Frontal eye field efferents in the macaque monkey: II. Topography of terminal fields in midbrain and pons

Abstract

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)

Monkey Dorsolateral Prefrontal Cortex Sends Task-Selective Signals Directly to the Superior Colliculus

“…It is therefore tempting to speculate that the output neurons of the dorsolateral PFC project predominately to the rostral SC. However, the fact that axons enter the colliculus via the rostral pole (Stanton et al, 1988) renders it impossible to determine the exact collicular site to which the DLPFC neurons we recorded projected. Thus, we feel that we cannot confidently distinguish whether DLPFC axons projected to fixation or saccade neurons and therefore suggest that both possibilities described above are equally likely based on our data.…”

Oculomotor Areas of the Primate Frontal Lobes: A Transneuronal Transfer of Rabies Virus and [14C]-2-Deoxyglucose Functional Imaging Study

“…In both cases, labeling was bilateral (Fig. 4D-H al., 1986; Stanton et al, 1988;Shook et al, 1990), and the primarily bilateral transneuronal labeling of the latter after unilateral rabies virus injections in the LR muscle (Grantyn et al, 2002).…”

“…Several of these nuclei are known to receive direct projections from the cortical areas containing labeled neurons. For example, the anterior bank of the AS projects to the MRF, SGI, NPH, Soc, NRTP, PPRF, NIC, and rip (Schnyder et al, 1985;Huerta et al, 1986;Stanton et al, 1988;Shook et al, 1990). Taking into consideration previous descriptions regarding the relative strength of these projections and the time course of labeling in cortical and subcortical structures in our experiments, the more likely sources of the labeling in the anterior bank of the AS are the Soc, PPRF, NRTP, and MRF at 3 d postinoculation (LR2) and the SGI at 3.5 d postinoculation (LR4).…”

Modulation of Presaccadic Activity in the Frontal Eye Field by the Superior Colliculus

“…In the context of that experiment, a simple explanation is that the presaccadic activity in the FEF neuron increased to counterbalance the impairment of the corresponding spatial representation in SC. The increase in FEF activity could have a compensatory effect via its direct projections to oculomotor regions of the pons (Huerta et al 1986;Leichnetz et al 1984;Segraves and Goldberg 1987;Stanton et al 1988b).…”