Frontal eye field efferents in the macaque monkey: I. Subcortical pathways and topography of striatal and thalamic terminal fields

Abstract

Anterograde tracers (tritiated leucine, proline, fucose; WGA‐HRP) were injected into sites within the frontal eye fields (FEF) of nine macaque monkeys. Low thresholds (≤50 μA) for electrically evoking saccadic eye movements were used to locate injection sites in four monkeys. Cases were grouped according to the amplitude of saccades evoked or predicted at the injection site. Dorsomedial prearcuate injection sites where large saccades were elicited were classified as lFEF cases, whereas ventrolateral prearcuate sites where small saccades were evoked were designated sFEF cases. One control case was injected in the medial postarcuate area 6. We found five descending fiber bundles from FEF; fibers to the striatum, which enter the caudate nucleus at or just rostral to the genu of the internal capsule; fibers to the claustrum, which travel in the external capsule; and transthalamic, subthalamic, and pedunculopontine fibers. Our results indicate that transthalamic and subthalamic pathways supply all terminal sites in the thalamus, subthalamus, and tegmentum of the midbrain and pons, whereas pedunculopontine fibers appear to terminate in the pontine and reticularis tegmenti pontis nucleus exclusively. Frontal eye field terminal fields in the striatum were topographically organized: lFEF projections terminated dorsal and rostral to sFEF projections. Thus, lFEF terminal fields were located centrally in the head and body of the caudate nucleus and a small dorsomedial portion of the putamen, whereas sFEF terminal fields were located in ventrolateral parts of the caudate body and ventromedial parts of the putamen. In the claustrum, lFEF projections terminated dorsal and rostral to sFEF projections. Projections from FEF terminated in ventral and caudal parts of the subthalamic nucleus without a clear topography. By comparison, terminal fields from medial postarcuate area 6 were located more caudally and laterally in the striatum and claustrum than projections from FEF, and more centrally in the subthalamic nucleus. In the thalamus, FEF terminal patches in some thalamic nuclei were also topographically organized. Projections from lFEF terminated in dorsal area X, dorsolateral medial dorsal nucleus, pars parvicellularis (MDpc), and the caudal pole of MDpc, whereas projections from sFEF terminated in ventral area X, medial dorsal nucleus, pars multiformis, and caudal medial dorsal nucleus pars densocellularis. Characteristically, projections from postarcuate area 6 terminated in central ventral lateral nucleus, pars caudalis, ventral posterior lateral nucleus, pars oralis. Projections from dorsomedial postarcuate area 6 terminated in the paracentral and central lateral nuclei.