Dynamic neural architecture for social knowledge retrieval

Abstract

Social behavior is often shaped by the rich storehouse of biographical information that we hold for other people. In our daily life, we rapidly and flexibly retrieve a host of biographical details about individuals in our social network, which often guide our decisions as we navigate complex social interactions. Even abstract traits associated with an individual, such as their political affiliation, can cue a rich cascade of person-specific knowledge. Here, we asked whether the anterior temporal lobe (ATL) serves as a hub for a distributed neural circuit that represents person knowledge. Fifty participants across two studies learned biographical information about fictitious people in a 2-d training paradigm. On day 3, they retrieved this biographical information while undergoing an fMRI scan. A series of multivariate and connectivity analyses suggest that the ATL stores abstract person identity representations. Moreover, this region coordinates interactions with a distributed network to support the flexible retrieval of person attributes. Together, our results suggest that the ATL is a central hub for representing and retrieving person knowledge.person knowledge | anterior temporal lobe | person identity node | semantic memory | social neuroscience A s social creatures, it is essential that we develop a rich storehouse of knowledge about other members of our social network, such as who they are, how they look and sound, where they live, and what they do for a living. However, little is known about how and where such "person knowledge" is represented, stored, and retrieved in the brain. This inquiry is challenging because person knowledge is highly multimodal and multifaceted, being linked to both abstract features such as personality and social status as well as more concrete features such as eye color; in addition, familiar individuals are associated with detailed episodic and semantic memories (e.g., memories of shared experiences and biographic information) (1, 2). The neural circuit for person knowledge must therefore have the ability to combine multiple sources of information into an abstract representation accessible from multiplicative cues.An influential theory by Burton and Bruce (3) proposes that person recognition is achieved through a hierarchical process that begins with the activation of modality-specific recognition units that selectively respond to the presence of a known face, name, or voice. This information is then sent to an amodal person identity node (PIN) that integrates information from the modality-specific recognition units into a multimodal representation for that individual. Excitation of the PIN ultimately allows the retrieval of personspecific semantic information independently of stimulus modality (4, 5). A similar design is embedded in the "hub-and-spoke" theory of semantic knowledge, which proposes that different features of a concept (such as its color or taste) are distributed throughout the brain (the "spokes") and that a centralized "hub" integrates these features into a cohe...

Close yet independent: Dissociation of social from valence and abstract semantic dimensions in the left anterior temporal lobe

“…Therefore, the brain regions activated in our study and in social processing studies could be different due to different experimental tasks and contrasts. The left aSTS found here has not been reported in experiments using nonverbal person-related stimuli (e.g., human voices, faces, or biological motion; Deen, Koldewyn, Kanwisher, & Saxe, 2015) or cartoons depicting social interactions (Centelles, Assaiante, Nazarian, Anton, & Schmitz, 2011;Isik, Koldewyn, Beeler, & Kanwisher, 2017; but see Ross & Olson, 2010), either, and seems to be located posteriorly to the TP area that stores personrelated semantic knowledge (Ross & Olson, 2012;Simmons et al, 2010;Wang et al, 2017;Wang, Peelen, Han, Caramazza, & Bi, 2016).…”

“…Note that social knowledge has been very broadly defined, from the mere presence of persons (Mellem et al, 2016;Norris, Chen, Zhu, Small, & Cacioppo, 2004), to the biographical information of specific persons (Simmons et al, 2010;Wang et al, 2017), and to socially interactive behaviors or properties (Zahn et al, 2007). Note that social knowledge has been very broadly defined, from the mere presence of persons (Mellem et al, 2016;Norris, Chen, Zhu, Small, & Cacioppo, 2004), to the biographical information of specific persons (Simmons et al, 2010;Wang et al, 2017), and to socially interactive behaviors or properties (Zahn et al, 2007).…”

“…In this study, we first examined the effects of sociality, valence, and their potential interactions in the ATL using a 2 (social/nonsocial) × 2 (valenced/neutral) factorial design in an fMRI experiment. Note that social knowledge has been very broadly defined, from the mere presence of persons (Mellem et al, 2016;Norris, Chen, Zhu, Small, & Cacioppo, 2004), to the biographical information of specific persons (Simmons et al, 2010;Wang et al, 2017), and to socially interactive behaviors or properties (Zahn et al, 2007).…”

Anterior temporal lobe and the representation of knowledge about people

“…Wang et al (5) asked 50 participants to learn biographical information (name, age, marital status, occupation, city of residence, and the appearance of their house as presented in a photograph) about four fictitious people over 2 d of training. On the third day, participants completed an fMRI experiment in which they were shown images of the four people's faces (pictured from different viewpoints with respect to the training), their names (written in a different font and color), their houses (pictured from different viewpoints), and images of objects associated with their occupation.…”

“…A model in which retrieval of person knowledge represented in the IPL and PCC from perceptual cues was mediated by the ATL ("ATL as hub") was selected as optimal by Bayesian model selection, outperforming a model in which retrieval was achieved directly from representations of the perceptual cues in the FFA/WVFA, and a model in which retrieval was mediated by the hippocampus. Furthermore, using psychophysiological interactions, Wang et al (5) showed that the ATL increased its connectivity with the IPL during the retrieval of a person's status, but with the PCC during the retrieval of a person's personality traits. Multivariate pattern analyses showed that status could be decoded from the IPL (and from none of the other ROIs), and personality traits could be decoded from the PCC (and from none of the other ROIs).…”