Face the hierarchy: ERP and oscillatory brain responses in social rank processing

Abstract

Recognition of social hierarchy is a key feature that helps us navigate through our complex social environment. Neuroimaging studies have identified brain structures involved in the processing of hierarchical stimuli but the precise temporal dynamics of brain activity associated with such processing remains largely unknown. Here, we used electroencephalography to examine the effect of social hierarchy on neural responses elicited by faces. In contrast to previous studies, the key manipulation was that a hierarchical context was constructed, not by varying facial expressions, but by presenting neutral-expression faces in a game setting. Once the performance-based hierarchy was established, participants were presented with high-rank, middle-rank and low-rank player faces and had to evaluate the rank of each face with respect to their own position. Both event-related potentials and task-related oscillatory activity were investigated. Three main findings emerge from the study. First, the experimental manipulation had no effect on the early N170 component, which may suggest that hierarchy did not modulate the structural encoding of neutral-expression faces. Second, hierarchy significantly modulated the amplitude of the late positive potential (LPP) within a 400-700 ms time-window, with more a prominent LPP occurring when the participants processed the face of the highest-rank player. Third, high-rank faces were associated with the highest reduction of alpha power. Taken together these findings provide novel electrophysiological evidence for enhanced allocation of attentional resource in the presence of high-rank faces. At a broader level, this study brings new insights into the neural processing underlying social categorization.

Figure 1. Representation of the nine experimental sub-conditions in the design.

Columns (yellow) correspond to the three participant rank conditions (highest, middle and lowest rank); rows (green) depict the three player rank conditions (the same three conditions). Note that the term “Player” refers to the face stimuli, while the participant is the subject that took part in the EEG experiment.

Figure 2. Examples of round and associated ranking proposed to the participant during phase 1.

A) Example of one round of the game during phase 1. In this game, the participant was asked to decide which side of the screen contained the largest amount of dots. B) Example of three-level ranking presented to the participant after each round of the game. Participant's face was the only photograph displayed in color during this phase. All the subjects of the photographs used here have given written informed consent, as outlined in the PLOS consent form, to publication of their photograph.

Figure 3. Temporal course representation of stimuli displayed during the phase 3.

The subject of the photograph has given written informed consent, as outlined in the PLOS consent form, to publication of their photograph.

Figure 4. ERP waveforms and averaged signal of P100, N170 and LPP components.

A) ERP waveforms of early (P100 and N170) and late (LPP) responses in the three player rank conditions (highest, middle or lowest rank). Associated back-view topographic maps represent the averaged amplitude of LLPs at 550 ms. B) Averaged LPP amplitude in the 400–700 ms time window computed on the left (F3, C3, P3), central (FZ, CZ, PZ) and right (F4, C4, P4) scalp regions in the 3 player rank conditions. * indicates a significant difference (p<0.05).

Figure 5. TF maps and averaged profile of alpha oscillatory response.

A) TF map depicting the color-coded mean energy (in μV²) in response to faces in the three player rank conditions (Highest, Middle and Lowest) at the electrode Pz. The red zone depicts an energy decrease in the [9–12 Hz] × [150–700 ms] TF domain (white box). B) Time course of the energy in the alpha band during the responses to the three player rank conditions: highest (blue), middle (yellow) and lowest (green). C) Z-score topographic maps for the Wilcoxon comparisons with the baseline when the participant was in the middle position, in the three sub-conditions of player rank. The player's relative status is, from top to bottom, superior, equal and inferior. White dots indicate electrodes where the alpha reduction was significant compared with the baseline (p<0.05). D) Averaged alpha power for the three player rank conditions computed on Pz in [100–400 ms] and [400–700 ms]. Significant differences (p<0.05) are indicated by *.