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J Neurophysiol 57: 1383-1409, 1987;
0022-3077/87 $5.00
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Journal of Neurophysiology, Vol 57, Issue 5 1383-1409, Copyright © 1987 by APS

ARTICLES

Loss of the neural integrator of the oculomotor system from brain stem lesions in monkey

S. C. Cannon and D. A. Robinson

Eye movement were recorded from four juvenile rhesus monkeys (Macaca mulatta) before and after the injection of neurotoxins (kainate or ibotenate) in the region of the medial vestibular and prepositus hypoglossi nuclei, an area hypothesized to be the locus of the neural integrator for horizontal eye movement commands. Eye movements were measured in the head-restrained animal by the magnetic field/eye-coil method. The monkeys were trained to follow visual targets. A chamber implanted over a trephine hole in the skull permitted recordings to be made in the brain stem with metal microelectrodes. The abducens nuclei were located and used as a reference point for subsequent neurotoxin injections through cannulas. The effects of these lesions on fixation, vestibuloocular and optokinetic responses, and smooth pursuit were compared with predicted oculomotor anomalies caused by a loss of the neural integrator. Kainate and ibotenate did not create permanent lesions in this region of the brain stem. All the eye movements returned toward normal over the course of a few days to 2 wk. Histological examination revealed that the cannula tips were mainly located between the vestibular and prepositus hypoglossi nuclei, in their rostral 2 mm, bordered rostrally by the abducens nuclei. Dense gliosis clearly demarcated the cannula tracks, but for most injections there were no surrounding regions of neuronal loss. Thus the eye movement disorders were due to a reversible, not a permanent, lesion. The time constant for the neural integrator was determined from the velocity of the centripetal drift of the eyes just after an eccentric saccade in total darkness. For intact animals this time constant was greater than 20 s. Shortly after bilateral injections of neurotoxin, the time constant began to decrease and reached a minimum of 200 ms; every horizontal saccade was followed by a rapid centripetal drift with a time constant of approximately 200 ms. For vertical eye movements, in this acute phase, the time constant was approximately 2.5 s. The vestibuloocular reflex (VOR) was drastically changed by the lesions. A step of constant head velocity in total darkness evoked a step change in eye position rather than in velocity. In the absence of the neural integrator, the step velocity command from the canal afferents was not integrated to produce a ramp of eye position (normal slow phases); rather this signal was relayed directly to the motoneurons and caused a step in eye position. The per- and postrotatory decay of the head velocity signal was decreased to 5-6 s indicating that vestibular velocity storage was also impaired.(ABSTRACT TRUNCATED AT 400 WORDS)


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