Visual and oculomotor selection: links, causes and implications for spatial attention

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Natural scenes contain far more information than can be processed simultaneously. Thus, our visually guided behavior depends crucially on the capacity to attend to relevant stimuli. Past studies have provided compelling evidence of functional overlap of the neural mechanisms that control spatial attention and saccadic eye movements. Recent neurophysiological work demonstrates that the neural circuits involved in the preparation of saccades also play a causal role in directing covert spatial attention. At the same time, other studies have identified separable neural populations that contribute uniquely to visual and oculomotor selection. Taken together, all of the recent work suggests how visual and oculomotor signals are integrated to simultaneously select the visual attributes of targets and the saccades needed to fixate them.

Introduction

Visually guided behavior depends first and foremost on the ability to construct an accurate representation of the many objects within the visual environment. In turn, because of the precipitous drop in acuity that occurs with increasing retinal eccentricity, visual perception in foveate animals relies upon the sequential scanning of the items within a scene by way of saccadic eye movements. Thus, the construction of an accurate visual representation depends crucially on the optimal and precise selection of successive fixation locations [1].

Recent evidence suggests that the visuo-oculomotor system of primates has evolved to select the visual parameters of objects concurrently with the specification of oculomotor commands needed to fixate those objects. Further evidence suggests that this system has evolved the capacity to amplify target visual signals covertly in the absence of the overt deployment of eye movements. Although the neural mechanisms involved in the triggering of visually guided saccades and those involved in covert attention must diverge at the point where eye movements are either made or withheld, results to date suggest considerable overlap of the circuits mediating both functions (e.g. [2]).

Here we review recent studies of the relationship between visual selection and oculomotor programming. These experiments reveal a causal relationship between the neural circuits controlling saccadic eye movements and shifts of covert spatial attention. Although some studies have identified separable neural populations that contribute uniquely to visual selection or oculomotor programming, recent work suggests how these processes might be integrated during visually guided behavior.

Section snippets

Links between selective attention and saccadic programming

Psychophysical evidence linking selective attention and oculomotor programming is abundant. A classic demonstration of the influence of directed attention on saccades was provided by Rizzolatti and colleagues [3]. This study examined the influence of covert attention on saccade trajectories in subjects instructed to initiate saccades to a location in one-half of the visual field (e.g. the lower half) according to cues presented in the other half. The cues themselves could be presented in one of

Causal mechanisms of spatial selective attention

If you are instructed to continue reading this text while preparing to detect the occurrence of some visual event in one corner of the page (e.g. a change in page number), your ability to detect the event would be heightened in comparison to a situation in which you had not been given those instructions. This is despite the fact that in neither case should your gaze shift to the corner of the page. In the macaque brain, the visual and oculomotor systems are highly interconnected, with cortical

Heterogeneous neural populations and implications for neurophysiological models of spatial attention

Despite evidence of a causal role of oculomotor circuits in the deployment of visual spatial attention, it remains to be seen to what extent particular neurons within those circuits contribute directly to both oculomotor behavior and visual selection. As stated earlier, by definition, covert attention requires at some level the divergence of neural mechanisms controlling visual filtering and the triggering of orienting behaviors. But where in the visuo-oculomotor axis does neural activity have

Top-down versus bottom-up control of attention

Although these electrophysiological studies provide evidence of functional heterogeneity at the single neuron level within the FEF and SC, one common characteristic deserves further comment. In each of the studies, covert shifts of spatial attention were elicited towards locations that had a high bottom-up salience. That is, spatial attention was shifted towards an object that had a unique color or shape 41, 42, 43 or towards the abrupt onset of a peripheral cue [44]. Past research has

Concluding remarks

Does the recent neurophysiological evidence confirm or weaken motor-based theories of attention, such as the premotor theory [3]? It can be said that the evidence appears to do both. Increasing the probability that a visual target will be foveated by electrically stimulating oculomotor structures, such as the FEF or the SC, concomitantly increases the probability that visual events at the target location will be detected. Furthermore, the perceptual improvements seen with electrical

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