Ocular oscillations generated by coupling of brainstem excitatory and inhibitory saccadic burst neurons

Abstract The human saccadic system is potentially
unstable and may oscillate if the burst neurons, which
generate saccades, are not inhibited by omnipause
neurons. A previous study showed that combined saccade
vergence movements can evoke oscillations in normal
subjects. We set out to determine: 1) whether similar
oscillations can be recorded during other paradigms
associated with inhibition of omnipause neurons; 2)
whether lesions of the fastigial nuclei disrupt such
oscillations; and 3) whether such oscillations can be
reproduced using a model based on the coupling of
excitatory and inhibitory burst neurons. We recorded
saccadic oscillations during vergence movements, combined
saccade-vergence movements, vertical saccades,
pure vergence and blinks in three normal subjects, and in a
patient with saccadic hypermetria due to a surgical lesion
affecting both fastigial nuclei. During combined saccadevergence,
normal subjects and the cerebellar patient
developed small-amplitude (0.1–0.5°), high-frequency
(27–35 Hz), conjugate horizontal saccadic oscillations.
Oscillations of a similar amplitude and frequency occurred
during blinks, pure vergence and vertical saccades. One
normal subject could generate saccadic oscillations
voluntarily (~0.7° amplitude, 25 Hz) during sustained
convergence. Previous models proposed that high-frequency
eye oscillations produced by the saccadic system
(saccadic oscillations), occur because of a delay in a
negative feedback loop around high-gain, excitatory burst
neurons in the brainstem. The feedback included the
cerebellar fastigial nuclei. We propose another model that
accounts for saccadic oscillations based on 1) coupling of
excitatory and inhibitory burst neurons in the brainstem
and 2) the hypothesis that burst neurons show postinhibitory
rebound discharge. When omnipause neurons
are inhibited (as during saccades, saccade-vergence movements
and blinks), this new model simulates oscillations
with amplitudes and frequencies comparable to those in
normal human subjects. The finding of saccadic oscillations
in the cerebellar patient is compatible with the new
model but not with the recent models including the
fastigial nuclei in the classic negative-feedback loop
model. Our model proposes a novel mechanism for
generating oscillations in the oculomotor system and
perhaps in other motor systems too.