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• W1990602625 abstract "The frontal eye field (FEF) has been known as a key player in the generation of saccade motor commands and in the allocation of spatial attention. In this issue of Neuron, Schafer and Moore demonstrate that FEF microstimulation enhances the effect of a position illusion induced by visual motion on saccades. This finding suggests that FEF activity can modulate the deployment of spatial attention, which in turn can alter saccade motor commands. The frontal eye field (FEF) has been known as a key player in the generation of saccade motor commands and in the allocation of spatial attention. In this issue of Neuron, Schafer and Moore demonstrate that FEF microstimulation enhances the effect of a position illusion induced by visual motion on saccades. This finding suggests that FEF activity can modulate the deployment of spatial attention, which in turn can alter saccade motor commands. The majority of our visual system is devoted to the processing of visual information from the fovea, a small area on the retina of just a few degrees in diameter. This heavy bias in dedicated neural resources allows us to identify objects within this region in great detail. To compensate for the low resolution outside of this region, our brains house a complex network of cortical and subcortical areas that allow us to keep an object of interest on the fovea or to move the fovea to a new, potentially interesting object with a rapid saccadic eye movement. However, as we all know from daily experience, we can also shift our attention to the periphery of our visual field while keeping our eyes still. The “premotor theory of attention” proposes that covert shits of attention involve the same brain areas that move the eyes and that a covert shift of attention corresponds to the preparation of a latent saccade (Rizzolatti et al., 1987Rizzolatti G. Riggio L. Dascola I. Umilta C. Neuropsychologia. 1987; 25: 31-40Crossref PubMed Scopus (1326) Google Scholar). Support for this theory has come from functional brain imaging studies that have shown similar activated brain areas for covert shifts of spatial attention and saccade generation (Corbetta et al., 1998Corbetta M. Akbudak E. Conturo T.E. Snyder A.Z. Ollinger J.M. Drury H.A. Linenweber M.R. Petersen S.E. Raichle M.E. Van Essen D.C. Shulman G.L. Neuron. 1998; 21: 761-773Abstract Full Text Full Text PDF PubMed Scopus (1217) Google Scholar). One of the most prominent areas that is activated by both processes is the FEF (Bruce et al., 2004Bruce C.J. Friedman H.R. Kraus M.S. Stanton G.B. Chalupa L.M. Werner J.S. The Visual Neurosciences. The MIT Press, Cambridge, MA2004: 1428-1448Google Scholar). Although functional imaging studies have suggested that the attentional and saccade generation functions are identical in FEF, single-neuron recordings in monkey FEF have demonstrated that these two functions are associated with activity in different neural populations. In a seminal study, Sato and Schall recorded from FEF neurons while monkeys were presented with a rectangle and several distractors in the periphery (Sato and Schall, 2003Sato T.R. Schall J.D. Neuron. 2003; 38: 637-648Abstract Full Text Full Text PDF PubMed Scopus (199) Google Scholar). The rectangle's orientation provided the instruction whether to look toward it or to make an antisaccade away from it to the opposite side. Sato and Schall were able to separate FEF neurons into two types. Type I initially indicated the location of the rectangle, and in most cases, later indicated the target for the antisaccade, whereas type II neurons only signaled the target location for the antisaccade. Sato and Schall suggested that type I neurons form part of an attentional saliency map that signals the location of relevant stimuli, whereas type II neurons code the motor command for the saccade. This functional distinction was also supported by the close relationship between the neural activity of type II neurons and saccadic reaction times, which was absent for type I neurons. Interestingly, this separation into type I and type II neurons did not tightly correspond to the traditional separation into visual and motor neurons, as some of the type II neurons were classified as purely visual neurons. Further, Thompson and colleagues (Thompson et al., 2005Thompson K.G. Biscoe K.L. Sato T.R. J. Neurosci. 2005; 25: 9479-9487Crossref PubMed Scopus (287) Google Scholar) reported recently that motor neurons in FEF are not activated in a purely attention task. Although these studies have supported a functional dissociation between attention- and saccade-related signals in FEF, it remained unknown how these two systems interact during the planning of visually guided saccades. In this issue of Neuron, Schafer and Moore (Schafer and Moore, 2007Schafer R.J. Moore T. Neuron. 2007; 56 (this issue): 541-551Abstract Full Text Full Text PDF PubMed Scopus (64) Google Scholar) utilized a known visual illusion to investigate this interaction between spatial attention and saccade generation in monkey FEF. When human subjects are presented with a flashed stimulus near a moving grating, the perceived position of the flash is shifted in the direction of grating motion (Whitney, 2002Whitney D. Trends Cogn. Sci. 2002; 6: 211-216Abstract Full Text Full Text PDF PubMed Scopus (158) Google Scholar). Similarly, when instructed to make saccades toward a moving grating, saccades of humans and monkeys deviate away from the center of the grating in the direction of motion, consistent with the apparent position illusion. Schafer and Moore tested what happens when the activity of FEF neurons that generate saccade commands toward the center of the grating is artificially enhanced. To do this, the authors first determined the center of the movement field of a given site in FEF by applying electrical microstimulation that was sufficient to evoke a saccade. Electrical microstimulation at a given FEF site evokes fixed-vector saccades, i.e., the direction and amplitude of the evoked saccade is independent of initial eye position (Bruce et al., 2004Bruce C.J. Friedman H.R. Kraus M.S. Stanton G.B. Chalupa L.M. Werner J.S. The Visual Neurosciences. The MIT Press, Cambridge, MA2004: 1428-1448Google Scholar). Schafer and Moore then proceeded to the experimental paradigm. The monkeys began by fixating the central spot and were then presented with two moving gratings. One of the gratings was always presented at the center of the identified movement field. In order to obtain a reward, the monkeys simply had to make a saccade to one of the gratings. A sophisticated reward schedule ensured that the monkeys balanced their target choices. On half of the trials, the authors applied a subthreshold level of microstimulation, i.e., not sufficient to evoke a saccade, at the time when the gratings appeared. The first and predicted result was that the monkeys selected the grating in the movement field more often on microstimulation trials. This is consistent with both a stimulation-induced attentional and motor bias. Furthermore, both monkeys showed a deviation of their saccades away from the grating's center in the direction of the motion on control trials, an effect consistent with the apparent position illusion. The crucial test was then what would happen on stimulation trials. Previous studies predicted that microstimulation would reduce the deviation by imposing a competing saccade goal toward the center of the movement field (Schiller and Sandell, 1983Schiller P.H. Sandell J.H. Exp. Brain Res. 1983; 49: 381-392Crossref PubMed Scopus (137) Google Scholar). Surprisingly, Schafer and Moore observed the opposite effect. On stimulation trials, saccades deviated more strongly away from the movement field in the direction of the grating's motion. Therefore, subthreshold FEF microstimulation enhanced the apparent position illusion and did not bias a saccade toward the movement field. Schafer and Moore's study does not refute a functional separation between spatial attention and saccade commands in FEF (Sato and Schall, 2003Sato T.R. Schall J.D. Neuron. 2003; 38: 637-648Abstract Full Text Full Text PDF PubMed Scopus (199) Google Scholar, Thompson et al., 2005Thompson K.G. Biscoe K.L. Sato T.R. J. Neurosci. 2005; 25: 9479-9487Crossref PubMed Scopus (287) Google Scholar), but rather indicates that spatial attention influences the saccade function of FEF. Although the mechanism by which subthreshold FEF stimulation leads to an increase in the motion-induced bias is presently unknown, the authors hypothesize that FEF stimulation enhances motion signals in the visual cortex via top-down signals that then influence the localization of the target stimulus, ultimately altering the saccade command in the FEF (Figure 1). In this model, the motion-induced bias does not originate within the FEF, but in visual areas that receive an increased attentional signal from the FEF on microstimulation trials. This model is convincing because it is consistent with the finding that subthreshold FEF stimulation leads to better visual discrimination in the movement field (Moore and Fallah, 2004Moore T. Fallah M. J. Neurophysiol. 2004; 91: 152-162Crossref PubMed Scopus (342) Google Scholar) and the observation that FEF microstimulation enhances activity in visual area V4, which is reminiscent of an attentional effect (Moore and Armstrong, 2003Moore T. Armstrong K.M. Nature. 2003; 421: 370-373Crossref PubMed Scopus (792) Google Scholar). The authors' model further highlights the emerging view that microstimulation of a brain area does not simply modulate activity at the tip of the microelectrode, but also induces activity changes in distantly connected brain regions. Taken together, these data are exciting, because they demonstrate that attention and action interact more closely in the FEF than previously thought, and they suggest a mechanism by which attention can modulate saccade motor commands. Of course, many interesting questions will have to await future investigations. For example, it may be that the position illusion alters the saccade command not in the FEF, but in an area downstream of the FEF. Such a dissociation between the motor signal and saccade metric has been found for saccades to remembered stimuli (Stanford and Sparks, 1994Stanford T.R. Sparks D.L. Vision Res. 1994; 34: 93-106Crossref PubMed Scopus (83) Google Scholar) and for saccades to moving targets in the superior colliculus (Keller et al., 1996Keller E.L. Gandhi N.J. Weir P.T. J. Neurophysiol. 1996; 76: 3573-3577PubMed Google Scholar). Another open question is whether this effect is specific to the FEF or whether attentional signals change saccade commands in other cortical or subcortical areas as well. An obvious candidate would be the superior colliculus, whose activity has been linked to both saccade generation and attention (Ignashchenkova et al., 2004Ignashchenkova A. Dicke P.W. Haarmeier T. Thier P. Nat. Neurosci. 2004; 7: 56-64Crossref PubMed Scopus (280) Google Scholar). Schafer and Moore's study invites us to attend to and act on these questions. Attention Governs Action in the Primate Frontal Eye FieldSchafer et al.NeuronNovember 08, 2007In BriefWhile the motor and attentional roles of the frontal eye field (FEF) are well documented, the relationship between them is unknown. We exploited the known influence of visual motion on the apparent positions of targets, and measured how this illusion affects saccadic eye movements during FEF microstimulation. Without microstimulation, saccades to a moving grating are biased in the direction of motion, consistent with the apparent position illusion. Here we show that microstimulation of spatially aligned FEF representations increases the influence of this illusion on saccades. Full-Text PDF Open Archive" @default.
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• W1990602625 date "2007-11-01" @default.
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• W1990602625 title "Where Do I look? From Attention to Action in the Frontal Eye Field" @default.
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