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The Journal of Neuroscience, June 23, 2004, 24(25):5726-5740; doi:10.1523/JNEUROSCI.1223-04.2004

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

A. K. Moschovakis,¹ G. G. Gregoriou,¹ G. Ugolini,² M. Doldan,² W. Graf,³ W. Guldin,⁴ K. Hadjidimitrakis,¹ and H. E. Savaki¹

¹Institute of Applied and Computational Mathematics, Foundation for Research and Technology-Hellas, and Department of Basic Sciences, Faculty of Medicine, School of Health Sciences, University of Crete, Heraklion 71003, Crete, Greece, ²Laboratory de Neurobiologie Cellulaire et Moléculaire, Centre National de la Recherche Scientifique, 91198 Gif-sur-Yvette, France, ³Laboratory de Physiologie de la Perception et Action, Centre National de la Recherche Scientifique-Collège de France, 75005 Paris, France, and ⁴Department of Psychology, University of Landau, 76829 Landau, Germany

We used the [¹⁴C]-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.

Key words: saccades; frontal eye field; supplementary eye field; principal sulcus; cingulate eye fields; oculomotor

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Received Dec 22, 2003; revised May 6, 2004; accepted May 9, 2004.

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