Abstract
The planning, control and execution of eye movements in 3D space relies on a distributed system of cortical and subcortical brain regions. Within this network, the Eye Fields have been described in animals as cortical regions in which electrical stimulation is able to trigger eye movements and influence their latency or accuracy. This review focuses on the Frontal Eye Field (FEF) a “hub” region located in Humans in the vicinity of the pre-central sulcus and the dorsal-most portion of the superior frontal sulcus. The straightforward localization of the FEF through electrical stimulation in animals is difficult to translate to the healthy human brain, particularly with non-invasive neuroimaging techniques. Hence, in the first part of this review, we describe attempts made to characterize the anatomical localization of this area in the human brain. The outcome of functional Magnetic Resonance Imaging (fMRI), Magneto-encephalography (MEG) and particularly, non-invasive mapping methods such a Transcranial Magnetic Stimulation (TMS) are described and the variability of FEF localization across individuals and mapping techniques are discussed. In the second part of this review, we will address the role of the FEF. We explore its involvement both in the physiology of fixation, saccade, pursuit, and vergence movements and in associated cognitive processes such as attentional orienting, visual awareness and perceptual modulation. Finally in the third part, we review recent evidence suggesting the high level of malleability and plasticity of these regions and associated networks to non-invasive stimulation. The exploratory, diagnostic, and therapeutic interest of such interventions for the modulation and improvement of perception in 3D space are discussed.
Highlights
FEF, A CROSSROADS FOR EYE MOVEMENTS AND VISUO-SPATIAL COGNITION The frontal eye field (FEF) is an area of the frontal cortex in animals over which electrical stimulation is able to trigger eye movements
In humans for example, such gaze control systems include in the frontal lobe the supplementary eye field (SEF), the Abbreviations: CEF, cingulate eye field; DLPFC, dorsolateral prefrontal cortex; EEG, electroencephalography; FEF, frontal eye field; functional Magnetic Resonance Imaging (fMRI), functional magnetic resonance imaging; IPS, intraparietal sulcus; LIP, lateral intraparietal area; MEG, magneto-encephalography; medial superior temporal area (MST), medial superior temporal; PEF, parietal eye field; PET, positron emission tomography; PPC, posterior parietal cortex; rTMS, repetitive transcranial magnetic stimulation; SC, superior colliculus; SEF, supplementary eye field; Transcranial Alternate Current Stimulation (tACS), transcranial alternate current stimulation; tDCS, transcranial direct current stimulation; Transcranial Magnetic Stimulation (TMS), transcranial magnetic stimulation
Pre-supplementary eye field, the dorsolateral prefrontal cortex (DLPFC), the cingulate eye field (CEF) within the anterior cingulate cortex and the dorso-medial frontal cortex, and in the parietal lobe, the parietal eye field (PEF) and areas of the posterior parietal cortex (PPC). Subcortical structures, such as the superior colliculus (SC) in the midbrain are considered essential to trigger eye movements. All these areas operate cooperatively, some of them contribute to the triggering of eye movements under specific situations: the PEF for example has a role in reflexive saccades, the FEF participates in voluntary saccades, the SEF contributes to the development of more complex motor programs involving gaze (Pierrot-Deseilligny et al, 2002)
Summary
FEF, A CROSSROADS FOR EYE MOVEMENTS AND VISUO-SPATIAL COGNITION The frontal eye field (FEF) is an area of the frontal cortex in animals over which electrical stimulation is able to trigger eye movements. More than one hundred years later, other microstimulation studies evoking eye movements (Robinson and Fuchs, 1969; MacAvoy et al, 1991; Gottlieb et al, 1993; Izawa et al, 2004a,b, 2009), electrophysiological recordings during visual stimulation and/or eye movements (Bizzi, 1968; Wurtz and Mohler, 1976; Bruce and Goldberg, 1985; Segraves and Goldberg, 1987) and studies comparing cells discharge patterns during behavior or its alteration during the stimulation of these same neuronal populations (Bruce et al, 1985; Gottlieb et al, 1994) confirmed the existence of an FEF located in the posterior part of the prearcuate sulcus They distinguished visual (modulated by functional significance), motor and visuo-motor neural populations for saccade, pursuit and fixation/saccade suppression, somehow spatially segregated and with different stimulation thresholds, which depended on the activation state of the monkey at the time of the stimulation. RECONCILING NON-HUMAN PRIMATES’ AND HUMANS’ LOCATIONS FOR THE FEF? In brief, the non-human primate FEF, localized mainly thanks to microstimulation studies, lies in a more rostral location
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