Efficient "pop-out" visual search elicits sustained broadband γ activity in the dorsal attention network

Abstract

An object that differs markedly from its surrounding-for example, a red cherry among green leaves-seems to pop out effortlessly in our visual experience. The rapid detection of salient targets, independently of the number of other items in the scene, is thought to be mediated by efficient search brain mechanisms. It is not clear, however, whether efficient search is actually an "effortless" bottom-up process or whether it also involves regions of the prefrontal cortex generally associated with top-down sustained attention. We addressed this question with intracranial EEG (iEEG) recordings designed to identify brain regions underlying a classic visual search task and correlate neural activity with target detection latencies on a trial-by-trial basis with high temporal precision recordings of these regions in epileptic patients. The spatio-temporal dynamics of single-trial spectral analysis of iEEG recordings revealed sustained energy increases in a broad gamma band (50-150 Hz) throughout the duration of the search process in the entire dorsal attention network both in efficient and inefficient search conditions. By contrast to extensive theoretical and experimental indications that efficient search relies exclusively on transient bottom-up processes in visual areas, we found that efficient search is mediated by sustained gamma activity in the dorsal lateral prefrontal cortex and the anterior cingulate cortex, alongside the superior parietal cortex and the frontal eye field. Our findings support the hypothesis that active visual search systematically involves the frontal-parietal attention network and therefore, executive attention resources, regardless of target saliency.

Figures

Figure 1.

Experimental conditions, behavior, and time-frequency responses. A, The experimental design. After a 1000 ms interstimulus interval, a visual array is presented for 3000 ms. When the target is detected, subjects press a button to indicate in which quadrant of the array (upper or lower) it is located. In the inefficient search condition (in red), target and distractors have the same color. In the efficient search condition (in blue), the target has a different contrast than the distractors. B, Reaction time distribution for efficient (blue) and inefficient visual search (red). C, Statistical time-frequency maps (Wilcoxon Z, FDR corrected) for efficient (left) and inefficient (right) visual search from a recording site (patient 10; Talairach coordinates: [−43 −3 34]), located in dorsolateral prefrontal cortex.

Figure 2.

Broadband gamma activity response patterns during visual search. A, Grand average broadband gamma response topography across all recording sites and all patients, plotted on a “glass brain” in MNI coordinates. B, Top, Single-trial BGA responses recorded from DLPFC (left, Talairach coordinates [−37 17 27]) and primary motor cortex (right, Talairach coordinates [−57 −28 48]) from patient 23 in the inefficient search condition. Middle, Scatter plot of single-trial BGA quanta versus reaction times. A BGA quantum is a significant time-sample of BGA response versus baseline power evaluated between stimulus onset and offset (Wilcoxon test, FDR corrected). Left and right panels correspond to upper BGA responses. C, Average BGA responses aligned to the response (button-press). Left and right panels correspond to top panel BGA responses.

Figure 3.

Single-trial gamma-band responses to efficient and inefficient visual search from frontal-parietal recording sites. A, All recording sites with a transient gamma-band response (see Materials and Methods) located in glass brain (Talairach). B, Four illustrative examples (MRI, right) of single-trial gamma-band responses to efficient (eff) and inefficient (ineff) visual search (left) recorded within 4 regions of interest of the frontal-parietal network: DLPFC (patient 5, Talairach coordinates [−58 −1 34]), dACC (patient 10, Talairach coordinates [−12 11 47]), PrCS/MFG putative FEF (patient 10, Talairach coordinates [−46 −2 34]), and IPS (patient 23, Talairach coordinates [−52 −42 46]).

Figure 4.

Single-trial gamma-band responses (Transient,Type 1) during efficient and inefficient visual search. A, Recording sites located in glass brain (Talairach). In blue: contacts with a stronger response during efficient vs inefficient search (Kruskal-Wallis, FDR corrected). B, Two illustrative examples of single-trial gamma-band responses during efficient (eff) and inefficient (ineff) search in the right and left fusiform gyrus: (patient 6, Talairach coordinates [36 −52 −12] and patient 20 [−30 −41 −16]). Bottom, Profile of gamma-band responses aligned to stimuli onset. Left and right panels correspond to top panel responses.