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

Abstract

We used the [14 C]-2-deoxyglucose method to study the location and extent of primate frontal lobe areas activated for saccades and fixation and the retrograde transneuronal transfer of rabies virus to determine whether these regions are oligosynaptically connected with extraocular motoneurons. Fixation-related increases of local cerebral glucose utilization (LCGU) values were found around the fundus of the inferior limb of the arcuate sulcus (AS) just ventral to its genu, in the dorsomedial frontal cortex (DMFC), cingulate cortex, and orbitofrontal cortex. Significant increases of LCGU values were found in and around both banks of the AS, DMFC, and caudal principal, cingulate, and orbitofrontal cortices of monkeys executing visually guided saccades. All of these areas are oligosynaptically connected to extraocular motoneurons, as shown by the presence of retrogradely transneuronally labeled cells after injection of rabies virus in the lateral rectus muscle. Our data demonstrate that the arcuate oculomotor cortex occupies a region considerably larger than the classic, electrical stimulation-defined, frontal eye field. Besides a large part of the anterior bank of the AS, it includes the caudal prearcuate convexity and part of the premotor cortex in the posterior bank of the AS. They also demonstrate that the oculomotor DMFC occupies a small area straddling the ridge of the brain medial to the superior ramus of the AS. Our results support the notion that a network of several interconnected frontal lobe regions is activated during rapid, visually guided eye movements and that their output is conveyed in parallel to subcortical structures projecting to extraocular motoneurons.

Saccade-Related Information in the Superior Temporal Motion Complex: Quantitative Functional Mapping in the Monkey

“…1 B). The enhancement of glucose consumption (range, 14 -22% higher than the fixation control) was comparable to that induced by visually guided saccades in the SC, FEF, and LIP (range, 12-31%) and higher than that induced in the SEF (4 -11%) (Moschovakis et al, 2001(Moschovakis et al, , 2004Bakola et al, 2006). The V5/MT activation included its ventralmost posterior part, which corresponds to area MT-foveal (MTf) and represents central vision (Gattass and Gross, 1981).…”

“…In all tasks, parameters were chosen so that the total number of the stimulus-triggered saccades would be approximately equal. The saccades that brought the eyes back to the fixation point and the distribution of end points of all eye movements executed by the six monkeys have been presented previously (Moschovakis et al, 2004;Bakola et al, 2006). 14 C-DG procedure.…”

Performance Monitoring Local Field Potentials in the Medial Frontal Cortex of Primates: Anterior Cingulate Cortex

“…In doing so, though, it is critical to recognize that anatomical tracer studies have not been performed that restrict tracer injections to this portion of area 24c. Granting this, signals in the ACC can influence the ocular motor system because the rostral cingulate cortex of monkeys is oligosynaptically connected to extraocular motoneurons (Moschovakis et al 2004). The ACC is only weakly connected with the FEF (Barbas and Mesulam 1981;Huerta and Kaas 1990;Stanton et al 1993;Van Hoesen et al 1993; and does not project to the SC (Fries 1983).…”

“…First, the error-monitoring hypothesis proposes that the ERN/Ne reflects a comparison between the representations of the overt error response and the correct response (Falkenstein et al 1991;Gehring et al 1993), a function comparable to other midline negativities signaling mismatch (Näätänen et al 1978) and the N400 (Kutas and Hillyard 1984). However, the presence of frontocentral negativities during correct trials, albeit of smaller amplitude (e.g., Falkenstein et al 2000;Vidal et al 2000) is difficult for the error-monitoring hypothesis to account for (Coles et al 2001).…”

The Place Code of Saccade Metrics in the Lateral Bank of the Intraparietal Sulcus

“…For example, the frontal eye field (FEF) encodes saccade size in terms of the location of the active population within a small (ϳ6-mm-long) region of the anterior bank of the arcuate sulcus (As); small saccades are represented laterally and ventrally toward its inferior limb, whereas large saccades are represented medially and dorsally toward its superior limb (Sommer and Wurtz, 2000). However, no topographic map of direction has been found in this portion of the FEF; nor is there any information about the spatial representation of movement variables within the much bigger area in the posterior bank of the As that also houses the FEF (Moschovakis et al, 2004).…”