Cortical Mechanisms of Prioritizing Selection for Rejection in Visual Search

Abstract

In visual search, the more one knows about a target, the faster one can find it. Surprisingly, target identification is also faster with knowledge about distractor-features. The latter is paradoxical, as it implies that to avoid the selection of an item, the item must somehow be selected to some degree. This conundrum has been termed the "ignoring paradox", and, to date, little is known about how the brain resolves it. Here, in data from four experiments using neuromagnetic brain recordings in male and female humans, we provide evidence that this paradox is resolved by giving distracting information priority in cortical processing. This attentional priority to distractors manifests as an enhanced early neuromagnetic index, which occurs before target-related processing, and regardless of distractor predictability. It is most pronounced on trials for which a response rapidly occurred, and is followed by a suppression of the distracting information. These observations together suggest that in visual search items cannot be ignored without first being selected.SIGNIFICANCE STATEMENT How can we ignore distracting stimuli in our environment? To do this successfully, a logical hypothesis is that as few neural resources as possible should be devoted to distractor processing. Yet, to avoid devoting resources to a distractor, the brain must somehow mark what to avoid; this is a philosophical problem, which has been termed the "ignoring paradox" or "white bear phenomenon". Here, we use MEG recordings to determine how the human brain resolves this paradox. Our data show that distractors are not only processed, they are given temporal priority, with the brain building a robust representation of the to-be-ignored items. Thus, successful suppression of distractors can only be achieved if distractors are first strongly neurally represented.

Keywords: human; ignoring paradox; magnetoencephalography; visual attention; visual search.

Figure 1.

Stimulus setup and structure of trial-block sequence. a, Example search frames in Experiment 1. Each search frame contained four neutral distractors (blue Ts), one target (red T) and one distractor item (green T). To isolate the target-related magnetic response (top row), the distractor was placed at the vertical meridian position with the target appearing at one of the two positions in the left (left) or the right visual field (right). The distractor-related response (bottom row) was isolated analogously way by placing the distractor at lateral positions, with the target appearing on the vertical meridian. The tERL or dERL was derived by subtracting the response to right visual field items from left visual field items; a subtraction that nulls the magnetic response elicited by the item placed on the vertical meridian. b, Illustration of trial-block structure and color assignment to the search items in Experiment 1–4. Each of the colored bars indicates the color assigned to the target (T) and distractor (D) on a given trial. The four neutral distractors were always blue in all experiments, and, except for Experiment 3, the task was always to determine the orientation of the target “T”.

Figure 2.

ERMF results of Experiment 1. a, Waveforms elicited by the lateralized target (blue) and the lateralized distractor (pink) when presented in the contralateral (solid) and ipsilateral visual field (dashed) relative to the sensor hemisphere the ERMF response was recorded from. b, ERL difference waveforms (solid-minus-dashed in a) of the lateralized target (black) and the lateralized distractor (red). The black and red horizontal bars highlight time ranges of significant ERLs (sliding-window t test) for the target and distractor, respectively. c, Magnetic field distribution maps of the tERL and dERL at selected time points corresponding to the temporal maxima of the ERL responses (small vertical lines in b). The maps show the left-right hemisphere collapsed field distributions. The black ellipses encompass efflux-influx field components reflecting the N1pc, Pd, and N2pc. The asterisks mark the location of the efflux-influx field transition, where the underlying current source would approximately be located. Note, the scale varies across the different topographical maps, as demarcated.

Figure 3.

ERP results of Experiment 1. a, ERL difference waveforms elicited by the lateralized target (black) and lateralized distractor (red) at electrode sites PO7/8. The black and red horizontal bars highlight time ranges of significant ERLs for the target and distractor, respectively. b, Topographical maps of the tERL and dERL are depicted at the marked points (small vertical lines in a). The maps of the N2pc and Pd show the electric field distribution at the latency of the field maxima of the corresponding ERMF response (compare with Fig. 2). Note, the tERL shows no separate maximum corresponding with the tN1pc, presumably due to overlap with the following N2pc. The tN1pc map is therefore displayed at the latency of the dN1pc maximum. All topographical maps show left-right hemisphere collapsed field distributions, and the scales (variable) are demarcated in the figure.

Figure 4.

ERMF results of Experiment 2. a, ERL waveforms elicited by the lateralized target (black) and distractor (red). b, RT median-split analysis. ERL waveforms of fast (thick dashed) and slow RTs (thin dashed) are separately shown for the target (tERL; black) and the distractor (dERL; red). The gray and pink horizontal bars highlight time-ranges of significant ERLs for the tERL and dERL, respectively. The filled and open bars refer to the fast and slow RTs, respectively.

Figure 5.

ERMF results of Experiment 3. ERL waveforms elicited by the task-irrelevant color singletons whose color defined the target (black) or the distractor (red) in Experiment 2. The gray and light-red waveforms replot the N2pc and Pd of Experiment 2 (Fig. 4a), respectively, for comparison. The horizontal black bar highlights the time range of a significant tERL difference.

Figure 6.

ERMF results of Experiment 4. a, ERL waveforms elicited by the lateralized target (black) and distractor (red). b, Fractional peak latency analysis the tN1pc (black) and dN1pc (red) in Experiments 1, 2, and 4. c, Peak latency analysis the N2pc (black) and Pd (red) in Experiments 1, 2, and 4.