensory cues. The existence of specific patterns of vestibuloocular reflexes (VOR) related to these inaccurate estimates can be used to test the GIF resolution hypothesis. To investigate this hypothesis, we measured eye movements during two different protocols. In one experiment, eight subjects were rotated at a constant velocity about an earth-vertical axis and then tilted 90° in darkness to one of eight different evenly spaced final orientations, a so-called “dumping” protocol. Three speeds (200, 100, and 50°/s) and two directions, clockwise (CW) and counterclockwise (CCW), of rotation were tested. In another experiment, four subjects were rotated at a constant velocity (200°/s, CW and CCW) about an earth-horizontal axis and stopped in two different final orientations (nose-up and nose-down), a so-called “barbecue” protocol. The GIF resolution hypothesis predicts that post-rotatory horizontal VOR eye movements for both protocols should include an “induced” VOR component, compensatory to an interaural estimate of linear acceleration, even though no true interaural linear acceleration is present. The GIF resolution hypothesis accurately predicted VOR and induced VOR dependence on rotation direction, rotation speed, and head orientation. Alternative hypotheses stating that frequency segregation may discriminate tilt from translation or that the post-rotatory VOR time constant is dependent on head orientation with respect to the GIF direction did not predict the observed VOR for either experimental protocol.

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Multiple Sensory Cues Underlying the Perception of Translation and Path

Journal of Neurophysiology ◽

10.1152/jn.00694.2006 ◽

2007 ◽

Vol 97 (2) ◽

pp. 1100-1113 ◽

Cited By ~ 25

Author(s):

N. Au Yong ◽

G. D. Paige ◽

S. H. Seidman

Keyword(s):

Sudden Change ◽

Sensory Information ◽

Stimulus Frequency ◽

Linear Acceleration ◽

Low Frequencies ◽

Motion Cues ◽

High Frequencies ◽

Shift Experiment ◽

Self Motion ◽

Motion Profile

The translational linear vestibuloocular reflex compensates most accurately for high frequencies of head translation, with response magnitude decreasing with declining stimulus frequency. However, studies of the perception of translation typically report robust responses even at low frequencies or during prolonged motion. This inconsistency may reflect the incorporation of nondirectional sensory information associated with the vibration and noise that typically accompany translation, into motion perception. We investigated the perception of passive translation in humans while dissociating nondirectional cues from actual head motion. In a cue-dissociation experiment, interaural (IA) motion was generated using either a linear sled, the mechanics of which generated noise and vibration cues that were correlated with the motion profile, or a multiaxis technique that dissociated these cues from actual motion. In a trajectory-shift experiment, IA motion was interrupted by a sudden change in direction (±30° diagonal) that produced a change in linear acceleration while maintaining sled speed and therefore mechanical (nondirectional) cues. During multi-axis cue-dissociation trials, subjects reported erroneous translation perceptions that strongly reflected the pattern of nondirectional cues, as opposed to nearly veridical percepts when motion and nondirectional cues coincided. During trajectory-shift trials, subjects' percepts were initially accurate, but erroneous following the direction change. Results suggest that nondirectional cues strongly influence the perception of linear motion, while the utility of cues directly related to translational acceleration is limited. One key implication is that “path integration” likely involves complex mechanisms that depend on nondirectional and contextual self-motion cues in support of limited and transient otolith-dependent acceleration input.

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Gaze strategies during linear motion in head-free humans

Journal of Neurophysiology ◽

10.1152/jn.1994.72.5.2451 ◽

1994 ◽

Vol 72 (5) ◽

pp. 2451-2466 ◽

Cited By ~ 11

Author(s):

L. Borel ◽

B. Le Goff ◽

O. Charade ◽

A. Berthoz

Keyword(s):

Eye Movements ◽

Human Subjects ◽

Linear Acceleration ◽

Slow Phase ◽

Head Motion ◽

Functional Coupling ◽

Linear Motion ◽

Experimental Conditions ◽

Coordination Strategies ◽

Phase Direction

1. Eye-head coordination strategies during horizontal displacements along the y (interaural) axis were investigated in human subjects seated on a sled (linear accelerator device) and tested in head-free conditions. They were instructed to stabilize their gaze, while in motion, on an earth-fixed memorized target and then, after cart immobilization, to look again at the real target. The last part of the test required a corrective saccade, which enabled us to evaluate the error of the subject's displacement estimation. Eye and head compensatory reflexes were tested within the 0.001–0.2 g acceleration range with a sinusoidal motion amplitude of 0.8 m peak to peak. 2. Fixation stabilization on a memorized target was achieved by different eye-head coordination strategies. According to the relative contribution of eye and head motion, a continuum among individual strategies was observed, covering a range of head contributions varying from 0 to almost 100%. All these strategies were well adapted because they contributed to the counteraction of the displacement and led to an optimal gaze accuracy. 3. The use of various gaze strategies during linear motion to achieve the same movement differed according to the subject, but also depended upon motion kinematics. As a rule, head contribution increased as the magnitude of linear acceleration was enhanced. 4. Different eye-head coordination strategies implicated either a linear vestibulo-ocular reflex (LVOR) or ocular responses composed of a combination of antagonistic angular and linear vestibulo-ocular reflexes (AVOR-LVOR). The slow phase direction of these two oculomotor responses for fixation stabilization on the target were compensatory and anticompensatory, respectively. 5. One of the major points of this study was the contribution of the saccadic system to gaze strategies, even in our experimental conditions where the head was free to move. We concluded that vestibular-saccadic cooperation appears to be a common feature in the elaboration of adequate fixation stabilization in daily life situations. 6. The functional coupling of these various subsystems involved in fixation stabilization depended on the range of motion: while the acceleration increased, the saccadic eye movements were replaced by vestibulo-ocular responses whose slow phase direction was opposite that of head motion and, therefore, directed away from the target. 7. Fast components of the nystagmic pattern of eye movements were able to improve gaze position accuracy, bringing the eyes toward the memorized target.(ABSTRACT TRUNCATED AT 400 WORDS)

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Imaginary Gaze Effects on Eye Movements Induced by Linear Acceleration: Involvement of Vestibular Induced Smooth Pursuit Eye Movement

Acta Oto-Laryngologica ◽

10.3109/00016489509125274 ◽

1995 ◽

Vol 115 (sup520) ◽

pp. 372-376 ◽

Cited By ~ 3

Author(s):

M. Hashiba ◽

S. Watanabe ◽

H. Watabe ◽

T. Matsuoka ◽

S. Baba ◽

...

Keyword(s):

Eye Movements ◽

Eye Movement ◽

Smooth Pursuit ◽

Linear Acceleration ◽

Smooth Pursuit Eye Movement

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Motor Scaling By Viewing Distance of Early Visual Motion Signals During Smooth Pursuit

Journal of Neurophysiology ◽

10.1152/jn.00476.2002 ◽

2002 ◽

Vol 88 (5) ◽

pp. 2880-2885 ◽

Cited By ~ 5

Author(s):

Hui-Hui Zhou ◽

Min Wei ◽

Dora E. Angelaki

Keyword(s):

Eye Movements ◽

Visual Motion ◽

Neural Substrates ◽

Open Loop ◽

Target Distance ◽

Viewing Distance ◽

Major Pathway ◽

Gaze Stabilization ◽

Order Of Magnitude ◽

Eye Velocity

The geometry of gaze stabilization during head translation requires eye movements to scale proportionally to the inverse of target distance. Such a scaling has indeed been demonstrated to exist for the translational vestibuloocular reflex (TVOR), as well as optic flow–selective translational visuomotor reflexes (e.g., ocular following, OFR). The similarities in this scaling by a neural estimate of target distance for both the TVOR and the OFR have been interpreted to suggest that the two reflexes share common premotor processing. Because the neural substrates of OFR are partly shared by those for the generation of pursuit eye movements, we wanted to know if the site of gain modulation for TVOR and OFR is also part of a major pathway for pursuit. Thus, in the present studies, we investigated in rhesus monkeys whether initial eye velocity and acceleration during the open-loop portion of step ramp pursuit scales with target distance. Specifically, with visual motion identical on the retina during tracking at different distances (12, 24, and 60 cm), we compared the first 80 ms of horizontal pursuit. We report that initial eye velocity and acceleration exhibits either no or a very small dependence on vergence angle that is at least an order of magnitude less than the corresponding dependence of the TVOR and OFR. The results suggest that the neural substrates for motor scaling by target distance remain largely distinct from the main pathway for pursuit.

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Spatial organization of linear vestibuloocular reflexes of the rat: responses during horizontal and vertical linear acceleration

Journal of Neurophysiology ◽

10.1152/jn.1991.66.6.1805 ◽

1991 ◽

Vol 66 (6) ◽

pp. 1805-1818 ◽

Cited By ~ 58

Author(s):

B. J. Hess ◽

N. Dieringer

Keyword(s):

Eye Movements ◽

Spatial Organization ◽

Head Tilt ◽

Semicircular Canals ◽

Linear Acceleration ◽

Viewing Distance ◽

Phase Lag ◽

Linear Motion ◽

Common Reference ◽

Vertical Linear Acceleration

1. The spatial properties of linear vestibuloocular reflexes (LVOR) were studied in pigmented rats in response to sinusoidal linear acceleration on a sled. The orientation of the animal on the sled was altered in 15 degrees steps over the range of 360 degrees. Horizontal, vertical, and torsional components of eye movements were recorded with the magnetic field search coil technique in complete darkness. Conjugacy of the two eyes was studied in the horizontal movement plane. 2. Acceleration along the optic axis of one eye (approximately 50 degrees lateral) induced maximal vertical responses in the ipsilateral eye and, at the same time, maximal torsional responses in the contralateral eye. These vertical and torsional responses of the LVOR coincide with those obtained when the respective coplanar vertical semicircular canals are stimulated. Such a congruence suggests a common reference frame for LVOR and angular vestibuloocular reflexes (AVOR), with the result that direct combination of signals indicating apparent and real head tilt is facilitated. 3. Transformations of vertical and torsional responses into head coordinates (pitch and roll) show that these movements are compensatory in direction for any combination of apparent head tilt in pitch and roll planes. 4. Gain (rotation of the eye/apparent rotation of the gravity direction) was approximately 0.3 at 0.1 Hz and decreased to approximately 0.1 at 1.0 Hz. Vertical responses tended to have a larger gain than torsional responses. Phase lag relative to peak acceleration increased from about -9 degrees to about -47 degrees over the same frequency range. 5. Vertical linear acceleration evoked only vertical eye movements at a frequency of 1.0 Hz. 6. Horizontal responses of both eyes were symmetric or asymmetric in amplitude and in-phase (conjugate) or out-of-phase (disconjugate) with respect to each other, depending on the direction of linear acceleration. Translation in the transverse direction evoked conjugate compensatory horizontal responses. Forward-backward translation evoked movements of both eyes that were symmetric in amplitude, but 180 degrees out-of-phase. Translation along diagonal axes evoked almost no horizontal responses in the eye facing in the direction of linear motion but maximal horizontal responses in the eye facing away from the direction of linear motion. These disconjugate movements resulted in a modulation of the vergence angle of the eyes. 7. Disconjugate horizontal responses in darkness are best explained by the assumption that part of the visual consequences of a translational head displacement (i.e., change of viewing distance in light) is taken into account centrally.(ABSTRACT TRUNCATED AT 400 WORDS)

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