Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys: I. Subcortical connections.

Intracortical microstimulation was used to define the borders of the frontal eye fields in squirrel, owl, and macaque monkeys. The borders were marked with electrolytic lesions, and horseradish peroxidase conjugated to wheat germ agglutinin was injected within the field. Following tetramethyl benzidine histochemistry, afferent and efferent connections of the frontal eye field with subcortical structures were studied. Most connections were ipsilateral and were similar in all primates studied. These include reciprocal connections with the following nuclei: medial dorsal (lateral parts), ventral anterior (especially with pars magnocellularis), central lateral, paracentral, ventral lateral, parafascicular, medial pulvinar, limitans, and suprageniculate. The frontal eye field also projects to the ipsilateral pretectal nuclei, subthalamic nucleus, nucleus of the posterior commissure, superior colliculus (especially layer four), zona incerta, rostral interstitial nucleus of the medial longitudinal fasciculus, nucleus Darkschewitsch, dorsomedial parvocellular red nucleus, interstitial nucleus of Cajal, basilar pontine nuclei, and bilaterally to the paramedian pontine reticular formation and the nucleus reticularis tegmenti pontis. Many of these structures also receive input from deeper layers of the superior colliculus and are known to participate in visuomotor function. These results reveal connections that account for the parallel influence of the superior colliculus and the frontal eye field on visuomotor function; suggest that there has been little evolutionary change in subcortical connections, and therefore function, of the frontal eye fields since the time that these lines of primates diverged; and support the conclusion that the frontal eye fields are homologous in New and Old World monkeys.