Attention to features precedes attention to locations in visual search: evidence from electromagnetic brain responses in humans

Abstract

Single-unit recordings in macaque extrastriate cortex have shown that attentional selection of nonspatial features can operate in a location-independent manner. Here, we investigated analogous neural correlates at the neural population level in human observers by using simultaneous event-related potential (ERP) and event-related magnetic field (ERMF) recordings. The goals were to determine (1) whether task-relevant features are selected before attention is allocated to the location of the target, and (2) whether this selection reflects the locations of the relevant features. A visual search task was used in which the spatial distribution of nontarget items with attended feature values was varied independently of the location of the target. The presence of task-relevant features in a given location led to a change in ERP/ERMF activity beginning approximately 140 msec after stimulus onset, with a neural origin in the ventral occipito-temporal cortex. This effect was independent of the location of the actual target. This effect was followed by lateralized activity reflecting the allocation of attention to the location of the target (the well known N2pc component), which began at approximately 170 msec poststimulus. Current source localization indicated that the allocation of attention to the location of the target originated in more anterior regions of occipito-temporal cortex anterior than the feature-related effects. These findings suggest that target detection in visual search begins with the detection of task-relevant features, which then allows spatial attention to be allocated to the location of a likely target, which in turn allows the target to be positively identified.

Figure 1.

a, Stimulus arrays used in the first experiment. Stimuli consisted of arrays of C-shaped items placed to the left and right of fixation, with one distinctively colored item in each field (the red C in the LVF and the green C in the RVF). One of these colors indicated the target for half of the trial blocks, and the other color indicated the target for the other half. Distracter items (blue Cs) were placed in both visual fields surrounding the target and the potential target. The orientation of the distracters was either left-right like the target (ROD) or up-down (irrelevant-orientation distractors). The location of RODs and irrelevant-orientation distractors was varied to generate four different distractor distributions: (1) RODs in the target visual field and irrelevant-orientation distractors in the opposite field (target-side ROD); (2) RODs in the nontarget visual field and irrelevant-orientation distractors in the target field (nontarget-side ROD); (3) RODs in both visual fields (both-sides ROD); and (4) irrelevant-orientation distractors in both visual fields with no RODs (no ROD). b, Behavioral results (experiment 1). The average response times (left) and percentage of correct responses (right) for the four experimental conditions are shown.

Figure 6.

Source density estimates of the N2pc effect. Left, Source density estimates of the grand average N2pc for the target-side ROD, nontarget-side ROD, and both-sides ROD condition. Right, Source density maxima of the N2pc of individual subjects (yellow dots) plotted on lateral hemisphere views together with the maxima of the ROD-related negativity (target-side ROD) between 140 and 200 msec (red and blue dots), already shown in Figure 5b.

Figure 2.

a, ROD-related effects for left visual field targets (experiment 1). ERP waveforms elicited by target-side ROD (top), nontarget-side ROD (middle), and both-sides ROD (bottom, solid lines) trials superimposed onto waveforms of the no ROD condition (dashed lines) at selected electrode sites from the left parieto-occipital (PO7) and the right parieto-occipital (PO8) scalp are shown. The ROD-related negativity is indicated by unfilled arrows (early portion) and filled arrows (later portion). The middle column illustrates the distribution of the ROD-related negativity (mean effect between 140 and 190 msec) by showing voltage difference maps target-side ROD minus no ROD (top), nontarget-side ROD minus no ROD (middle), and both-sides ROD minus no ROD (bottom). Positive to negative voltage differences are scaled from dark to bright, repectively. b, ROD-related effects for right visual field targets.

Figure 3.

a, ERP difference waves target-side ROD minus no ROD (solid thin line), nontarget-side ROD minus no ROD (dash-dot line), and both-sides ROD minus no ROD (solid thick line) for left visual field targets and right visual field targets at selected electrode sites. b, ERMF waveforms and distributions of one observer (left) and the grand average (right). ERMF waveforms are shown from selected sensor sites that flank the efflux-influx reversal of the magnetic flux field (white ellipses). Waveforms elicited by target-side ROD (solid lines; top left waveforms at S59 and S120), nontarget-side ROD (solid lines; middle right waveforms at S42 and S142), and both-sides ROD (solid lines at the bottom left and right) trials are superimposed onto waveforms of the no ROD condition (dashed lines). The four black dots in the top right topographical map (grand average) highlight the sensor sites from which measures were taken to validate the ROD-related effects in the magnetic waveforms.

Figure 4.

Target-related effects (N2pc effect). Left, Average waveforms elicited by target items contralateral (solid line) and ipsilateral (dashed line) to electrode sites PO7/8. Data were collapsed over electrode sites to simplify presentation. The N2pc effect is highlighted by the gray areas between waveforms. Right, Time course of the N2pc effect shown as difference waves (contralateral targets minus ipsilateral targets; broken lines) and the ROD-related negativity, as in Figure 3a (thick solid line). The arrows indicate that the ROD-related negativity is visible in the N2pc difference waves of the target-side ROD and nontarget-side ROD condition. Triangles mark the onset latency of a significant ROD-related effect (filled) and the N2pc effect (unfilled) of the both-sides ROD condition.

Figure 5.

Source density estimates (ERMF data of experiment 1). a, Source density estimates for the ROD-related negativity (140-200 msec) of the grand average (left) and one single subject (right). Shown are results for left visual field target trials only. b, Maxima of the source density estimate for the ROD-related negativity of individual subjects (each dot represents one subject). Maxima were computed in early (140-200 msec; yellow and blue dots) and late (200-290 msec; pink and green dots) time ranges, using individual anatomical data, and then transformed into the MNI reference space.

Figure 7.

a, ROD-related negativity (experiment 2). Voltage difference maps nontarget-side ROD minus no ROD (top), target-side ROD minus no ROD (middle), and both-sides ROD minus no ROD (bottom). Positive to negative voltage differences are scaled from dark to bright, respectively. The order of conditions was changed (top and middle) to allow a direct comparison with corresponding topographical maps in Figure 2, a and b. b, ERP waveforms at the P07 and P08 electrode sites from experiment 3. Shown are waveforms that correspond to the conditions of target-side ROD (top), nontarget-side ROD (middle), and both-sides ROD (bottom; solid lines) trials from the first experiment, as shown in Figure 2a.