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

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.

Evidence for a retinal velocity memory underlying the direction of anticipatory smooth pursuit eye movements

“…Interconnected with FEF is the supplementary eye field (SEF) (Huerta and Kaas 1990;Schall et al 1993), which is also thought to be heavily involved in generating anticipatory pursuit movements (de Hemptinne et al 2008;Fukushima et al 2004;Heinen et al 1995;Heinen and Liu 1997). Given various representations of reference frames in SEF (Heinen and Liu 1997;Martinez-Trujillo et al 2004;Olson and Gettner 1999;Russo and Bruce 1996;Tehovnik et al 1998), the activities of SEF and FEF during both visually guided and anticipatory pursuit (Bruce and Goldberg 1985;de Hemptinne et al 2008;Fukushima et al 2002Fukushima et al , 2004Gottlieb et al 1994;Heinen et al 1995;Heinen and Liu 1997), their coding of head orientation signals (Fukushima et al 2004;Fukushima et al 2000;Gottlieb et al 1993;Gottlieb et al 1994;MacAvoy et al 1991;Lisberger 2002a, 2002b), and close proximity in the pursuit circuitry (Maunsell and van Essen 1983), these findings lend credence to the idea that a separate pathway including SEF and FEF could be responsible for the coding of velocity memory and the transformation of anticipatory pursuit signals (Barnes and Collins 2008;de Hemptinne et al 2008;Heinen and Liu 1997;Missal and Heinen 2004;Russo and Bruce 1996;Shichinohe et al 2009;Stanton et al 2005), while area MST could compute the velocity transformation for visually guided pursuit, as previously suggested <...>…”

Ultra-Rapid Sensory Responses in the Human Frontal Eye Field Region

“…Specifically, in the case of the frontal eye fields, only one intermediate processing stage may be needed to get from V1 (Petroni et al, 2001). For example, FEF receives direct inputs from area MT (Stanton et al, 2005), which itself receives direct input from V1. Here, we demonstrated that the short latencies found in the FEF for both visual and auditory stimuli are compatible with cortical routes.…”

Pathways of Attention: Synaptic Relationships of Frontal Eye Field to V4, Lateral Intraparietal Cortex, and Area 46 in Macaque Monkey

“…Mitchell et al (2007) found that presumed inhibitory neurons show larger attention-dependent increases in firing rates than do presumed excitatory neurons. Hussar and Pasternak (2009) reported similar biases for presumed inhibitory neurons in the effects of attention in area 46, which is monosynaptically connected to FEF (Barbas and Mesulam, 1981;Huerta et al, 1987;Barbas and Pandya, 1989;Stanton et al, 2005). Inhibitory neurons have also been implicated in the strong suppression effects of distractors on area 46 neurons (Lennert and Martinez-Trujillo, 2011).…”