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Cortical afferents to the smooth-pursuit region of the macaque monkey’s frontal eye field

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Abstract

In primates, the frontal eye field (FEF) contains separate representations of saccadic and smooth-pursuit eye movements. The smooth-pursuit region (FEFsem) in macaque monkeys lies principally in the fundus and deep posterior wall of the arcuate sulcus, between the FEF saccade region (FEFsac) in the anterior wall and somatomotor areas on the posterior wall and convexity. In this study, cortical afferents to FEFsem were mapped by injecting retrograde tracers (WGA-HRP and fast blue) into electrophysiologically identified FEFsem sites in two monkeys. In the frontal lobe, labeled neurons were found mostly on the ipsilateral side in the (1) supplementary eye field region and lateral area F7; (2) area F2 along the superior limb of the arcuate sulcus; and (3) in the buried cortex of the arcuate sulcus extending along the superior and inferior limbs and including FEFsac and adjacent areas 8, 45, and PMv. Labeled cells were also found in the caudal periprincipal cortex (area 46) in one monkey. Labeled cells were found bilaterally in the frontal lobe in the deep posterior walls of the arcuate sulcus and postarcuate spurs and in cingulate motor areas 24 and 24c. In postcentral cortical areas all labeling was ipsilateral and there were two major foci of labeled cells: (1) the depths of the intraparietal sulcus including areas VIP, LIP, and PEa, and (2) the anterior wall and fundus of the superior temporal sulcus including areas PP and MST. Smaller numbers of labeled cells were found in superior temporal sulcal areas FST, MT, and STP, posterior cingulate area 23b, area 3a within the central sulcus, areas SII, RI, Tpt in the lateral sulcus, and parietal areas 7a, 7b, PEc, MIP, DP, and V3A. Many of these posterior afferent cortical areas code visual-motion (MT, MST, and FST) or visual-motion and vestibular (PP, VIP) signals, consistent with the responses of neurons in FEFsem and with the overall physiology and anatomy of the smooth-pursuit eye movement system.

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Abbreviations

3a:

Sensorimotor cortex (Krubitzer et al. 2004)

7a:

Subdivision of Brodmann’s area 7 (Cavada and Goldman-Rakic 1989a)

7b:

Subdivision of Brodmann’s area 7 (Cavada and Goldman-Rakic 1989a)

8:

Brodmann’s area 8 (Preuss and Goldman-Rakic 1991)

23b:

Subdivision of Brodmann’s area 23 (Vogt et al. 1987)

24:

Brodmann’s area 24 (Vogt et al. 1987)

24c:

Subdivision of Brodmann’s area 24 (Vogt et al. 1987)

45:

Brodmann’s area 45 (Preuss and Goldman-Rakic 1991)

46:

Brodmann’s area 46 (Preuss and Goldman-Rakic 1991)

DP:

Dorsal prelunate area (Colby et al. 1988)

F2:

A dorsal premotor area (Matelli and Luppino 2001)

F7:

A dorsal premotor area (Matelli and Luppino 2001)

FEFsac:

Saccade part of the frontal eye field (Bruce et al. 1985)

FEFsem:

Smooth-pursuit part of the frontal eye field (MacAvoy et al. 1991)

FST:

Fundus of the superior temporal sulcus area (Boussaoud et al. 1990)

LIP:

Lateral intraparietal area (Blatt et al. 1990)

M1:

Primary motor cortex (Dum and Strick 1991)

MIP:

Medial intraparietal area (Colby et al. 1988)

MST:

Medial superior temporal area (Boussaoud et al. 1990)

MT:

Middle temporal area (Boussaoud et al. 1990)

PE:

Parietal area E (Brodmann’s area 5) (Marconi et al. 2001)

PEa:

Subdivision of area PE (Marconi et al. 2001)

PEc:

Subdivision of area PE (Marconi et al. 2001)

PMv:

Ventral part of the premotor area (Fujii et al. 2000)

PP:

Posterior parietal area (Colby et al. 1988)

RI:

Retroinsular area (Grüsser et al. 1990)

SEF:

Supplementary eye field (Schlag and Schlag-Rey 1987)

SII:

Secondary somatosensory area (Cipolloni and Pandya 1999)

STP:

Superior temporal polysensory area (Boussaoud et al. 1990)

Tpt:

Temporoparietal (auditory) area (Seltzer and Pandya 1989)

V3A:

A visuotopic prestriate area (Colby et al. 1988)

VIP:

Ventral intraparietal area (Bremmer et al. 2002a)

as:

arcuate sulcus

cs:

central sulcus

ips:

intraparietal sulcus

las:

lateral sulcus

lus:

lunate sulcus

ots:

occipitotemporal sulcus

pas:

postarcuate spur

ps:

principal sulcus

sts:

superior temporal sulcus

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Acknowledgments

This work was supported by National Eye Institute Grant EY-04740 and National Institute of Mental Health Grant MH-44866. Address reprint requests to Gregory B. Stanton, Department of Anatomy, Howard University College of Medicine, Washington DC 06520-8001.

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Authors and Affiliations

  1. Department of Anatomy, Howard University College of Medicine, 520 W St., N.W., Washington, DC, 20059, USA

    Gregory B. Stanton

  2. Department of Neurobiology, Yale University School of Medicine, New Haven, CT, 06520-8001, USA

    Harriet R. Friedman, Elisa C. Dias & Charles J. Bruce

  3. Nathan Kline Institute, 140 Old Orangeburg Rd, Orangeburg, NY, 10962, USA

    Elisa C. Dias

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  1. Gregory B. Stanton
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Stanton, G.B., Friedman, H.R., Dias, E.C. et al. Cortical afferents to the smooth-pursuit region of the macaque monkey’s frontal eye field. Exp Brain Res 165, 179–192 (2005). https://doi.org/10.1007/s00221-005-2292-z

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