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      Human gaze tracks attentional focusing in memorized visual space

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      1 , * , 1 , 2 , 1 , 2
      Nature human behaviour

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          Abstract

          Brain areas that control gaze are also recruited for covert shifts of spatial attention 19. In the external space of perception, there is a natural, ecological link between the control of gaze and of spatial attention, since information sampled at covertly attended locations can inform where to look next 2, 10, 11. Attention can also be directed internally to representations held within the spatial layout of visual working memory 1216. In such cases, the incentive for using attention to direct gaze disappears since there are no external targets to scan. Here we investigate whether the brain’s oculomotor system also participates in attention within the internal space of memory. Paradoxically, we reveal this participation through gaze behaviour itself. We demonstrate that selecting an item from visual working memory biases gaze in the direction of the memorised location of that item – despite there being nothing to look at and even though location memory was never explicitly probed. This retrospective ‘gaze bias’ occurs only when an item is not already in the internal focus of attention, and predicts the performance benefit associated with the focusing of internal attention. We conclude that the oculomotor system also participates in the focusing of attention within memorised space, leaving traces all the way to the eyes.

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          Most cited references36

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          Saccade target selection and object recognition: evidence for a common attentional mechanism.

          The spatial interaction of visual attention and saccadic eye movements was investigated in a dual-task paradigm that required a target-directed saccade in combination with a letter discrimination task. Subjects had to saccade to locations within horizontal letter strings left and right of a central fixation cross. The performance in discriminating between the symbols "E" and "E", presented tachistoscopically before the saccade within the surrounding distractors was taken as a measure of visual attention. The data show that visual discrimination is best when discrimination stimulus and saccade target refer to the same object; discrimination at neighboring items is close to chance level. Also, it is not possible, in spite of prior knowledge of discrimination target position, to direct attention to the discrimination target while saccading to a spatially close saccade target. The data strongly argue for an obligatory and selective coupling of saccade programming and visual attention to one common target object. The results favor a model in which a single attentional mechanism selects objects for perceptual processing and recognition, and also provides the information necessary for motor action.
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            Selective gating of visual signals by microstimulation of frontal cortex.

            Several decades of psychophysical and neurophysiological studies have established that visual signals are enhanced at the locus of attention. What remains a mystery is the mechanism that initiates biases in the strength of visual representations. Recent evidence argues that, during spatial attention, these biases reflect nascent saccadic eye movement commands. We examined the functional interaction of saccade preparation and visual coding by electrically stimulating sites within the frontal eye fields (FEF) and measuring its effect on the activity of neurons in extrastriate visual cortex. Here we show that visual responses in area V4 could be enhanced after brief stimulation of retinotopically corresponding sites within the FEF using currents below that needed to evoke saccades. The magnitude of the enhancement depended on the effectiveness of receptive field stimuli as well as on the presence of competing stimuli outside the receptive field. Stimulation of non-corresponding FEF representations could suppress V4 responses. The results suggest that the gain of visual signals is modified according to the strength of spatially corresponding eye movement commands.
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              Reorienting attention across the horizontal and vertical meridians: Evidence in favor of a premotor theory of attention

              Stimuli presented in a non-attended location are responded to much slower than stimuli presented in an attended one. The hypotheses proposed to explain this effect make reference to covert movement of attention, hemifield inhibition, or attentional gradients. The experiment reported here was aimed at discriminating among these hypotheses. Subjects were cued to attend to one of four possible stimulus locations, which were arranged either horizontally or vertically, above, below, to the right or left of a fixation point. The instructions were to respond manually as fast as possible to the occurrence of a visual stimulus, regardless of whether it occurred in a cued or in a non-cued location. In 70% of the cued trials the stimulus was presented in the cued location and in 30% in one of the non-cued locations. In addition there were trials in which a non-directional cue instructed the subject to pay attention to all four locations. The results showed that the correct orienting of attention yielded a small but significant benefit; the incorrect orienting of attention yielded a large and significant cost; the cost tended to increase as a function of the distance between the attended location and the location that was actually stimulated; and an additional cost was incurred when the stimulated and attended locations were on opposite sides of the vertical or horizontal meridian. We concluded that neither the hypothesis postulating hemifield inhibition nor that postulating movement of attention with a constant time can explain the data. The hypothesis of an attention gradient and that of attention movements with a constant speed are tenable in principle, but they fail to account for the effect of crossing the horizontal and vertical meridians. A hypothesis is proposed that postulates a strict link between covert orienting of attention and programming explicit ocular movements. Attention is oriented to a given point when the oculomotor programme for moving the eyes to this point is ready to be executed. Attentional cost is the time required to erase one ocular program and prepare the next one.
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                Author and article information

                Journal
                101697750
                Nat Hum Behav
                Nat Hum Behav
                Nature human behaviour
                2397-3374
                6 February 2019
                04 March 2019
                May 2019
                04 September 2019
                : 3
                : 5
                : 462-470
                Affiliations
                [1 ]Oxford Centre for Human Brain Activity, Wellcome Centre for Integrative Neuroimaging, Department of Psychiatry, University of Oxford
                [2 ]Department of Experimental Psychology, University of Oxford
                Author notes
                [* ]Corresponding author: Dr Freek van Ede - frederik.vanede@ 123456ohba.ox.ac.uk
                Article
                EMS81525
                10.1038/s41562-019-0549-y
                6546593
                31089296
                8647f2ad-695c-44d4-b8a6-b9bc6a818975

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