SEMICIRCULAR CANAL CONTRIBUTIONS TO THE THREE-DIMENSIONAL VESTIBULO-OCULAR
REFLEX: A MODEL-BASED APPROACH.
Yakushin, Sergei, Mingjia Dai, Jun-Ichi Suzuki, Theodore Raphan and Bernard
Cohen.
Departments of Neurology and Physiology and Biophysics, Mount Sinai School
of Medicine, New York, New York, 10029 USA, the Department of Otolaryngology,
Teikyo University, Tokyo, Japan, the Departments of Computer and Information
Science and Experimental Psychology, Brooklyn College, Brooklyn, New York
11210.
APStracts 2:0203N, 1995.
SUMMARY AND CONCLUSIONS
We studied the contribution of the individual semicircular canals to the
generation of horizontal and torsional eye movements in cynomolgus monkeys.
Eye movements were elicited by sinusoidal rotation about a vertical
(gravitational) axis with the animals tilted in various attitudes of static
forward or backward pitch. The gains of the horizontal and torsional
components of the vestibulo-ocular reflex (VOR) were measured for each tilt
position. The gains as a function of tilt position were fit with sinusoidal
functions, and spatial gains and phases were determined. After recording
control responses, the semicircular canals were plugged, animals were allowed
to adapt and the test procedure was repeated. Animals were prepared with only
the anterior and posterior canals intact (vertical canal ( VC ) animals), only
the lateral canals intact (lateral canal ( LC ) animal) and only one anterior
and the contralateral posterior canals intact (right anterior and left
posterior canal ( RALP ) animals; left anterior and right posterior canal (
LARP ) animals). In normal animals, the gain of the horizontal (yaw axis)
velocity of the compensatory movements decreased as they were pitched forward
or backward, and a torsional velocity appeared, reversing phase at the peak of
the horizontal gain. After the anterior and posterior canals were plugged ( LC
animal), the horizontal component was reduced when the animal was tilted
backward; the gain was zero with about -60 degrees backward tilt. The spatial
phase of the torsional component had the same characteristics. This is
consistent with the fact that both responses are produced by the lateral
canals which from our results are tilted between 28 degrees and 39 degrees
above the horizontal stereotaxic plane. After both lateral canals were plugged
( VC animals), horizontal velocity was reduced in the upright position but
increased as the animals were pitched backward relative to the axis of
rotation. Torsional velocities, which were zero in the upright position in the
normal animal, were now 180 degrees out of phase with the horizontal velocity.
The peak values of the horizontal and torsional components were significantly
shifted from the normal data and were closely aligned with each other,
reaching a peak value at approximately -56 degrees pitched back (-53 degrees
horizontal, -58 degrees torsional). The same was true for the LARP and RALP
animals; the peak values were at -59 degrees pitched back (-55 degrees
horizontal, -62 degrees torsional). Likewise, in the LC animal, the peak yaw
and roll gains occurred at about the same angle of forward tilt, 35 degrees
(30 degrees horizontal, 39 degrees torsional). Thus, in each case, the canal
plugging had transformed the VOR from a compensatory to a direction-fixed
response with regard to the head. Thus, there was no adaptation of the
response planes of the individual canals after plugging. The data were
compared to eye velocity predictions of a model based on the geometric
organization of the canals and their relation to a head coordinate frame. The
model used the normal to the canal planes to form a non-orthogonal coordinate
basis for representing eye velocity. An analysis of variance was used to
define the goodness of fit of model predictions to the data. Model predictions
and experimental data agreed closely for both normal animals and for the
animals after canal lesions. Moreover, if horizontal and roll components from
the LC and VC animals were combined, the summation overlay the response of the
normal monkeys and the predictions of the model. In addition, a combination of
the RALP and LARP animals predicted the response of the lateral canal plugged
( VC ) animals. When the operated animals were tested in light, the gains,
peak values and spatial phases of horizontal and roll eye velocity returned to
the preoperative values, regardless of the type of surgery performed. This
indicates that vision had compensated for the lack of spatial adaptation of
the response planes after plugging. It converted a non-compensatory,
direction-fixed response with regard to the head to an appropriate
compensatory response. These results indicate that both the vertical and
lateral canals contribute a horizontal and torsional component to the
vestibulo-ocular reflex (VOR) in the monkey according to the vector projection
of head velocity onto the normals of the individual canals. The individual
components can be predicted according to the position of the canals in the
head with regard to the plane of rotation. The non-orthogonality of the canal
planes must be considered when predicting canal activation of eye movements in
response to rotation around any axis.
Received 29 March 1995; accepted in final form 12 July 1995.
APS Manuscript Number J205-5.
Article publication pending J. Neurophysiol.
ISSN 1080-4757 Copyright 1995 The American Physiological Society.
Published in APStracts on 30 July 1995.