Downward gaze in monkeys: stimulation and lesion studies

Ten monkeys were stimulated unilaterally and bilaterally through bipolar electrodes placed stereotactically on each side of the midline under light barbiturate anaesthesia. Bilateral simultaneous stimulation elicited straight downward binocular movements from a core of tissue about 40 mm3 on each side which included the fields of Forel, zona incerta, subthalamic nucleus, oral pole of the red nucleus, fasciculus retroflexus and 'area tegmentalis'. Unilateral stimulation of the same points yielded downward eye movements in only 25 per cent of the instances. Upward deviation of the globes could be elicited by bilateral stimulation of tissue located more caudal, ventral and medial than that from which downward movements were obtained. Bilateral electrolytic lesions within the region outlined above caused significant defects in downward gaze both in saccadic and slow pursuit binocular movements. Passive bending of the head backwards, however, resulted in downward deviation of the globes (oculocephalic reflex). Optokinetic nystagmus and after-nystagmus downward were abolished. Oblique (45 degrees) optokinetic stimulation elicited a perverted response in the horizontal plane. Vestibulo-ocular reflexes elicited by bilateral warm irrigation of both ear canals with the monkey in the erect position, or by turning the animal while lying on one side, caused a strong tonic deviation upward with absence of nystagmus downward. Some of these monkeys showed additional alterations in upward gaze but they were less severe in intensity and duration than those of downward gaze. All eye deviations in the horizontal plane were consistently normal. Recovery occurred in all types of vertical binocular movements except in the rapid motions (saccades and quick phases of nystagmus) below the horizontal meridian. A unilateral lesion had no effect. The minimal damage producing downward gaze defects was about 1.7 mm in diameter, cetred in the prerubral fields, rostral and medial to the red nuclei with minimal involvement of the oral pole of these structures. The nuclei of Cajal, Darkschewitsch and interstitialis of the posterior commissure, as well as the fasciculus retroflexus and the posterior commissure, were spared by this lesion. The so-called rostral interstitial nucleus of the medial longitudinal fasciculus and the nucleus campi Foreli appear to be destroyed. These structures are known to receive an input from the paramedian pontine reticular formation and project on to the oculomotor nerve nucleus. These results demonstrate that the prerubral fields contain structures which are critical for rapid eye movements downward, and therefore an isolated downward gaze palsy is a strong indicator of a bilateral lesion of this zone. The findings in the few reported cases with this sign and available pathological analysis suggest that our conclusions from the experimental monkey apply to man as well. The concept of bilateral innervation for vertical eye movements is amply confirmed for the downward vectors...