We studied single neurons in the frontal eye fields of awake macaque monkeys and compared their activity with the saccadic eye movements elicited by microstimulation at the sites of these neurons. Saccades could be elicited from electrical stimulation in the cortical gray matter of the frontal eye fields with currents as small as 10 microA. Low thresholds for eliciting saccades were found at the sites of cells with presaccadic activity. Presaccadic neurons classified as visuomovement or movement were most associated with low (less than 50 microA) thresholds. High thresholds (greater than 100 microA) or no elicited saccades were associated with other classes of frontal eye field neurons, including neurons responding only after saccades and presaccadic neurons, classified as purely visual. Throughout the frontal eye fields, the optimal saccade for eliciting presaccadic neural activity at a given recording site predicted both the direction and amplitude of the saccades that were evoked by microstimulation at that site. In contrast, the movement fields of postsaccadic cells were usually different from the saccades evoked by stimulation at the sites of such cells. We defined the low-threshold frontal eye fields as cortex yielding saccades with stimulation currents less than or equal to 50 microA. It lies along the posterior portion of the arcuate sulcus and is largely contained in the anterior bank of that sulcus. It is smaller than Brodmann's area 8 but corresponds with the union of Walker's cytoarchitectonic areas 8A and 45. Saccade amplitude was topographically organized across the frontal eye fields. Amplitudes of elicited saccades ranged from less than 1 degree to greater than 30 degrees. Smaller saccades were evoked from the ventrolateral portion, and larger saccades were evoked from the dorsomedial portion. Within the arcuate sulcus, evoked saccades were usually larger near the lip and smaller near the fundus. Saccade direction had no global organization across the frontal eye fields; however, saccade direction changed in systematic progressions with small advances of the microelectrode, and all contralateral saccadic directions were often represented in a single electrode penetration down the bank of the arcuate sulcus. Furthermore, the direction of change in these progressions periodically reversed, allowing particular saccade directions to be multiply represented in nearby regions of cortex.(ABSTRACT TRUNCATED AT 400 WORDS)

Frontal eye field (FEF) projections to posterior cortical areas were mapped by autoradiography of tritiated amino acids (Leu, Pro) in six macaque monkeys. In three monkeys, the large saccade part of the FEF (IFEF) was identified by microstimulation and injected with tracers. In a fourth monkey, the small saccade part of the FEF (sFEF) was identified by microstimulation and injected with tracer. Tracer injections were placed into the sFEF region of two other monkeys using anatomical landmarks. The IFEF and sFEF generally had distinct and largely segregated projections to posterior cortical areas, and the overall pattern of labeling in visual areas with established topology indicates that IFEF neurons preferentially project to areas having large and eccentric receptive fields, whereas sFEF neurons project to areas having smaller, more centrally located fields. The terminal fields from the sFEF were more widespread than those from IFEF. Projections from sFEF terminated in the lateral intraparietal area (LIP), the ventral intraparietal area (VIP), and the parietal part of visual area V3A, in the fundus of the superior temporal visual area (FST), the middle temporal area (MT), the medial superior temporal area (MST), the temporal part of visual area V4, the inferior temporal area (IT), and the temporal-occipital area (TEO) and in occipital visual areas V2, V3, and V4. Projections from IFEF terminated in parietal areas 7a, LIP, and VIP and the medial part of parietal area PE; in temporal areas MST and the superior temporal polysensory area (STP); and in occipital area V2 and posterior cingulate area 23b. Projections from IFEF and sFEF appeared to terminate in different parts of common target areas in MST, LIP, and V2. The topography of IFEF and sFEF projections to LIP suggests that this posterior eye field may also be organized by saccade amplitude. Most terminal labeling from FEF injections was bilaminar to layers I and V/VI, but labeling in area LIP, area MT, the medial part of area PE, and area 23b was columnar-form to all layers.

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Frontal eye field (FEF) projections to the midbrain and pons were studied in nine macaque monkeys that were used to study FEF projections to the striatum and thalamus (Stanton et al.: J. Comp. Neurol. 271:473-492, '88). Injections of tritiated amino acids or WGA-HRP were made into FEF cortical locations where low-level microstimulation (less than or equal to 50 microA) elicited saccadic eye movements, and anterograde axonal labeling was mapped. The injections were made into the anterior bank of the arcuate sulcus from dorsomedial sites where large saccades were evoked (lFEF) to ventrolateral sites where small saccades were evoked (sFEF). The largest terminal fields of FEF fibers were located in the ipsilateral superior colliculus (SC). Projections to SC were topographically organized: lFEF sites projected to intermediate and deep layers of caudal SC, sFEF sites projected to intermediate and superficial layers of rostral SC, and FEF sites between these extremes projected to intermediate locations in SC. Patches of terminal labeling were located ipsilaterally in the lateral mesencephalic reticular formation near the parabigeminal nucleus and the ventrolateral pontine reticular formation. These patches were larger from lFEF injections. Small, dense terminal patches were seen in the ipsilateral pontine gray, mostly along the medial and dorsal borders of these nuclei but occasionally in central and dorsolateral regions. Patches of label like those in the pontine nuclei were located ipsilaterally in the reticularis tegmenti pontis nucleus in lFEF cases and bilaterally in sFEF cases. Small terminal patches were found in the nucleus of Darkschewitsch and dorsal and medial parts of the parvicellular red nucleus in most FEF cases. In the pretectal region, labeled terminal patches were consistently found in the nucleus limitans of the posterior thalamus, but we could not determine if label in the nucleus of the pretectal area and dorsal parts of the nucleus of the posterior commissure marked axon terminals or fibers of passage. We found small, lightly labeled terminal patches in the pontine raphe between the rootlets of the abducens nerve (three cases) or in the adjacent paramedian pontine reticular formation (one case). Omnipauser cells in this region are important in initiating saccades. In one sFEF case, very small patches of label were located in the supragenual nuclei anterior to the abducens nuclei and in the ipsilateral nucleus prepositus hypoglossi posterior to the abducens nucleus. Presaccadic burster neurons in the periabducens region are known to fire immediately before horizontal saccades.(ABSTRACT TRUNCATED AT 400 WORDS)