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. 2023 Oct 2:11:e16139.
doi: 10.7717/peerj.16139. eCollection 2023.

Different patterns of foreground and background processing contribute to texture segregation in humans: an electrophysiological study

Baoqiang Zhang  1   2   3 , Saisai Hu  1   2   3 , Tingkang Zhang  1   2   3 , Min Hai  1   2   3 , Yongchun Wang  1   2   3 , Ya Li  1   2   3 , Yonghui Wang  1   2   3
Affiliations

Different patterns of foreground and background processing contribute to texture segregation in humans: an electrophysiological study

Baoqiang Zhang et al. PeerJ. .

Abstract

Background: Figure-ground segregation is a necessary process for accurate visual recognition. Previous neurophysiological and human brain imaging studies have suggested that foreground-background segregation relies on both enhanced foreground representation and suppressed background representation. However, in humans, it is not known when and how foreground and background processing play a role in texture segregation.

Methods: To answer this question, it is crucial to extract and dissociate the neural signals elicited by the foreground and background of a figure texture with high temporal resolution. Here, we combined an electroencephalogram (EEG) recording and a temporal response function (TRF) approach to specifically track the neural responses to the foreground and background of a figure texture from the overall EEG recordings in the luminance-tracking TRF. A uniform texture was included as a neutral condition. The texture segregation visual evoked potential (tsVEP) was calculated by subtracting the uniform TRF from the foreground and background TRFs, respectively, to index the specific segregation activity.

Results: We found that the foreground and background of a figure texture were processed differently during texture segregation. In the posterior region of the brain, we found a negative component for the foreground tsVEP in the early stage of foreground-background segregation, and two negative components for the background tsVEP in the early and late stages. In the anterior region, we found a positive component for the foreground tsVEP in the late stage, and two positive components for the background tsVEP in the early and late stages of texture processing.

Discussion: In this study we investigated the temporal profile of foreground and background processing during texture segregation in human participants at a high time resolution. The results demonstrated that the foreground and background jointly contribute to figure-ground segregation in both the early and late phases of texture processing. Our findings provide novel evidence for the neural correlates of foreground-background modulation during figure-ground segregation in humans.

Keywords: Electroencephalogram (EEG); Figure-ground organization; Temporal response function (TRF); Texture segregation.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Figure 1
Figure 1. Stimulus of experiment.
The luminance-defined figure and uniform texture are presented in the central visual field (A: figure texture; B: uniform texture).
Figure 2
Figure 2. Psychophysical procedure and illustration of the temporal response function (TRF) approach.
(A) A sample trial sequence of experiment. (B) Three independent 5 s random temporal sequences were generated by modulating the luminance of the foreground, background, and uniform independently and randomly throughout the trial (e.g., left of B, top: foreground luminance sequence, middle: background luminance sequence, bottom: uniform luminance sequence). The EEG response was also recorded simultaneously (middle of B, top: figure EEG, bottom: uniform EEG). The TRF response for each stimulus condition (e.g. foreground, background and uniform) could be estimated from the EEG data based on the corresponding luminance temporal sequence (e.g., right of B, top: foreground TRF, middle: background TRF, bottom: uniform TRF). In order to compute the TRF, a regularized linear regression was applied between the stimulus luminance value and EEG amplitude.
Figure 3
Figure 3. Original TRF waveforms.
The average (N = 22) TRF waveforms for the foreground (salmon pink lines), background (dark blue lines), and uniform (gray lines) were plotted in different brain regions (occipital, parieto-occipital, parietal, central, and frontal regions) as a function of temporal lag (0 to 800 ms).
Figure 4
Figure 4. TRFs obtained after the stimulus sequences and EEG were shuffled (B) or not shuffled (A).
Figure 5
Figure 5. Foreground tsVEP and background tsVEP waveforms in different regions.
Foreground tsVEP (foreground-uniform, red line) and background tsVEP (background-uniform, black line) waveforms in the different regions (occipital, parieto-occipital, parietal, central and frontal regions) as a function of latency (0–800 ms). Shaded regions represent analysis time windows (left to right: 100–140, 150–200, 250–320 ms). Red and black asterisks in the shaded regions indicate that the mean foreground and background tsVEP amplitudes deviated significantly from zero (p < 0.050) in the corresponding time windows, respectively.
Figure 6
Figure 6. Topographies of foreground tsVEP and background tsVEP for three components.
Grand average distribution maps for foreground tsVEP (top panel) and background tsVEP (bottom panel) at 100–140, 150–200, and 250–320 ms time range. White asterisks in occipital and frontal regions indicate foreground tsVEP or background tsVEP significantly different from zero (*p < 0.050, **p < 0.010, ***p < 0.001).
Figure 7
Figure 7. Results for experiment: different patterns of foreground and background processing at 100–140 and 250–320 ms windows.
(A) Results for 100–140 ms window. (B) Results for 250–320 ms window. Error bars represent standard errors of the means. *p < 0.050, **p < 0.010, ***p < 0.001.
Figure 8
Figure 8. Schematic illustration of the figure-ground segregation.
First, image features, i.e., the local luminance and orientation of bars, are registered. Second, in the early stage of texture segregation, foreground enhancement and background suppression are expressed in the visual cortex, as evidenced by early negative components in the posterior region for both foreground- and background-tsVEPs. The positive component in the anterior region may be related to the process of filtering out the background signal in order to perform the detection task. Third, the background continues to be suppressed, which may be complete by feedback processing from the frontal areas to visual areas, as suggested by both the anterior positive component and the posterior negative component in the late time window. The positive component may be related to attention or other cognitive processes being directed to the figure-defined objects. The red dashed line represents foreground related processes, while the blue dashed line represents background related processes.
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Grants and funding

This work was supported by the National Natural Science Foundation of China (No. 31800910). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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