Daniel M. Merfeld

The vestibulo-ocular reflex of the squirrel monkey during eccentric rotation and roll tilt

The vestibulo-ocular reflexes (VOR) are determined not only by angular acceleration, but also by the presence of gravity and linear acceleration. This phenomenon was studied by measuring three-dimensional nystagmic eye movements, with implanted search coils, in six male squirrel monkeys during eccentric rotation. Monkeys were rotated in the dark at a constant velocity of 200°/s (centrally or 79 cm off axis) with the axis of rotation always aligned with gravity and the spinal axis of the upright monkeys. The monkeys orientation (facing-motion or back-to-motion) had a dramatic influence on the VOR. These experiments show that: (a) the axis of eye rotation always shifted toward alignment with gravito-inertial force; (b) the peak value of horizontal slow phase eye velocity was greater with the monkey facingmotion than with back-to-motion; and (c) the time constant of horizontal eye movement decay was smaller with the monkey facing-motion than with back-to-motion. All of these findings were statistically significant and consistent across monkeys. In another set of tests, the same monkeys were rapidly tilted about their naso-occipital (roll) axis. Tilted orientations of 45° and 90° were maintained for 1 min. Other than a compensatory angular VOR during the angular rotation, no consistent eye velocity response was observed during or following the tilt for any of the six monkeys. The absence of any eye movement response following tilt weighs against the possibility that translational linear VOR responses are due to simple high-pass filtering of the otolith signals. The VOR response during eccentric rotation was divided into the more familiar angular VOR and linear VOR components. The angular component is known to depend upon semicircular canal dynamics and central influences. The linear component of the response decays rapidly with a mean duration of only 6.6 s, while the axis of eye rotation rapidly aligns (<10 s) with gravito-inertial force. These results are consistent with the hypothesis that the measurement of gravito-inertial force by the otolith organs is resolved into central estimates of linear acceleration and gravity, such that the central estimate of gravitational force minus the central estimate of linear acceleration approximately equals the otolith measurement of gravito-inertial force.

Modeling Human Vestibular Responses during Eccentric Rotation and Off Vertical Axis Rotation

A mathematical model has been developed to help explain human multi-sensory interactions. The most important constituent of the model is the hypothesis that the nervous system incorporates knowledge of sensory dynamics into an internal model of these dynamics. This internal model allows the nervous system to integrate the sensory information from many different sensors into a coherent estimate of self-motion. The essence of the model is unchanged from a previously published model of monkey eye movement responses; only a few variables have been adjusted to yield the prediction of human responses. During eccentric rotation, the model predicts that the axis of eye rotation shifts slightly toward alignment with gravito-inertial force. The model also predicts that the time course of the perception of tilt following the acceleration phase of eccentric rotation is much slower than that during deceleration. During off vertical axis rotation (OVAR) the model predicts a small horizontal bias along with small horizontal, vertical, and torsional oscillations. Following OVAR stimulation, when stopped right- or left-side down, a small vertical component is predicted that decays with the horizontal post-rotatory response. All of the predictions are consistent with measurements of human responses.

The dynamic contributions of the otolith organs to human ocular torsion

We measured human ocular torsion (OT) monocularly (using video) and binocularly (using search coils) while sinusoidally accelerating (0.7 g) five human subjects along an earth-horizontal axis at five frequencies (0.35, 0.4, 0.5, 0.75, and 1.0 Hz). The compensatory nature of OT was investigated by changing the relative orientation of the dynamic (linear acceleration) and static (gravitational) cues. Four subject orientations were investigated: (1) Y-upright — acceleration along the interaural (y) axis while upright; (2) Y-supine — acceleration along the y-axis while supine; (3) Z-RED — acceleration along the dorsoventral (z) axis with right ear down; (4) Z-supine — acceleration along the z-axis while supine. Linear acceleration in the Y-upright, Y-supine and Z-RED orientations elicited conjugate OT. The smaller response in the Z-supine orientation appeared disconjugate. The amplitude of the response decreased and the phase lag increased with increasing frequency for each orientation. This frequency dependence does not match the frequency response of the regular or irregular afferent otolith neurons; therefore the response dynamics cannot be explained by simple peripheral mechanisms. The Y-upright responses were larger than the Y-supine responses (P<0.05). This difference indicates that OT must be more complicated than a simple low-pass filtered response to interaural shear force, since the dynamic shear force along the interaural axis was identical in these two orientations. The Y-supine responses were, in turn, larger than the Z-RED responses (P<0.01). Interestingly, the vector sum of the Y-supine responses plus Z-RED responses was not significantly different (P=0.99) from the Y-upright responses. This suggests that, in this frequency range, the conjugate OT response during Y-upright stimulation might be composed of two components: (1) a response to shear force along the y-axis (as in Y-supine stimulation), and (2) a response to roll tilt of gravitoinertial force (as in Z-RED stimulation).

Spatial orientation in the squirrel monkey : an experimental and theoretical investigation

Thesis (Ph. D.)--Massachusetts Institute of Technology, Dept. of Aeronautics and Astronautics, 1990.

Spatial Orientation of VOR to Combined Vestibular Stimuli in Squirrel Monkeys

The interaction of angular and linear stimuli produces a complex alignment of spatial orientation and the VOR. This phenomenon was studied by measuring three dimensional eye movements in 6 squirrel monkeys during centrifugation in the dark. The axis of eye rotation was always aligned with gravity and with the spinal axis of the upright monkeys. The erect monkeys were oriented such that they were either facing toward the direction of motion or were facing away from the motion. Angular velocity trapezoids were utilized as the motion stimuli with a ramp acceleration of 10 degrees/s2 to a constant velocity of 200 degrees/s. This yields a final centripetal acceleration of 1 g. The orientation of centripetal acceleration dramatically altered the VOR by changing the axis of eye rotation, the peak value of slow phase eye velocity, and the time constant of per-rotary decay. The axis of eye rotation always tended to align with gravito-inertial force, the peak value of slow phase eye velocity was greater when the monkey faced the motion than when it faced away from the motion, and the time constant of decay was smaller when the monkey faced the motion than when it faced away from the motion. These findings were statistically significant (p less than 0.05) and were consistent across all monkeys. The data also indicate that the VOR may be separated into two reflexes, a linear reflex and a rotational reflex. The linear reflex decays as the axis of eye rotation aligns with gravito-inertial force (GIF). These results indicate that GIF is resolved into two components: one representing an internal estimate of linear acceleration and one representing an internal estimate of gravity.

Effect of vergence on the gain of the linear vestibulo-ocular reflex

We measured the linear vestibulo-ocular reflex (LVOR) and vergence, using binocular search coils, in 3 humans. The subjects were accelerated sinusoidally at 0.5 Hz and 0.2 g peak acceleration, in complete darkness, while performing three different tasks: i) mental arithmetic; ii) tracking a remembered target at either 0.34 m or 0.14 m distance; and iii) maintaining vergence at either of these distances by means of audio biofeedback based on vergence. Subjects could control vergence using the audio feedback; there was greater convergence with the near audio target. However, there was no significant difference in vergence between the near and far remembered target conditions. With audio feedback, the amplitude of smooth tracking was not consistently different for the near and the far conditions. However, the amplitude of tracking (saccades and smooth component) in the remembered target conditions was greater for near than for far targets. These results suggest that linear VOR amplitude is not determined by vergence alone.

Three-dimensional eye velocity measurement following postrotational tilt in the monkey

Angular head accelerations are known to elicit reflexive movements of the eye called the angular vestibuloocular reflex (VOR). If an upright subject is rotated about an earth-vertical axis a t a constant angular velocity and then decelerated after some time, horizontal postrotatory nystagmus follows. Recently a number of studies (monkey; human;* cat3) have demonstrated the existence of an exponentially decaying vertical nystagmus as well as horizontal nystagmus following rotation about a nonvertical axis. Each of these studies indicated that the vertical response, combined with the horizontal nystagmus, tended t o align the compensatory motion of the pupil with earth horizontal. Two earlier human studies reported the presence of a vertical nystagmus during cent r i fuga t i~n .~ .~ A later set of studies repeated this paradigm with monkeys and measured the extent of an axis transformation that moved the axis of eye rotation toward alignment with gravitoinertial Monkey studies have also demonstrated a shift in the axis of the optokinetic after-nystagmus ( O W ) response when the rotational axis of the stimuli did not align with gravity.8 While the authors acknowledged the presence of cross-talk between the channels and could not quantitatively show the extent to which the response deviated from yaw, these data showed the presence of position dependent vertical or torsional responses which shifted the axis of the eye movement responses toward a spatial-vertical axis. We have measured all three dimensions of eye rotation during and following vestibular stimulation. We also have developed and implemented a n algorithm that allows us to minimize the cross-talk between the eye measurement channels and permits us to evaluate the change in the axis of eye rotation quantitatively.

Vergence can be controlled by audio feedback, and induces downward ocular deviation

We measured horizontal and vertical eye positions, using binocular search coils, in three humans. Subjects could maintain vergence by means of audio biofeedback. Feedback consisted of a pair of audio tones, one variable and one fixed at a reference frequency. The variable tone was controlled by instantaneous vergence and provided immediate feedback on the vergence state. The reference frequency, which they attempted to match, was set to correspond to a target distance of either 0.34 m or 0.14 m. Subjects could maintain vergence consistently, even while undergoing lateral motions at 0.5 Hz and 0.2 g peak acceleration in darkness. There was also a consistent tendency for the eyes to deviate downward during near vergence. The results may be useful in experiments in which one wishes to control vergence without providing a visual reference which might inhibit conjugate eye movements.