Attention to Color Sharpens Neural Population Tuning via Feedback Processing in the Human Visual Cortex Hierarchy

Abstract

Attention can facilitate the selection of elementary object features such as color, orientation, or motion. This is referred to as feature-based attention and it is commonly attributed to a modulation of the gain and tuning of feature-selective units in visual cortex. Although gain mechanisms are well characterized, little is known about the cortical processes underlying the sharpening of feature selectivity. Here, we show with high-resolution magnetoencephalography in human observers (men and women) that sharpened selectivity for a particular color arises from feedback processing in the human visual cortex hierarchy. To assess color selectivity, we analyze the response to a color probe that varies in color distance from an attended color target. We find that attention causes an initial gain enhancement in anterior ventral extrastriate cortex that is coarsely selective for the target color and transitions within ∼100 ms into a sharper tuned profile in more posterior ventral occipital cortex. We conclude that attention sharpens selectivity over time by attenuating the response at lower levels of the cortical hierarchy to color values neighboring the target in color space. These observations support computational models proposing that attention tunes feature selectivity in visual cortex through backward-propagating attenuation of units less tuned to the target.SIGNIFICANCE STATEMENT Whether searching for your car, a particular item of clothing, or just obeying traffic lights, in everyday life, we must select items based on color. But how does attention allow us to select a specific color? Here, we use high spatiotemporal resolution neuromagnetic recordings to examine how color selectivity emerges in the human brain. We find that color selectivity evolves as a coarse to fine process from higher to lower levels within the visual cortex hierarchy. Our observations support computational models proposing that feature selectivity increases over time by attenuating the responses of less-selective cells in lower-level brain areas. These data emphasize that color perception involves multiple areas across a hierarchy of regions, interacting with each other in a complex, recursive manner.

Keywords: MEG; color; extrastriate cortex; feature-based attention; selective tuning.

Figure 1.

Experimental design. A, FBA experiment. On each trial, the subjects were presented a bicolored target circle in the LVF and a task-irrelevant color probe in the RVF. Subjects were asked to report whether the red half-circle appeared at the left or right side of the circle. The probe in the RVF varied randomly between different red and purple hues spanning from focal red (R0) to focal purple (P6). The brain response elicited by the color probe was analyzed as a function of color distance to the target red. B, Control experiments. Left, Control Experiment 1: Attention was drawn away from the color target by presenting an RSVP stream at fixation. Subjects ignored the colored circles and reported whether the RSVP stream contained the character “O” (present in 50% of the trials) or not. Right, Control Experiment 2: Subjects fixated the central cross, ignored the colored circles, and reported whether the small black bar superimposed on the target circle was tilted clockwise or counterclockwise from vertical. C, Behavioral color categorization test. While fixating subjects covertly attended to the RVF, each trial started with the presentation of two circles (drawn in R0 and P6), which served as a color reference, before a unicolored circle was presented for 300 ms. Subjects reported whether the circle was a red or a purple. D, Behavioral data of the color categorization test. Error bars indicate SEM. Independent of the partition of the color range, the subjects set the categorical border somewhere between R3 (classified as red) and P4 (classified as purple).

Figure 2.

Magnetic field maps and source localization results of the FBA experiment (overall response). A, Field maps and corresponding current source density distributions of the average FBA response at three selected time points (130 ms, orange; 230 ms, blue; and 320 ms, green) after probe onset. The black ellipses highlight the magnetic field components (efflux–influx configurations, red–blue) that give rise to the current source maxima visible in the 3D CSD maps. B, Time course of average CSD estimates in ROIs (blue/green dots in the 3D map) corresponding with the anterior (blue) and posterior ventral extrastriate maximum (green) of the FBA response. The colored windows mark the early and late time ranges that served to analyze the FBA response in ventral extrastriate cortex as a function of probe color distance. Blue marks the time range (205–275 ms) during which source activity in the anterior ROI reached the temporal maximum and was stronger than in the posterior ROI. Green highlights the time range (275–390 ms) during which source activity in the posterior ROI showed a temporal maximum and was stronger than the anterior ROI.

Figure 3.

Magnetic response as a function of probe color distance (FBA experiment). A–C, Difference waveforms (probe color minus P6 difference) at selected sensor sites representing the initial response in early visual cortex (A) and the subsequent response in anterior (B) and in posterior ventral extrastriate cortex (C). Black horizontal bars index the time range of significant overall response differences between probe colors (time-sliding one-way seven-level rANOVA; see Materials and Methods). The colored windows highlight the time range in which response averages, shown in the bar plots on the right, were computed. Window averages of the 110–150 ms, 205–275 ms, and 275–390 ms range are plotted in orange, blue, and green, respectively. Error bars indicate SEM.

Figure 4.

Cluster validity analysis (FBA experiment). A, 3D maps showing maxima of cluster validity (silhouette values, blue) for a given membership assignment testing coarse selectivity for R0 ([R0,R1,R2,R3,P4] [P5,P6], left) versus sharpened selectivity for R0 ([R0,R1,R2,R3,] [P4,P5,P6], right). The overlaid dashed outlines mark the extension of areas hV4 (red), VO-1 (yellow), and PHC-2 (orange). The outlines highlight probabilistic distributions (shown on the far right) derived from a subset of eight subjects participating in the reported experiments (hV4, VO-1) or from the probabilistic atlas of topographically defined visual areas (PHC-2) (Wang et al., 2015). B, Time course of the average cluster validity in ROIs defined by the anterior (blue dots, solid blue trace) and posterior (white dots, dashed blue trace) silhouette maximum shown in A.

Figure 5.

Results of Control Experiment 1. A, Magnetic field maps and corresponding current source density distributions of the average probe response at 150 ms (orange), 230 ms (blue), and 320 ms (green) after probe onset. B–D, Magnetic difference waveforms (probe color minus P6 difference) for each probe color distance at selected sensor sites corresponding with the response in early visual cortex (B) and in anterior (C) and posterior (D) ventral extrastriate cortex. Black horizontal bars index the time range of significant response differences (time-sliding one-way five-level ANOVA; see Materials and Methods). The colored windows highlight the time ranges (defined in the FBA experiment) for which response averages are plotted on the right. Orange, blue, and green bar plots show window averages in the 110–150 ms, 205–275 ms, and 275–390 ms time range, respectively. The colored circles replot window averages of the FBA experiment (Fig. 3) for comparison. Error bars indicate SEM.

Figure 6.

Results of Control Experiment 2. A, Magnetic field maps and CSD distributions of the average probe response at 130 ms (orange), 230 ms (blue), and 320 ms (green) after probe onset. B–D, Difference waveforms (probe color minus P6) for each probe color distance at selected sensor sites corresponding with the response in early visual cortex (B), in anterior (C) and posterior (D) ventral extrastriate cortex. Black horizontal bars highlight the time range of significant response differences (time-sliding one-way five-level ANOVA; see Materials and Methods). The colored windows mark the time range (defined in the FBA experiment) for which response averages are plotted on the right. Orange, blue, and green bar plots show window averages in the 110–150 ms, 205–275 ms, and 275–390 ms time range, respectively. The colored circles replot window averages of the FBA experiment (Fig. 3) for comparison. Error bars indicate SEM.