Frontal eye field

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Ryan Fox Squire et al. (2012), Scholarpedia, 7(10):5341. doi:10.4249/scholarpedia.5341 revision #129338 [link to/cite this article]
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Authors RFS and NAS contributed equally to this work.

The Frontal Eye Field (FEF) is a region of primate prefrontal cortex defined as the area in which low-current electrical stimulation evokes saccadic eye movements. On the basis of stimulation, recording, and inactivation experiments, the FEF appears to play a significant role in the planning and execution of saccadic eye movements. These same types of experiments have more recently demonstrated that the FEF also participates in the control of visual selective attention. In this article, we discuss the Frontal Eye Field’s connectivity with other structures in visual and oculomotor regions of the brain and examine the evidence for its multiple functional roles in visually guided behavior. We focus primarily on the FEF as studied in macaque monkeys, though we briefly discuss its homologues in other species, including humans. Finally, we suggest important future directions for FEF research.


A Historical Look at the Frontal Eye Field

In 1875, David Ferrier presented a paper to the Royal Society of London to convey “the results obtained by electrical stimulation of the brain of monkeys.” (Ferrier, 1875, p. 409). Among other interesting observations, he described a small portion of the frontal lobe that upon unilateral stimulation produced, “…turning of the eyes and head to the opposite side” (Ferrier, 1875, p. 424). Over the next one hundred years the results of stimulating this area were replicated in many species of primates, including monkeys, gorillas, orangutans, chimpanzees, and even humans with increasing focus on anatomy, electrical stimulation parameters, anesthesia type and level, and the nature of the movements evoked (Smith, 1949; Crosby et al., 1952). In the modern era of brain research this small sliver of the prefrontal cortex (PFC) known as the Frontal Eye Field (FEF) is localized to the area of PFC from which short-latency saccadic eye movements (saccades) can be evoked reliably by electrical stimulation using relatively low electrical currents (Robinson and Fuchs, 1969). In fact, this is presently how the FEF is identified.

Around the same time that Ferrier conducted stimulation experiments on the Frontal Eye Field, he and others had studied the effects of lesions to this part of the brain (as well as surrounding tissue) to understand its role in behavior (Ferrier, 1890; Bianchi, 1895). Consistent with the stimulation experiments, the most readily apparent effects of unilateral lesions was an immediate dearth of orienting head and eye movements to the contralateral side, suggesting a role of this area in gaze control. Moreover, these lesion studies and others during the next 100 years are marked by two additional observations which have been at the heart of the discussion and controversy about the FEF ever since (Ferrier, 1890; Bianchi, 1895; Kennard, 1939; Welch and Stuteville, 1958). First, the effects of these lesions seemed to be temporary; within weeks after surgery the animal subjects showed few lingering signs of impairment. Second, besides the anticipated deficits in eye movements, experimenters noted a profound cognitive and perceptual deficit: “After unilateral ablation of area 8 [(the FEF),] objects in the contralateral visual field are ignored.” (Kennard, 1939, p. 1165). “…It is a form of mental degradation which appears to me to depend on the loss of the faculty of attention...” (Ferrier, 1890 p. 74). The advent of single neuron electrophysiological recordings in alert monkeys in the last 50 years, accompanied by more precise lesion and stimulation experiments, have helped to clarify the function of the FEF in motor, perceptual, and cognitive processes. Nonetheless, a unified understanding of the role of the FEF in these multiple brain functions has been controversial.

A striking aspect of the last 125 years of research on the Frontal Eye Field is the persistent difficulty to conceptualize the FEF as a motor structure versus a sensory structure (e.g. Bizzi, 1968; Bruce and Goldberg, 1985; Schafer and Moore, 2007). This problem is apparent in the very first descriptions by Ferrier, Bianchi, and others and continues throughout history, even in contemporary discussions. Modern proposals integrate data from psychology, psychophysics, and neurobiology and suggest that a useful way to approach a sensorimotor structure like the FEF is to consider the functional relationship between motor control and perception in the context of selective attention. At its heart, this is an old idea (see Moore, Armstrong, & Fallah, 2003). In fact, in trying to explain his observations about the FEF, Ferrier insightfully wrote, “…my hypothesis is that the power of attention is intimately related to the volitional movements of the head and eyes.” (Ferrier, 1890, p. 74). Still, an integrated understanding of the function of the FEF remains a challenge of contemporary research. Modern tools and increasingly interdisciplinary thinking promise to extend our knowledge further than perhaps Ferrier might have imagined.

Anatomical Organization and Functional Topography

Figure 1: The connectivity and anatomical locations of the Frontal Eye Field (FEF) and other structures within the visual and oculomotor systems of the rhesus macaque monkey brain. Left panel, diagram of the connectivity of the FEF (orange) with other visual and oculomotor structures. Some connections that do not directly involve the FEF are omitted. Right panel, locations of the brain regions pictured in the left panel shown in the lateral view of the monkey brain. In both panels, surface structures other than the FEF are colored darker blue. Deep structures are illustrated as lighter blue and with a dashed outline. Abbreviations: BG, basal ganglia; BSG, brainstem saccade generator; Cbl, cerebellum; Ex Vis Ctx, extrastriate visual cortex; LIP, lateral intraparietal area; SC, superior colliculus; SEF, supplementary eye field; Thal, thalamus; V1, primary visual cortex.

As stated above, the Frontal Eye Field is defined as that part of the PFC in which saccades can be elicited with low amplitude electrical stimulation. Anatomical studies have shown that this part of cortex is located primarily in the prearcuate sulcus, specifically Brodmann areas 45A, 45B, and 8Ac (see Figure 1). These areas notably share cytoarchitectural characteristics of both primary motor cortex (in which other types of motor actions can also be elicited with low-current stimulation) and granular frontal cortex (which are typically associated with higher-order cognitive functions). Specifically, the FEF, as opposed to surrounding cortex, has a high concentration of large (>22µm diameter) pyramidal neurons in Layer 5 (Stanton et al., 1989), a feature common in primary motor cortical areas. The FEF also has a population of large Layer 3 pyramidal neurons and has a visible, though not entirely well defined, granular layer (Layer 4), both of which characteristics also distinguish it from surrounding cortex (Stanton et al., 1989). The presence of the granular layer is consistent more with the properties of granular frontal cortex (GFC) than with “true” motor cortex (which lacks the granular layer), and is perhaps consistent with the FEF’s involvement in cognitive functions, like other regions of GFC.

The saccades evoked by electrical stimulation of the Frontal Eye Field can be used to reveal its functional topography as stimulation of nearby sites usually elicits saccades to nearby locations in retinotopic space (Bruce et al., 1985). However, discontinuities in a series of evoked saccades from nearby cortical sites are frequently encountered, suggesting that the topography is not strictly retinotopic. Nonetheless, small saccades are generally elicited by stimulation of area 45 within the ventrolateral limb of the arcuate sulcus, while large amplitude saccades are elicited by stimulation of area 8A within the dorsomedial limb. In addition, within the dorsomedial portion of the FEF, combined head and eye movements can be elicited (Tu and Keating, 2000; Monteon et al., 2010) consistent with a general role of the FEF in gaze control, as gaze is defined as involving both head and eye components.

Connections with the Oculomotor System

Frontal Eye Field neurons interconnect extensively with other known structures of the primate saccadic system (see Figure 1). The FEF has topographic projections directly to the intermediate layers of the ipsilateral superior colliculus (SC) (Leichnetz et al., 1981), particularly to neurons exhibiting saccade related activity (Helminski and Segraves, 2003). The FEF also projects to the ipsilateral caudate and putamen (Künzle and Akert, 1977), to the cerebellum via the pontine nuclei, and to many oculomotor-associated nuclei in the midbrain and pons including the “brainstem saccade generator” nuclei (Leichnetz et al., 1984; Huerta et al., 1986). In the brainstem, the FEF drives “burst” neurons in the paramedian pontine reticular formation, which control the direction and amplitude of saccades. These burst neurons are gated by “pause” neurons in the nucleus raphe interpositus, and directly drive the motor neurons when ungated. The FEF receives subcortical projections from various saccade-related thalamic nuclei including the lateral mediodorsal (MD), medial ventral anterior (VA), and medial pulvinar, among others (Huerta et al., 1986). In addition, the intermediate layers of the SC, the substantia nigra pars reticulata, and the dentate nucleus of the cerebellum all project to the FEF indirectly via the MD and VA thalamic nuclei (Lynch et al., 1994). In addition to the extensive connections with subcortical oculomotor structures, the FEF has extensive connections with other saccade-related cortical areas, including the supplementary eye field (SEF), dorsolateral prefrontal cortex (dlPFC), area 7m in the medial parietal lobe, and the lateral intraparietal area (LIP), all cortical regions from which saccades can also be elicited via electrical stimulation, albeit with higher currents (Lynch and Tian, 2006).

Role in Gaze Control

Figure 2: Basic electrophysiological features of Frontal Eye Field neurons. Left panel, hypothetical responses of some (but not all) types of FEF neurons during a memory-guided delayed saccade task. The sequence of events within this task is illustrated in the upper part of the panel. The monkey foveates the fixation point (small white circle), and a visual stimulus (white square) is transiently displayed shortly thereafter. The monkey continues to hold his gaze on the fixation point for a variable delay period. After the fixation point disappears, the monkey is free to execute a saccade (black arrow) to the remembered location of the visual target to earn a juice reward. The top two rows of the panel depict the screen contents during the visual stimulation, delay period, and saccade execution (from left to right, respectively). The top row shows an “inside-RF” trial in which the visual stimulus and saccade both in the receptive field (RF, indicated by dashed line) of the recorded FEF neuron. The second row of screens depicts an “outside-RF” trial in which the visual stimulus and saccade are away from the RF of the neuron. The lower part of the panel depicts the time course of trial events and the hypothetical recorded neuronal responses, aligned to stimulus onset time (left) and saccade onset (right). The inside-RF and outside-RF trials illustrated in the upper-half of the figure correspond respectively to the solid and dashed lines in the eye position and neural firing rate traces in the lower half of the figure. Separate bold black lines indicate the times when the fixation point or visual stimulus appears on the screen. Hypothetical eye position is shown for both inside- and outside-RF trial types as a solid or dashed black line, respectively. Several firing rate traces associated with inside-RF trials (colored lines) are displayed, corresponding to visuomotor (red), visual transient (blue), motor (orange), and motor with delay activity (green) neuron response types. Right panel, the results of electrical stimulation at a FEF site. As the monkey fixates, a brief (e.g. 50 ms) train of electrical stimulation pulses is applied via a microelectrode in the FEF. A short-latency (e.g. 40 ms) saccade is evoked toward the movement field of the recording site.

As it is entirely unclear to what extent the behavioral responses evoked via electrical microstimulation demonstrate a role of the stimulated neural tissue in producing those behaviors under normal physiological conditions (Clark et al., 2011), corroborative evidence for such a role must be obtained from other methods. In the case of the Frontal Eye Field, stimulation evoked saccades could result from antidromic activation of the axonal projections from other oculomotor structures (e.g. LIP, SEF, thalamic nuclei, etc.) rather than orthodromic activation of FEF neurons projecting to the SC or brainstem. Thus, evidence from electrical stimulation studies alone is insufficient to understand the role that FEF neurons play in the control of gaze. Following reversible pharmacological inactivation of sites within the FEF, saccades to contralateral visual targets have longer reaction times and lower peak velocities, are fewer in number, and less accurately targeted (for review of inactivation and lesion experiments in the FEF, see Tehovnik et al., 2000). Lesions of the FEF produce similar deficits that recover with time (Schiller et al., 1980, 1987). The deficits in both inactivation and lesion experiments are particularly pronounced for contralateral antisaccades, i.e. saccades directed to locations opposite a visual target, or for saccades made to remembered targets (memory guided saccades). The fact that saccades persist after temporary or permanent inactivation of the FEF suggests that the FEF is not necessary for saccade production. Indeed, a classic set of experiments showed that although neither lesions of the FEF nor lesions of the superior colliculus (SC) eliminate saccades, combined lesions to both structures completely abolishes them (Schiller et al., 1980). Thus, though the FEF is clearly part of the network controlling saccades, it appears to be either partly redundant with, complementary to, or acting in conjunction with, the SC. Structures homologous with the FEF, defined primarily on the basis of lesion and stimulation experiments, have been described in the forebrain of many other species. These include numerous New and Old World primate species (Schall, 1997), rat (Sinnamon and Galer, 1984; Erlich et al., 2011), cat (Schlag-Rey and Lindsley, 1970), and owl (Knudsen and Knudsen, 1996), among others. Classic electrical stimulation studies initially established the existence and location of human FEF homologue (Penfield and Boldrey, 1937), and more recent stimulation and neuroimaging studies have further corroborated the role of this area in gaze control (Blanke et al., 2000; Levy et al., 2007).

The common scheme of functionally classifying Frontal Eye Field neurons involves correlating their activity with the onset of visual stimuli and with the onset of saccades in a memory-guided saccade task (Figure 2). FEF neurons are classified by whether they respond to the onset of a visual stimulus (“visual”), before the onset of a saccade (“movement”), or both (“visuomovement”). Like neurons within posterior visual areas, FEF neurons exhibiting visual responses have a receptive field (RF), i.e. a region of visual space in which stimulation elicits a response. Neurons exhibiting movement-related responses likewise exhibit those responses only prior to saccades to a restricted portion of visual space, known as the movement field (MF). The RFs and MFs of visuomovement neurons tend to be coextensive. Likewise, saccadic eye movements driven by electrical microstimulation at the recording site are consistent with the MF (Bruce et al., 1985).

Generally, visual and visuomovement neurons are more frequently encountered than movement neurons. For example, Bruce and Goldberg (1985) reported that approximately 20% were visual, 10% were movement and 20% were visuomovement. Although this functional scheme is widely utilized and useful in describing the sensory and motor properties of the Frontal Eye Field (e.g. Thompson et al., 2005) these cell classes are not strictly distinct. FEF neurons instead appear to fall on a continuum between purely visual and purely movement responsiveness (Bruce and Goldberg, 1985). Moreover, a substantial proportion of FEF neurons respond neither to visual stimuli nor prior to saccades, but instead either respond post-saccadically or exhibit no modulation during the memory-guided saccade task. While the exact proportions of FEF neuron types is difficult to determine due to sampling biases (Olshausen and Field, 2005) and variation across experiments, it is nevertheless an interesting observation that a substantial majority of FEF neurons do not respond immediately preceding a saccade, and therefore those neurons cannot participate directly in the generation of saccades.

The correlation between the functional properties of Frontal Eye Field neurons and their anatomical neuron classes (layer, morphological cell type, or connectivity) remains largely ambiguous. Over half of the FEF neurons that project to the superior colliculus (corticotectal neurons), located in layer 5, are movement neurons (Segraves and Goldberg, 1987), though it is unclear whether this population of corticotectal movement neurons accounts for all movement neurons. Some of these corticotectal cells also show visual and memory related activity (Sommer and Wurtz, 2001). Considering all FEF neurons, those with visuomovement responses tend to have narrower spike waveforms, possibly indicating that they tend to be fast-spiking inhibitory interneurons, as opposed to visual and movement neurons which have broader waveforms and are therefore more likely to be pyramidal (Cohen et al., 2008). Importantly, as it is known that nonpyramidal neurons do not generally make long-range connections, this result suggests that visuomovement neurons are unlikely to project outside of the FEF. A computational model has attempted to link the observations of functionally defined cell types in the FEF with known underlying connectivity between anatomical classes of neocortical neurons (Heinzle et al., 2007). The neurons in the model reproduce all observed response types of real FEF neurons, though in the model, functional types are segregated to separate anatomical layers, a design that appears to be in conflict with earlier studies localizing some movement and visual type neurons to Layer 5 pyramidal cells (Sommer and Wurtz, 2001). Thus, while progress has been made in understanding the functional architecture of FEF circuits, this area remains largely unexplored.

One conception of the role of the Frontal Eye Field in generating saccades is as a salience map that compares the relative importance of parts of the visual scene as targets for foveation, then selects the most salient in a winner-take-all competition (Itti and Koch, 2000; Thompson and Bichot, 2005), a process sometimes called “saccade target selection.” In this scenario, all types of evidence bearing on the salience of parts of the visual scene, including bottom-up sensory information (independent of its particular features) and top-down goal-related signals, would be combined to drive the activity of FEF neurons (Thompson and Bichot, 2005). Indeed, FEF neurons are rarely tuned for the specific features of visual stimuli except in the context of their salience as saccade targets (Mohler et al., 1973; Schall et al., 1995a), sometimes respond to auditory stimuli (Bruce and Goldberg, 1985; Russo and Bruce, 1994), and are driven by planned and remembered saccade targets (Bruce and Goldberg, 1985). Additionally, FEF neurons appear to increase their firing rate up to a “bound”, at which point saccades are generated to the location of the MF of that neuron, an observation consistent with winner-take-all models of competition (Hanes and Schall, 1996). Importantly, in a task in which a monkey is trained to detect a salient stimulus and saccade to a separate location, different neural populations within the FEF select either the salient stimulus (“visual selection”) or the eventual location of the saccade itself (“saccade selection”; Sato and Schall, 2003). Thus the FEF may have a role as a salience map for visual stimuli even independent of its role in generating saccades, though the most salient stimulus is normally the same as the target of the saccade.

Connections with Visual Cortex

The Frontal Eye Field is intricately connected with areas within posterior visual cortex of the occipital, parietal, and temporal lobes beyond primary visual cortex. The connections, which are reciprocal, include areas V2, V3, V4, MT, MST, LIP, TEO, and TE, and thus both dorsal and ventral visual ‘streams’ (Stanton et al., 1995; Schall et al., 1995b) (See Figure 1). Since the FEF generally receives “feedforward” input and sends “feedback” projections to and from all of these visual cortical areas, the FEF is placed high within the visual hierarchy (Felleman and Van Essen, 1991). Moreover, visual regions representing central visual space (i.e. within ~10 degrees of the fovea), are interconnected with the ventrolateral limb of the FEF that represents small-amplitude saccades (Stanton et al., 1995; Schall et al., 1995b). Visual regions representing the visual periphery are interconnected with the dorsomedial limb of the FEF that represents large-amplitude saccades to peripheral locations (Stanton et al., 1995; Schall et al., 1995b). Thus, these organized and reciprocal connections indicate that not only does the FEF receive information from across the visual hierarchy, but that it also has the capacity to influence the processing of visual information in neurons that vary widely in the type of visual information they encode (e.g., orientation, motion, color, form, object identity) (Moore et al., 2003). The FEF is also reciprocally connected to other visually responsive areas of the frontal lobe (e.g., dlPFC) as well as subcortical structures (e.g., pulvinar), which may contribute to a more general role of the FEF in visually guided behavior.

Role in Attention and Perception

Initially, the investigation of the Frontal Eye Field's role in sensory function was largely focused on its role in the selection of visual stimuli as saccade targets (i.e. saccade target selection) (Schall, 1997). However, the idea that the FEF may have a more fundamental role in perception and cognition dates back to the original description of the FEF by Ferrier in the late 19th century (Ferrier, 1890), as discussed. More broadly, the idea that oculomotor structures may also be involved in the control of spatial attention is rooted in a long history of psychophysical observations closely linking visual perception with the planning and executing of saccades (e.g., Ribot, 1898; see Moore et al., 2003 for discussion). This history, combined with the FEF’s wide spread anatomical connections with the visual system, provides a compelling basis to consider a possible role of the FEF in perception and attention beyond its role in the control of gaze. To understand how the FEF may have a role in perception and attention independent of eye movements, it is first important to note that attention can be controlled independently from eye movements. In most day-to-day life we tend to look directly (i.e., overtly attend) at whatever is the focus of our attention. However, it is an interesting and well-documented feature of (at least) the primate visual system that attention can be deployed to an object or location in peripheral vision without moving the eyes or head, (i.e., covertly attend), and some have argued for the adaptive functions of this ability (Posner, 1980; Wright and Ward, 2008).

If it is the case that activity in the Frontal Eye Field is related to covert attention, then one would expect the activity of neurons in the FEF to be correlated with the focus of the monkey’s attention, even in the absence of saccades. Single-neuron recordings of the FEF neurons indeed show a significant modulation in firing rates associated with the spatial location of covert attention independent of any eye movements (Kodaka et al., 1997; Thompson et al., 2005; Monosov et al., 2008; Armstrong et al., 2009; but see Goldberg and Bushnell, 1981). For example, the responses of FEF neurons are selectively enhanced to a peripheral visual stimulus in its RF when that stimulus is the target of a challenging visual discrimination (and thus the focus of covert attention), even when the monkey is rewarded for not overtly orienting (i.e., not saccading) to the visual stimulus (Armstrong et al., 2009). But are the attention-modulated FEF neurons the same or different from the FEF neurons that seem to be involved in controlling eye movements? Interestingly, a significant proportion of the covert attention-modulated FEF neurons are also activated presaccadically during eye movements; moreover, it was shown that visual and visuomovement neurons are significantly modulated by covert attention, whereas movement neurons are not (Thompson et al., 2005). Although there is some data linking visual, movement, and visuomovement neurons with anatomy (see Role in Gaze Control) there are no published reports attempting to link the functional responses of FEF neurons during attention to specific anatomical properties (e.g., layer, morphological cell type, connectivity, etc). Thus, although it has been shown that the activity of neurons in the FEF correlates with covert spatial attention, the identity of these cells remains open to speculation.

If neural activity in the Frontal Eye Field is involved in the control of attention, then perturbing activity in the FEF should affect attention. Indeed, unilateral lesions to the FEF result in transient contralateral neglect (Welch and Stuteville, 1958; Lynch and McLaren, 1989). Consistent with the lesion studies, unilateral pharmacological inactivation of the FEF leads to spatially specific contralateral reaction time deficits in a visual search task, even when the monkey abstains from eye movements during the search (Wardak et al., 2006; Monosov and Thompson, 2009). Some of the most compelling data to support the role of the FEF in attention and perception are experiments using electrical microstimulation. If increased activity in the FEF is causally related to the focus of spatial attention, then generating activity in the FEF through stimulation should produce spatially specific attention-like effects on behavior and physiology. To test this, Moore and Fallah (2001, 2004) electrically stimulated FEF sites of monkeys performing a change detection task. Change detection tasks are effective in measuring the influence of selective attention on visual perception. Trying to detect a change in a complex and dynamic display can be challenging, but is made much easier if one knows ahead of time where in the scene the change will occur (Rensink, 2002). In stimulating the FEF, Moore and Fallah used stimulation currents that were too weak to evoke saccades (i.e. subthreshold currents), but were nonetheless expected to facilitate the preparation of saccades to a particular location (Schiller and Tehovnik, 2001). The authors found that such stimulation could improve the ability of monkeys to detect changes in the target. Moreover, Just like stimulating different parts of the FEF evokes saccades to different locations in space, stimulating the FEF only improved change detection if the to-be-detected visual change occurred at a specific spatial location.

Further experiments showed that Frontal Eye Field microstimulation not only improves behavioral performance in attention demanding tasks but also modulates the processing of visual information by neurons within visual cortex (e.g., in V4 neurons) in ways that resemble the widely studied effects of spatial attention (Moore and Armstrong, 2003; Armstrong et al., 2006; Armstrong and Moore, 2007; Ekstrom et al., 2008, 2009). Like the behavioral effect of FEF microstimulation, the effects on visual cortical neurons required that the RFs of visual neurons and the representation of the stimulated FEF sites were spatially overlapping. Thus, behavioral performance and visual information processing was not globally enhanced by stimulating the FEF, as might be associated with an increase in arousal or alertness, but was only enhanced at a specific spatial location dictated by where in the FEF the experimenters had positioned their electrode. Thus, these experiments provide evidence that enhanced activity within the FEF is sufficient to drive neural and behavioral correlates of spatial attention, suggesting that the FEF may be a source of attentional control in the primate brain. More recent work not only confirms that FEF neuronal activity per se influences the “gain” of visual cortical activity, but has also identified a role of the neuromodulator dopamine in mediating that control (Noudoost and Moore, 2011a) This latter observation may provide a basis for the apparent role of prefrontal dopamine in disorders of attentional control, such as in attention-deficit hyperactivity disorder (ADHD; e.g. Ernst et al., 1998).

In non-macaque species, the gaze control region that appears to be homologous with macaque Frontal Eye Field also appears to play an important role in attention. Studies using functional magnetic resonance imaging (fMRI) have shown that human FEF is activated during covert shifts of attention (Corbetta et al., 1998; Kastner et al., 1999; Nobre et al., 2000). A number of studies using transcranial magnetic stimulation (TMS) to non-invasively and reversibly perturb the activity of the FEF in awake human subjects have provided causal evidence of a role of the FEF in human attention (Grosbras and Paus, 2003; Muggleton et al., 2003; Ruff et al., 2006). Other studies have found that manipulating the activity in the human FEF via TMS modulates retinotopic visual representations in human visual cortex as measured by fMRI (Silvanto et al., 2006; Ruff et al., 2006). These results are analogous to the results in the macaque monkey using simultaneous electrical microstimulation and single-neuron recordings or fMRI (Moore and Armstrong, 2003; Armstrong et al., 2006; Armstrong and Moore, 2007; Ekstrom et al., 2008, 2009). Thus studies from both human and monkeys have established an important role of the FEF in the control of attention and sensory processing in the visual system.

In addition to the work in humans and non-human primates, research in the barn owl (Tyto alba), and its Frontal Eye Field homologue, the arcopallial gaze field (AGF), deserves special mention. Winkowski and Knudsen demonstrated a role of the AGF in modulating sensory processing in a manner consistent with the effects of attention (Winkowski and Knudsen, 2006, 2007, 2008). Similarities between the primate FEF and the barn owl AGF in attention is particularly interesting because the evolutionary lines of these two species diverged over 300 million years ago (Reynolds, 2008). Thus, these data suggest that there may be generalizable evolutionary principles (either conserved or converged) for how overt and covert orienting mechanisms are functionally organized by the nervous system. More research on the FEF homologues in non-primate species is needed to provide further insight into this interesting idea. Together, anatomical, neurophysiological, and behavioral data to date suggest that the FEF controls the deployment of both covert and overt spatial attention. When a subject attends to a particular location, spatially specific activity within the FEF may be conveyed to extrastriate visual cortex via the FEF’s extensive retinotopically organized feedback projections. These signals improve the visual cortical processing of objects at the targeted location. These enhanced representations can then facilitate visually guided behavior, such as saccades to moving targets (Schafer and Moore, 2007). Importantly, FEF is just one of several structures in the brain that contain attention-modulated neurons and/or that can be experimentally manipulated to modulate attention (Noudoost et al., 2010; Baluch and Itti, 2011). The relative role of the FEF within this attention network remains unknown.

Future Directions and Open Questions

The preceding summary of what we know about the Frontal Eye Field also highlights how much we have yet to understand. Even the organization of this review, which divides the function of the FEF into two parts--the control of overt gaze and the control of covert visual attention--is an oversimplification. Such a division underscores the lack of an integrated understanding of the FEF as a single structure that simultaneously performs both of these functions. Ultimately, this division may fail to appropriately describe the complexity of the FEF’s function. For example, we have omitted discussion of a wide variety of reported properties of FEF neurons other than those related to vision, eye movements and attention. FEF neurons can exhibit visual feature selectivity (Xiao et al., 2006; Peng et al., 2008), decision-related signals (Ferrera et al., 2009), corollary discharge-related activity (Sommer and Wurtz, 2006), and auditory responses (Schall, 1997), among other properties. How do the FEF neurons that encode these different types of information relate to one another? Which anatomical or functional subtypes of FEF neurons exhibit these properties? Do all the different types of information encoded in the FEF correspond to a fundamental set of functional cell types? What cellular properties (e.g., cellular morphology, synaptic receptors, membrane channels) enable FEF neuronal types to exhibit different functional properties? Are different FEF neuron types associated with specific neocortical layers or unique patterns of connectivity within the local FEF microcircuitry? What (if any) unique computations or transformations underlying behavior are performed within the FEF? How are these transformations implemented by the different functional or anatomical cell types found in FEF or by the dynamics of recurrent, local FEF microcircuits?

As important as it is to understand the functions of the local circuitry within the Frontal Eye Field , it is equally important to understand the function of the FEF within a broader network of brain structures. Some of these structures, like area LIP or the SC, have many similarities with the FEF, such as the patterns of neuronal responses, and the effects of perturbing these structures on vision, eye movements, and attention. At present, all three structures appear to play a crucial role in gaze control and visual attention (Wurtz, 2008; Baluch and Itti, 2011), and it is unclear how their roles relate to one another. For example, these structures could play redundant or complementary roles in those functions. Indeed, recent studies suggest that area LIP may have a more specialized role in bottom-up attention (Buschman and Miller, 2007), while the FEF may play a specialized role in top-down attention (Schafer and Moore, 2011). In addition, the relationship between the FEF and other frontal areas is particularly interesting. For example, to what degree will the properties found in FEF generalize to the other less well-studied structures within PFC? Given that the FEF must interact with many other structures to guide behavior, relatively little is understood about the mechanisms underlying these interactions. For example, in the case of the FEF’s influence on visual responses within area V4 (e.g. Moore and Armstrong, 2003), it is not known whether those influences act via direct projections to V4 or through intermediary structures. Is the influence mediated purely through these feedback connections, or are reciprocal interactions between FEF and V4 necessary (Noudoost and Moore, 2011b)? What are the circuit mechanisms by which relevant feedback projections actually influence information processing in V4? What kinds of V4 neurons directly (and indirectly) receive this feedback? What are the roles of neural oscillations and neuromodulators in these interactions (Gregoriou et al., 2009; Noudoost and Moore, 2011a, 2011b)?

In closing, we point out that the Frontal Eye Field was named because of its apparent role in the control of gaze, particularly saccadic eye movements. However, as the study of the Frontal Eye Field has continued, descriptions of the FEF as a purely motor structure have faded from the literature due to the equally strong evidence linking the FEF to attention. In reconsidering the function of the FEF, we might conclude that perhaps its role in the control of saccades is just one manifestation of a broader role in the control of visual spatial attention, which encompasses both overt attention (i.e., saccades) and covert attention. This may provide a more parsimonious unification of two seemingly disparate functions. In light of this, we suggest that perhaps the name “Frontal Attention Field” might better reflect our understanding of this brain region. It may also facilitate establishing its homology with structures in other species (e.g. the rodent FOF, Erlich et al., 2011).

[Thanks to T.J. Buschman, V.P. Ferrera, E.K. Miller, J.D. Schall, M.A. Sommer, and R.H. Wurtz for their helpful suggestions for this section.]


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