Conjugate oscillations of the eyes at frequencies exceeding 10 Hz
are generally thought to be saccadic in origin.
8 9 Their
presence during vergence movements was an unexpected finding. Although
records of eye acceleration are prone to noise, the magnitude of these
oscillations in each subject was much greater than when the eyes were
still, and they did not occur with conjugate saccades
(Fig. 2D) .
Furthermore, the same oscillations were often detectable in our
position records and appear on some published figures of combined
saccadic–vergence movements from other
laboratories.
1 13 17 In one such study, occasional
horizontal, conjugate oscillations were noted when a vertical saccade
was combined with a horizontal vergence movement
17 ; this
is similar to our midsagittal and vertical paradigm. Our observations
indicate that horizontal conjugate oscillations occur whenever a shift
in the fixation point requires a substantial vergence component in
addition to a saccade. Thus, the highest incidence in our study
occurred during the Müller paradigm, in which no saccade was
required (although a disjunctive one invariably occurred) and most of
the shift of the point of fixation was achieved by a vergence movement.
Because almost all vergence movements are accompanied by a
saccade,
1 any large change in the vergence angle might be
expected to induce these conjugate oscillations. This is an issue
deserving of further study.
The presence of these conjugate oscillations suggests that the saccadic
system is still active (i.e., the omnipause neurons are silent) during
the vergence movement that follows the saccade. Current models of
saccade generation suggest that if the omnipause neurons are not
inhibiting burst neurons and a motor command is no longer provided to
the burst neurons, then small saccadic oscillations will
occur.
8 This occurs, for example during oblique saccades
if the vertical component is pathologically slow; horizontal
oscillations occur during the completion of the vertical
component.
18 The oscillations shown by our subjects also
support the hypothesis that both saccades and vergence burst neurons
are gated by omnipause neurons.
18 The latter idea has
received electrophysiological support from the demonstration that
microstimulation of omnipause neurons slows ongoing vergence
movements.
11 Thus, one interpretation of the present
findings is that omnipause neurons become silent whenever the motor
error (difference between desired change in eye position and the
current eye position) calls for a conjugate gaze shift above a minimum
threshold. The inhibition of omnipause neurons allows for the
generation of a saccadic eye movement, but the firing of these neurons
does not resume until the global motor error (combined version and
vergence errors) declines below a threshold level. If the version error
is reduced below threshold before the vergence error, then the
omnipause neurons are still silent, and saccadic oscillations may be
produced by discharge of burst neurons.
Although our subjects showed conjugate oscillations during most of the
vergence movements that followed saccades, oscillations were usually
absent for the vergence movement made before the saccadic movement.
Thus, it appears that the initial vergence movement that preceded the
saccade did not require that the omnipause neurons cease discharge. Our
subjects made self-paced gaze shifts, and it is possible that the
initial vergence movements were anticipatory in nature, similar to the
conjugate drifts of the eyes that precede saccades made in response to
predictable target jumps.
19 The dynamic properties of
these initial vergence movements suggests that they may not depend on
vergence burst neurons.
Some normal subjects are able to induce a “voluntary” nystagmus,
which consists of high-frequency saccadic
oscillations.
20 21 Interestingly, such people commonly use
a voluntary vergence effort as a strategy to induce their saccadic
oscillations. Our observations suggest that most people unwittingly
show development of saccadic oscillations during combined
saccadic–vergence movements—a marker of the common pontine switch
that enables us to make such gaze shifts. The ability to induce
saccadic oscillations experimentally provides a new tool to test
current models for saccade generation.
The authors are grateful to David S. Zee for his critical comments.