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      A Common Network of Functional Areas for Attention and Eye Movements

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          Abstract

          Functional magnetic resonance imaging (fMRI) and surface-based representations of brain activity were used to compare the functional anatomy of two tasks, one involving covert shifts of attention to peripheral visual stimuli, the other involving both attentional and saccadic shifts to the same stimuli. Overlapping regional networks in parietal, frontal, and temporal lobes were active in both tasks. This anatomical overlap is consistent with the hypothesis that attentional and oculomotor processes are tightly integrated at the neural level.

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          Most cited references49

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          A cortical network for directed attention and unilateral neglect.

          Unilateral neglect reflects a disturbance in the spatial distribution of directed attention. A review of unilateral neglect syndromes in monkeys and humans suggests that four cerebral regions provide an integrated network for the modulation of directed attention within extrapersonal space. Each component region has a unique functional role that reflects its profile of anatomical connectivity, and each gives rise to a different clinical type of unilateral neglect when damaged. A posterior parietal component provides an internal sensory map and perhaps also a mechanism for modifying the extent of synaptic space devoted to specific portions of the external world; a limbic component in the cingulate gyrus regulates the spatial distribution of motivational valence; a frontal component coordinates the motor programs for exploration, scanning, reaching, and fixating; and a reticular component provides the underlying level of arousal and vigilance. This hypothetical network requires at least three complementary and interacting representations of extrapersonal space: a sensory representation in posterior parietal cortex, a schema for distributing exploratory movements in frontal cortex, and a motivational map in the cingulate cortex. Lesions in only one component of this network yield partial unilateral neglect syndromes, while those that encompass all the components result in profound deficits that transcend the mass effect of the larger lesion. This network approach to the localization of complex functions offers an alternative to more extreme approaches, some of which stress an exclusive concentration of function within individual centers in the brain and others which advocate a more uniform (equipotential or holistic) distribution. In human beings, unilateral neglect syndromes are more frequent and severe after lesions in the right hemisphere. Also, right hemisphere mechanisms appear more effective in the execution of attentional tasks. Furthermore, the attentional functions of the right hemisphere span both hemispaces, while the left hemisphere seems to contain the neural apparatus mostly for contralateral attention. This evidence indicates that the right hemisphere of dextrals has a functional specialization for the distribution of directed attention within extrapersonal space.
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            The role of attention in the programming of saccades.

            Accurate saccadic programming in natural visual scenes requires a signal designating which of the many potential targets is to be the goal of the saccade. Is this signal controlled by the allocation of perceptual attention, or do saccades have their own independent selective filter? We found evidence for the involvement of perceptual attention, namely: (1) summoning perceptual attention to a target also facilitated saccades; (2) perceptual identification was better at the saccadic goal than elsewhere; and (3) attempts to dissociate the locus of attention from the saccadic goal were unsuccessful, i.e. it was not possible to prepare to look quickly and accurately at one target while at the same time making highly accurate perceptual judgements about targets elsewhere. We also studied the trade-off between saccadic and perceptual performance by means of a novel application of the "attentional operating characteristic" (AOC) to oculomotor performance. This analysis revealed that some attention could be diverted from the saccadic goal with virtually no cost to either saccadic latency or accuracy, showing that there is a ceiling on the attentional demands of saccades. The links we discovered between saccades and attention can be explained by a model in which perceptual attention determines the endpoint of the saccade, while a separate trigger signal initiates the saccade in response to transient changes in the attentional locus. The model will be discussed in the context of current neurophysiological work on saccadic control.
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              The role of visual attention in saccadic eye movements.

              The relationship between saccadic eye movements and covert orienting or visual spatial attention was investigated in two experiments. In the first experiment, subjects were required to make a saccade to a specified location while also detecting a visual target presented just prior to the eye movement. Detection accuracy was highest when the location of the target coincided with the location of the saccade, suggesting that subjects use spatial attention in the programming and/or execution of saccadic eye movements. In the second experiment, subjects were explicitly directed to attend to a particular location and to make a saccade to the same location or to a different one. Superior target detection occurred at the saccade location regardless of attention instructions. This finding shows that subjects cannot move their eyes to one location and attend to a different one. The result of these experiments suggest that visuospatial attention is an important mechanism in generating voluntary saccadic eye movements.
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                Author and article information

                Journal
                Neuron
                Neuron
                Elsevier BV
                08966273
                October 1998
                October 1998
                : 21
                : 4
                : 761-773
                Article
                10.1016/S0896-6273(00)80593-0
                9808463
                365c814d-331d-469d-997a-1d56b2b460a8
                © 1998

                https://www.elsevier.com/tdm/userlicense/1.0/

                https://www.elsevier.com/open-access/userlicense/1.0/

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