More direct evidence for the idea that attention shifts are planned in oculomotor coordinates comes from stimulation experiments performed by Kustov and Robinson in the deep layers of the superior colliculus (52). They trained monkeys in a spatially cued oculomotor task, in which visual locations were cued peripherally by a sensory stimulus or symbolically by a change in color of the fixation point. Saccadic reaction times for cued locations were faster than for uncued locations both for sensory (exogenous) and symbolic (endogenous) cueing. During the task, electrical stimulation with microcurrents was applied to certain portions of the deep layers of the superior colliculus. Normally, this stimulation produces a saccadic eye movement of constant direction and amplitude. When the monkey was cued to a location, the stimulation produced a displacement of the constant saccadic vector in the direction of the cued location. This displacement occurred with both types of cues. Similar deviations of the eye movements evoked from the stimulation of the superior colliculus occurred during new symbolic and sensory cueing tasks, in which the monkey maintained central fixation and responded to the probe stimuli with a manual response only. Hence, attentional shifts that are independent of eye movements still lead to the modification of the evoked saccades. The simpler explanation for these findings is that attentional signals during spatial cueing are oculomotor in nature and coded in motor coordinates. Alternatively, they represent an epiphenomenon of no functional significance, i.e., a “spillover” of activity from cognitive circuits. This spillover, however, could be potentially detrimental to performance because the precision of an eye movement would be affected by the direction of attention. Unlikely, such an interference would have not been corrected during evolution.
This review highlights psychological, functional anatomical, and cellular levels of analysis of a relatively simple visual behavior such as visual orienting. There are two main conclusions that can be derived from this body of results. First, there appears to be a robust set of neural signals in parietal cortex (and frontal cortex) indexed both with neuroimaging and electrophysiological methods that clearly reflects spatial attentional processes during covert orienting. These signals can be reasonably linked to some of the psychological effects described when subjects (human or monkeys) reflexively or voluntarily allocate attention to a visual location/object. These neural signals are the source of a selective location signal that biases visual processing in ventral visual areas related to object analysis. Second, psychological, functional anatomical, and neuronal analyses indicate that attentional processes are tightly linked to oculomotor processes. An extreme view of this functional relationship is that attentional shifts are oculomotor in nature, i.e., being planned within oculomotor circuits in motor coordinates (amplitude, direction). This view is supported by the following results. (i) In dual-task conditions in which eye movement and attention are cued to opposite locations, the focus of processing is obligatorily linked to the eye movement. (ii) Neuronal signals related to covert (attentional) orienting have been recorded both in humans and monkeys in areas such as FEF and deep layers of the superior colliculus in monkeys that are essential nodes of the oculomotor system. (iii) The patterns of cortical activation for attention and eye movement overlap in our metaanalysis of functional imaging studies, (iv) In parietal cortex, the same neurons that show purely attentional modulations also code oculomotor parameters. A more moderate view of the relationship between attention and eye movement is that their processes are interdependent. This view is supported by: (i) a relative slowing of saccades when attention is oriented elsewhere: (ii) the partial segregation of regions for attention and eye movement in our metaanalysis; and (iii) some neural models of parietal function that emphasize sensory and attentional functions and deemphasize visuomotor functions. Finally, the hypothesis that attention and eye movements are segregated processes can be rejected on the basis of the current anatomical and physiological evidence.
I thank Gordon Shulman for discussion and careful reading of a draft of the manuscript, and Marc Raichle and Steve Petersen for enthusiastic support. This work was supported by National Institutes of Health Grant K08-EY00379–01, and the Charles A.Dana Foundation.
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