Three-dimensional organization of otolith-ocular reflexes in rhesus monkeys
I. Linear acceleration responses during off-vertical axis rotation.
ANGELAKI, DORA E. AND BERNHARD J. M. HESS.
Dept. of Surgery (Otolaryngology), University of Mississippi Medical
Center, Jackson MS, Dept. of Neurology, University Hospital Zürich, CH-8091,
APStracts 2:0007N, 1996.
SUMMARY AND CONCLUSIONS
1. The dynamic properties of otolith-ocular reflexes elicited by sinusoidal
linear acceleration along the three cardinal head axes were studied during
off-vertical axis rotations in rhesus monkeys. As the head rotates in space at
constant velocity about an off-vertical axis, otolith-ocular reflexes are
elicited in response to the sinusoidally varying linear acceleration (gravity)
components along the interaural, nasooccipital or vertical head axis. Since
the frequency of these sinusoidal stimuli is proportional to the velocity of
rotation, rotation at low and moderately fast speeds allows the study of the
mid and low frequency dynamics of these otolith-ocular reflexes. 2. Animals
were rotated in complete darkness in the yaw, pitch and roll planes at
velocities ranging between 7.4(/s and 184(/s. Accordingly, otolith-ocular
reflexes (manifested as sinusoidal modulations in eye position and/or slow
phase eye velocity) were quantitatively studied for stimulus frequencies
ranging between 0.02 Hz and 0.51 Hz. During yaw and roll rotation, torsional,
vertical and horizontal slow phase eye velocity was sinusoidally modulated as
a function of head position. The amplitudes of these responses were symmetric
for rotations in opposite directions. In contrast, mainly vertical slow phase
eye velocity was modulated during pitch rotation. This modulation was
asymmetric for opposite direction rotations. 3. Each of these response
components in a given rotation plane could be associated with an otolith-
ocular response vector whose sensitivity, temporal phase and spatial
orientation were estimated based on the amplitude and phase of sinusoidal
modulations during both directions of rotation. Based on this analysis which
was performed either for slow phase eye velocity alone or for total eye
excursion (including both slow and fast eye movements), two distinct response
patterns were observed: (a) Response vectors with pronounced dynamics and
spatial/temporal properties that could be characterized as the low frequency
range of "translational" otolith-ocular reflexes. (b) Response vectors
associated with an eye position modulation in phase with head position ("tilt"
otolith-ocular reflexes). 4. The responses associated with two otolith-ocular
vectors with pronounced dynamics consisted of horizontal eye movements evoked
as a function of gravity along the interaural axis and vertical eye movements
elicited as a function of gravity along the vertical head axis. Both responses
were characterized by a slow phase eye velocity sensitivity that increased
three-to five-fold and large phase changes of approximately 100-180( between
0.02 Hz and 0.51 Hz. These dynamic properties could suggest non-traditional
temporal processing in utriculo-ocular and sacculo-ocular pathways, possibly
involving spatio-temporal otolith-ocular interactions. 5. The two otolith-
ocular vectors associated with eye position responses in phase with head
position ("tilt" otolith-ocular reflexes) consisted of torsional eye movements
in response to gravity along the interaural axis, and vertical eye movements
in response to gravity along the nasooccipital head axis. These otolith-ocular
responses did not result from an otolithic effect on slow eye movements alone.
Particularly at high frequencies (i.e., high speed rotations), saccades were
responsible for most of the modulation of torsional and vertical eye position
which was relatively large (on average ( 8-10(/g) and remained independent of
frequency. This reflex dynamics can be simulated by a direct coupling of
primary otolith afferent inputs to the oculomotor plant. Despite the large
modulation of torsional and vertical eye position due to both fast and slow
eye movements, modulation of slow phase eye velocity was small for all
frequencies (on average ( 4-10 (/s/g). 6. These results suggest that torsional
and vertical responses (previously described as "counter-rolling" and
"counter-pitching" or "tilt" otolith-ocular reflexes) represent an otolithic
effect on both fast and slow eye movement components of the primate oculomotor
system. The combined otolithic effect on both fast and slow eye movements
possibly reflects a dynamic dependence of oculomotor (i.e., Listing's)
coordinates on head orientation in space, suggesting a function that is
probably related to spatial orientation and motor coordination rather than
Received 4 April 1995; accepted in final form 28 December 1995.
APS Manuscript Number J301-5.
Article publication pending J. Neurophysiol.
ISSN 1080-4757 Copyright 1996 The American Physiological Society.
Published in APStracts on 22 January 96