A source for awareness-dependent figure-ground segregation in human prefrontal cortex

Abstract

Figure-ground modulation, i.e., the enhancement of neuronal responses evoked by the figure relative to the background, has three complementary components: edge modulation (boundary detection), center modulation (region filling), and background modulation (background suppression). However, the neuronal mechanisms mediating these three modulations and how they depend on awareness remain unclear. For each modulation, we compared both the cueing effect produced in a Posner paradigm and fMRI blood oxygen-level dependent (BOLD) signal in primary visual cortex (V1) evoked by visible relative to invisible orientation-defined figures. We found that edge modulation was independent of awareness, whereas both center and background modulations were strongly modulated by awareness, with greater modulations in the visible than the invisible condition. Effective-connectivity analysis further showed that the awareness-dependent region-filling and background-suppression processes in V1 were not derived through intracortical interactions within V1, but rather by feedback from the frontal eye field (FEF) and dorsolateral prefrontal cortex (DLPFC), respectively. These results indicate a source for an awareness-dependent figure-ground segregation in human prefrontal cortex.

Trial registration: ClinicalTrials.gov NCT00001360.

Keywords: awareness; background suppression; boundary detection; prefrontal cortex; region filling.

Conflict of interest statement

The authors declare no competing interest.

Figures

Fig. 1.

Stimuli, psychophysical protocol, and data. (A) Two sample orientation-defined figures presented in the upper visual field (Left: large figure; Right: small figure). The orientation contrasts between the figure bars and the background bars was 60° (the yellow dot indicates the fixation point). (B) Large (Left) and small (Right) grating probes, with the same diameter as the large and small figures, respectively. (C) Low- (Left) and high- (Right) luminance mask stimuli used in the visible and invisible conditions, respectively. (D) Psychophysical protocol. A figure–ground stimulus was presented for 50 ms, followed by a 100-ms mask and another 50-ms fixation interval. Then a large or small grating probe, with the same diameter as the large figure and small figure, respectively, was randomly presented for 50 ms with equal probability and presented randomly at either the figure location (valid cue condition) or its contralateral counterpart (invalid cue condition) with equal probability. The grating probe was orientated at 45° or 135° away from the vertical. Subjects were asked to press one of two buttons as rapidly and correctly as possible to indicate the orientation of the grating probe (45° or 135°). The psychophysical cueing effect for the large (E) and small (F) figures and the large and small gratings in both visible and invisible conditions. Each cueing effect was quantified as the difference between the reaction time of the probe task performance in the invalid cue condition and that in the valid cue condition. Error bars denote 1 SEM calculated across subjects and colored dots denote the data from each subject.

Fig. 2.

fMRI stimuli and protocol. (A) ROI definition. The checkered patch on the Left was used to define ROIs corresponding to the figure center of the large figure and the whole small figure; the checkered patch on the Right was used to define ROIs corresponding to the figure boundary of the large figure and the small figure’s background. (B) The transparent squares show the size and location of the checkered patches relative to the large figure (Top) and small figure (Bottom). The red squares (Left) indicate the figure center of the large figure and the whole small figure; the blue squares (Right) indicate the figure boundary of the large figure and the small figure’s background. (C) ROIs on an inflated cortical surface of a representative subject. The ROIs in V1 were defined as the cortical regions responding to the figure center (red region, V1 center) and figure boundary (blue region, V1 boundary) of the large figure. These cortical regions in V1 were also used as the ROIs corresponding to the whole small figure (red region, V1 figure) and its surround background (blue region, V1 background). Both V1 boundary of the large figure and V1 background of the small figure contained two separate regions with different eccentricities: the parafovea and periphery, indicated by the dashed and solid rings, respectively. The ROIs in LGN and V2 to V4 were defined as the regions responding to the whole figure since activated areas in these areas showed a great deal of overlap. The boundaries among V1 to V4, defined by retinotopic mapping, are indicated by the white lines. (D) Block design fMRI procedure. On each trial in the figure and mask-only blocks, a figure–ground stimulus and the fixation were presented for 50 ms, respectively, followed by a 100-ms mask (low- and high-luminance for visible and invisible conditions, respectively) and 1,850-ms fixation interval. In the Invisible condition, on each trial during both the figure and mask-only blocks, subjects were asked to press one of two buttons to indicate the location of the figure, which was Left of fixation in one half of blocks and Right of fixation in the other half at random (i.e., the 2AFC task). In the visible condition, on each trial during the figure block, subjects needed to perform the same 2AFC task of the figure, whereas during the mask-only block, subjects were asked to press one of two buttons randomly.

Fig. 3.

fMRI results. (A, Left) Blocked BOLD signals averaged across subjects in the ipsilateral and contralateral ROIs in V1 center, V1 boundary, LGN, and V2 to V4 for the large figure, during the visible and invisible conditions. Error bars denote 1 SEM calculated across subjects at each time point. (A, Right) BOLD amplitude differences between the blocked BOLD signals at the contralateral ROIs and those at the ipsilateral ROIs in V1 center, V1 boundary, LGN, and V2 to V4 during the visible and invisible conditions. Error bars denote 1 SEM calculated across subjects and colored dots denote the data from each subject. (B, Left) Blocked BOLD signals averaged across subjects in the ipsilateral and contralateral ROIs in V1 figure, V1 background, LGN, and V2 to V4 for the small figure, during the visible and invisible conditions. Error bars denote 1 SEM calculated across subjects at each time point. (B, Right) BOLD amplitude differences between the blocked BOLD signals at the contralateral ROIs and those at the ipsilateral ROIs in V1 figure, V1 background, LGN, and V2 to V4 during the visible and invisible conditions. Error bars denote 1 SEM calculated across subjects and colored dots denote the data from each subject.

Fig. 4.

Results of whole-brain and correlation analyses. Whole-brain search for DLPFC {large figure: [43, 9, 29], t(17) = 4.441, P < 0.001, ηp2 = 0.537; small figure: [39, 23, 23], t(17) = 5.713, P < 0.001, ηp2 = 0.658}, MFG {large figure: [34, 45, 10], t(17) = 5.742, P < 0.001, ηp2 = 0.660; small figure: [30, 43, 13], t(17) = 4.653, P < 0.001, ηp2 = 0.560}, FEF {large figure: [32, −6, 47], t(17) = 4.179, P = 0.001, ηp2 = 0.507; small figure: [40, 3, 29], t(17) = 4.885, P < 0.001, ηp2 = 0.584}, insula {large figure: [Left: −34, 17, 1] and [Right: 28, 18, 4], t(17) = 4.999, P < 0.001, ηp2 = 0.595; small figure: Left: −36, 14, 5] and [Right: 27, 17, 5], t(17) = 5.176, P < 0.001, ηp2 = 0.612}, and IPS {large figure: [26, −59, 41], t(17) = 4.470, P < 0.001, ηp2 = 0.540; small figure: [26, −62, 33], t(17) = 3.434, P = 0.003, ηp2 = 0.410}, with all showing a significantly greater response in the visible than the invisible condition for the large figure (A) and small figure (B). Error bars denote 1 SEM calculated across subjects and colored dots denote the data from each subject. (C) Correlations between DBOLD in V1 center of the large figure and that in V4 (Left) and FEF (Right) across individual subjects. (D) Correlation coefficients (r values) between DBOLD in V1 center of the large figure and that in other cortical/subcortical areas across individual subjects. (E) Correlations between DBOLD in V1 background of the small figure and that in IPS (Left) and DLPFC (Right) across individual subjects. (F) Correlation coefficients (r values) between DBOLD in V1 background of the small figure and that in other cortical/subcortical areas across individual subjects.

Fig. 5.

DCM results for region-filling and background-suppression processes. (A) Eleven different models among FEF, V4, V1 center, and V1 boundary used to model the modulatory effect of the visible condition for region-filling process. The colored lines and arrows illustrate potential feedback modulations to V1 center. V1 center and V1 boudnary: ROI in V1 evoked by the figure center and figure boundary of the large figure, respectively. (D) Eleven different models among DLPFC, IPS, V1 figure, and V1 background used to model the modulatory effect of the visible condition for the background-suppression process. The colored lines and arrows illustrate potential feedback modulations to V1 background. V1 figure and V1 background: ROI in V1 evoked by the whole small figure and its surround background, respectively. Exceedance probabilities of the 11 models with the visible condition as the modulatory input for region-filling (B) and background-suppression (E) processes. The strength of the modulatory connections for the visible condition and its significance levels for region-filling (C) and background-suppression (F) processes (*P < 0.05).

Fig. 6.

Schematic illustration of the figure–ground segregation. First, features in the image, i.e., the local orientation of bars, are registered. Second, feature discontinuities that signal boundaries between the figure and background are detected (i.e., boundary-detection process) through local intracortical interactions within V1. Third, the neural response elicited by the center of the figure (i.e., the region-filling process) in V1 is enhanced through the increased feedback from FEF. The FEF directly sends top-down biasing signals to enhance the response of neurons tuned to the same orientation. Fourth, the neural response elicited by the preceding segregated figure’s background (i.e., the background-suppression process) in V1 is reduced through the decreased feedback (increased suppression) from DLPFC. The DLPFC directly filters out the task-irrelevant information. Finally, the neuronal response is enhanced in the region perceived to be the figure (dark gray region) and suppressed in the region perceived to be the background (light gray region), resulting that the visual system segments the image into the figure and background.