A cortical zoom-in operation underlies covert shifts of visual spatial attention

Abstract

Shifting the focus of attention without moving the eyes poses challenges for signal coding in visual cortex in terms of spatial resolution, signal routing, and cross-talk. Little is known how these problems are solved during focus shifts. Here, we analyze the spatiotemporal dynamic of neuromagnetic activity in human visual cortex as a function of the size and number of focus shifts in visual search. We find that large shifts elicit activity modulations progressing from highest (IT) through mid-level (V4) to lowest hierarchical levels (V1). Smaller shifts cause those modulations to start at lower levels in the hierarchy. Successive shifts involve repeated backward progressions through the hierarchy. We conclude that covert focus shifts arise from a cortical coarse-to-fine process progressing from retinotopic areas with larger toward areas with smaller receptive fields. This process localizes the target and increases the spatial resolution of selection, which resolves the above issues of cortical coding.

Fig. 1.. Experimental design.

In three experiments, participants performed different versions of a search task for a colored item, reporting its orientation (“C,” site of gap; bars, vertical, diagonal, or horizontal) via button press. Gray circles illustrate the focus of spatial attention, and gray dashed arrows illustrate its shift. (A) Experiment 1. Permanent placeholders (black rectangles) demarcated positions of upcoming stimuli (1 to 4). Endogenous cues (black arrows) informed participants every 10 trials about the current experimental focusing condition. The cue could be uninformative (search condition) or point to the visual hemifield of the upcoming target (here, red C), allowing for prefocusing (focus condition). (B) Experiment 2. Focus condition as in experiment 1 (focus-valid), except that, on 25% of the trials, the target appeared in the uncued hemifield (focus-invalid). Position task (position): Target appeared at the indicated item position (one of four) together with a differently colored distractor item. At the mirror position, an analogous two-color distractor was shown. (C) Experiment 3. Similar to search condition of experiment 1 but without placeholders or uninformative cues. On half of the blocks, participants were instructed to report the orientation of the color-defined target (single). On the remaining trial blocks, they had to use the orientation direction of the color target (T1) to shift their attention to a second target (T2) and report its orientation (sequential). Note that the exact size and distance of the search items shown in the figure differ from how they were presented during the experiment.

Fig. 2.. Results of experiment 1.

(A) N2pc waveforms of the search (thick solid line) and focus condition (thick dashed line). Below the waveforms, the time course of P values determined by tANOVAs (see Materials and Methods) testing the N2pc of the search (thin solid line) and focus (thin dashed line) conditions. The light gray horizontal dashed line marks the threshold of statistical significance. Significant time ranges in the N2pc difference are highlighted by black (search) and dashed (focus) horizontal bars below the waveforms. (B) Magnetic field distributions of the N2pc at early (220 ms) and late (270 ms) time points after stimulus onset. The black circles (search condition) mark the maximum efflux-influx field transition zone (red-to-blue field lines) that moves from a more anterior lateral region (difference between sensors b and a) to a posterior medial region (difference between sensors b and c). (C) CSD maps (views onto the basal brain) showing the N2pc sources of the search and focus conditions in early (220 ms) and late (270) time ranges corresponding to the field maps in (B) as well as at 290 ms (views at the mesial brain). The CSDs are arbitrarily thresholded (see Materials and Methods) to best illustrate the cortical localization of the source maxima. (D) Locations of source maxima in individual subjects in three consecutive time ranges (190 to 230 ms, red dots; 230 to 270 ms, green dots; 270 to 310 ms, blue dots) spanning the N2pc response. The red (green) lines connect corresponding 190- to 230-ms (230- to 270-ms) with the 230- to 270-ms (270- to 310-ms) maxima of individual subjects.

Fig. 3.. Summary of CSDs across experiments.

CSD distributions of the early (blue and red) and late N2pc sources (turquoise and orange) overlaid onto probabilistic maps of retinotopic visual areas (V1, hV4, VO-1, and VO-2). The latter are shown as yellow and blue areas rendered onto a cortex segmentation of the MNI152 (center). (A and B) Results of experiments 1 and 2. (C and D) Results of the single and sequential conditions of experiment 3.

Fig. 4.. Within-cued quadrant analysis (experiment 1).

Left: Source estimates of the response difference elicited by a target in the top left minus the bottom right item position in the bottom left visual quadrant of the focus condition. Right: Response difference elicited by a target in the bottom left minus the top right item position in the bottom right visual quadrant.

Fig. 5.. Results of experiment 2.

(A) N2pc waveforms of the focus-valid (thick solid line), focus-invalid (thick dashed line), and position (thick gray line) conditions together with the corresponding time courses of P values testing the N2pc for each condition. The horizontal dotted line marks the threshold of statistical significance. Significant time ranges in the N2pc difference are highlighted by black (focus-valid), dashed (focus-invalid), and gray (position) horizontal bars below the waveforms. (B) CSD maps showing the N2pc sources of the focus-invalid (top row), focus-valid (middle row), and position condition (bottom row) at selected time points after stimulus onset.

Fig. 6.. Results of experiment 3.

(A) N2pc waveforms and statistical validation of the N2pc elicited in the single (thick solid line) and sequential condition (thick dashed line). The diagram added below the waveforms replots the response of the response between 300 and 700 ms with reference to a baseline activity between 300 and 400 ms (gray horizontal bar). The second N2pc of the sequential condition (N2pc2) is highlighted as red area under the curve. (B) CSD maps showing the N2pc sources of the single (top row) and sequential condition (bottom row) at selected time points after stimulus onset. (C) Time course of the CSD estimates in an ROI in early visual cortex (white circle) of the single (solid line) and sequential condition (dashed line). Source activity reflecting the second N2pc of the sequential condition is highlighted in red.