Anterior temporal lobe and the representation of knowledge about people

Abstract

Patients with semantic dementia (SD), a neurodegenerative disease affecting the anterior temporal lobes (ATL) (1), present with striking cognitive deficits: they can have difficulties naming objects and familiar people from both pictures and descriptions (2, 3). Furthermore, SD patients make semantic errors (e.g., naming "horse" a picture of a zebra), suggesting that their impairment affects object knowledge rather than lexical retrieval. Because SD can affect object categories as disparate as artifacts, animals, and people, as well as multiple input modalities, it has been hypothesized that ATL is a semantic hub (4) that integrates information across multiple modality-specific brain regions into multimodal representations. With a series of converging experiments using multiple analysis techniques, Wang et al. (5) test the proposal that ATL is a semantic hub in the case of person knowledge, investigating whether ATL: (i) encodes multimodal representations of identity, and (ii) mediates the retrieval of knowledge about people from representations of perceptual cues.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. Multimodal representations of person identity were probed in a set of regions-of-interest (ROIs), training a support vector machine to classify between different face identities, and testing it to classify between the associated names, houses, and occupation-related objects. All four classifications were significant in the ATL, and none of the classifications was significant in any of the other ROIs, showing that ATL representations of person identity generalize across a variety of stimulus types. The ATL has been previously shown to encode information about face identity (6), generalizing across facial expressions (7), viewpoints (8), and face parts (9).The ATL has also been implicated in the association of names and faces with knowledge about people (10, 11). Wang et al.'s (5) classification results are an important extension of this work, revealing representations of identity that generalize across faces, names, and objects associated with one individual.In the ATL-hub hypothesis, the ATL acts as an intermediary for the linkage of different kinds of knowledge represented in specialized brain regions. To test this proposal, in a second study, Wang et al. (5) defined a set of ROIs showing stronger responses when retrieving information about a person compared with a resting baseline. The contrast identified as ROIs the left ATL, hippocampus, posterior cingulate (PCC), i...

Neural similarity between mentalizing and live social interaction

“…Consistent with the idea that the ATL supports the integration of online and offline social processes, different lines of research have demonstrated the convergence of multimodal, social information processing streams in the anterior portions of the temporal lobe. Ventral areas of the ATL are involved in the encoding and retrieval of person-specific knowledge (e.g., name and biographical information; 16,21,54,55), while more dorsal, anterior portions of the ATL are considered a semantic hub for abstract social knowledge (14,18,(56)(57)(58)(59)(60). Our findings span the middle ground between the aforementioned lines of research, such that our findings suggest an integration of person-specific and abstract social knowledge representations.…”

“…However, these regions are also associated with other functions that may play a role in social interaction. For example, the ATL and STS are also associated with the representation of person-specific information (14)(15)(16)(17)(18)(19)(20)(21), while the IFG has been implicated in a range of executive processes, such as working memory and behavioral inhibition (22)(23)(24). Thus, it is unclear if the overlapping activity associated with social interaction reported by Alkire et al (11) is specific to mentalizing or reflects other higher-order cognitive processes.…”

Neural similarity between mentalizing and live social interaction during the transition to adolescence

“…Consistent with the idea that the ATL supports the integration of online and offline social processes, different lines of research have demonstrated the convergence of multimodal, social information processing streams in the anterior portions of the temporal lobe. Ventral areas of the ATL have been associated with the representations of person‐specific knowledge (e.g., names, faces, and biographical information; Anzellotti, 2017 ; Blank et al, 2015 ; Borghesani et al, 2019 ; Kriegeskorte et al, 2007 ; Wang et al, 2017 ), while more dorsal, anterior portions of the ATL are considered to be a semantic hub for abstract social concepts (including mental‐state concepts; Arioli et al, 2020 ; Olson et al, 2007 , 2013 ; Skipper et al, 2011 ; Wang et al, 2019 ; Zahn et al, 2007 ). Conceptually, our findings span the middle ground between the aforementioned lines of research in that our results suggest that peer‐specific and abstract knowledge about mental states are integrated and represented similarly in the ATL.…”

“…For instance, Alkire et al ( 2018 ) reported overlapping activations in the ATL, STS, and IFG when children reasoned about the mental state of an abstract character and when they engaged in social interactions that did not explicitly require mental state reasoning, and inferred that social interaction may induce spontaneous mentalizing. However, these brain regions are associated with other, higher‐order cognitive processes that may be important for social interactions—the ATL and STS are associated with the representation of person‐specific information (Anzellotti, 2017 ; Anzellotti & Caramazza, 2017 ; Blank et al, 2015 ; Collins et al, 2016 ; Olson et al, 2013 ; Perrodin et al, 2015 ; Simmons et al, 2010 ; Wang et al, 2017 ), and the IFG is implicated in a range of executive processes, such as working memory and behavioral inhibition (Breitling et al, 2020 ; Drummond et al, 2017 ; Hartwigsen et al, 2019 ). Thus, it is unclear if the overlapping activity associated with social interaction reported by Alkire et al ( 2018 ) is specific to mentalizing, or reflects other cognitive processes utilized within social interactive contexts.…”

Evidence for a general neural signature of face familiarity

“…For example, regions considered to be outside the core face networks, such as different extrastriate visual areas, the structures in the anterior and medial temporal lobe (MTL) have been reliably demonstrated to exhibit stronger responses to familiar stimuli, including faces. The anterior temporal lobe (ATL), considered to be a semantic hub (Anzellotti, 2017), is involved in associations of person-related semantics (Morton et al, 2021), e.g. a connection between a name and a face (Tsukiura et al, 2010).…”