A Map for Social Navigation in the Human Brain

Abstract

Deciphering the neural mechanisms of social behavior has propelled the growth of social neuroscience. The exact computations of the social brain, however, remain elusive. Here we investigated how the human brain tracks ongoing changes in social relationships using functional neuroimaging. Participants were lead characters in a role-playing game in which they were to find a new home and a job through interactions with virtual cartoon characters. We found that a two-dimensional geometric model of social relationships, a "social space" framed by power and affiliation, predicted hippocampal activity. Moreover, participants who reported better social skills showed stronger covariance between hippocampal activity and "movement" through "social space." The results suggest that the hippocampus is crucial for social cognition, and imply that beyond framing physical locations, the hippocampus computes a more general, inclusive, abstract, and multidimensional cognitive map consistent with its role in episodic memory.

Copyright © 2015 Elsevier Inc. All rights reserved.

Figures

Figure 1. Experimental Design

(A) Schematic depiction of trial types and task structure. The example shows a power interaction (see Table S1 for examples of interactions; see Tables S2–S4 and Figure S4 for analysis of the Narrative and Options conditions). (B) Schematic depiction of the geometrical representation of social coordinates. The example shows a character moving through the course of four social interactions (blue line trajectory to point of interaction from the character’s origin). To calculate social coordinates, we drew a vector between the theoretical point of view (maximum intimacy, neutral power) and the character’s position. We calculated the vector length (V) and the vector angle (θ) for each social interaction (see Figure S3 for analysis of a non-egocentric angle).

Figure 2. Participants’ Behavior in the Task

(A) Examples of characters’ trajectories from three participants in a 3D view. The x axis represents affiliation, the y axis represents power, and the z axis represents the 12 total social interactions with each character (see Figure S1 for examples of 2D trajectories). (B) Mean and SD values of the vector angle (cosine θ) and length (V, arbitrary units) at the final time point for each of the five main characters (the sixth character served as control and did not change position; see Experimental Procedures). One-way ANOVA with a main factor of character type yielded a significant main effect for the vector angle and vector length (F = 5.46, F = 2.99, respectively; p < 0.05). Asterisks represent significant difference between two corresponding characters (post hoc t tests, p < 0.05).

Figure 3. Neural Correlates of Power Modulated by Affiliation, Measured by the Vector Angle

The regressor tracking the angle between the participant’s point of view and the character (cosine θ), which corresponds to a character’s interaction between power and affiliation at each social interaction throughout the task, was contrasted with baseline in a whole-brain analysis. (A) The resulting statistical map overlaid on the groups’ average anatomical image shows the hippocampus (p Z-scored beta weights extracted from that peak voxel are shown for each condition. (C) Options trials were separated into two types: high cosine θ and low cosine θ. Event-related averaging of the hippocampal mean percent signal change (from the entire cluster) shows higher BOLD responses for options trials where characters are perceived as having more power relative to the participant, modulated by affiliation (cosine θ closer to 1). (D) The parametric regressor tracking the character’s power as a Cartesian coordinate at each social interaction throughout the task correlated with the BOLD signal in the left middle temporal gyrus (BA 37). The right panel shows the resulting statistical map overlaid on the groups’ average anatomical image (p Z-scored beta weights extracted from that peak voxel for each condition. Error bars indicate SEM.

Figure 4. Hippocampal BOLD Correlations with Social Skills and Personality Scores

Significant linear correlations (Pearson’s r, p < 0.05) between the hippocampal beta weight values of the vector angle regressor, corresponding to the interaction between power and affiliation, and social avoidance (Liebowitz Social Anxiety Scale, avoidance dimension), neuroticism (Neo Personality Inventory), and conscientiousness (Neo Personality Inventory).

Figure 5. Neural Correlates of the Magnitude of Social Distance, Measured by the Vector Length

The regressor tracking the length of the vector drawn between the participant’s point of view and the character, which corresponds to the magnitude of a character’s social distance to the participant at each social interaction throughout the task, was contrasted against baseline in a whole-brain analysis. The resulting statistical map overlaid on the groups’ average anatomical image (left panel) revealed a single region (p Z-scored beta weights extracted from that peak voxel is shown in the right panel. Error bars indicate SEM.