Jessica A. Collins

Beyond the FFA: The Role of the Ventral Anterior Temporal Lobes in Face Processing

Extensive research has supported the existence of a specialized face-processing network that is distinct from the visual processing areas used for general object recognition. The majority of this work has been aimed at characterizing the response properties of the fusiform face area (FFA) and the occipital face area (OFA), which together are thought to constitute the core network of brain areas responsible for facial identification. Although accruing evidence has shown that face-selective patches in the ventral anterior temporal lobes (vATLs) are interconnected with the FFA and OFA, and that they play a role in facial identification, the relative contribution of these brain areas to the core face-processing network has remained unarticulated. Here we review recent research critically implicating the vATLs in face perception and memory. We propose that current models of face processing should be revised such that the ventral anterior temporal lobes serve a centralized role in the visual face-processing network. We speculate that a hierarchically organized system of face processing areas extends bilaterally from the inferior occipital gyri to the vATLs, with facial representations becoming increasingly complex and abstracted from low-level perceptual features as they move forward along this network. The anterior temporal face areas may serve as the apex of this hierarchy, instantiating the final stages of face recognition. We further argue that the anterior temporal face areas are ideally suited to serve as an interface between face perception and face memory, linking perceptual representations of individual identity with person-specific semantic knowledge.

Knowledge is power: How conceptual knowledge transforms visual cognition

In this review, we synthesize the existing literature demonstrating the dynamic interplay between conceptual knowledge and visual perceptual processing. We consider two theoretical frameworks that demonstrate interactions between processes and brain areas traditionally considered perceptual or conceptual. Specifically, we discuss categorical perception, in which visual objects are represented according to category membership, and highlight studies showing that category knowledge can penetrate early stages of visual analysis. We next discuss the embodied account of conceptual knowledge, which holds that concepts are instantiated in the same neural regions required for specific types of perception and action, and discuss the limitations of this framework. We additionally consider studies showing that gaining abstract semantic knowledge about objects and faces leads to behavioral and electrophysiological changes that are indicative of more efficient stimulus processing. Finally, we consider the role that perceiver goals and motivation may play in shaping the interaction between conceptual and perceptual processing. We hope to demonstrate how pervasive such interactions between motivation, conceptual knowledge, and perceptual processing are in our understanding of the visual environment, and to demonstrate the need for future research aimed at understanding how such interactions arise in the brain.

Focal temporal pole atrophy and network degeneration in semantic variant primary progressive aphasia

A wealth of neuroimaging research has associated semantic variant primary progressive aphasia with distributed cortical atrophy that is most prominent in the left anterior temporal cortex; however, there is little consensus regarding which region within the anterior temporal cortex is most prominently damaged, which may indicate the putative origin of neurodegeneration. In this study, we localized the most prominent and consistent region of atrophy in semantic variant primary progressive aphasia using cortical thickness analysis in two independent patient samples (n = 16 and 28, respectively) relative to age-matched controls (n = 30). Across both samples the point of maximal atrophy was located in the same region of the left temporal pole. This same region was the point of maximal atrophy in 100% of individual patients in both semantic variant primary progressive aphasia samples. Using resting state functional connectivity in healthy young adults (n = 89), we showed that the seed region derived from the semantic variant primary progressive aphasia analysis was strongly connected with a large-scale network that closely resembled the distributed atrophy pattern in semantic variant primary progressive aphasia. In both patient samples, the magnitude of atrophy within a brain region was predicted by that region’s strength of functional connectivity to the temporopolar seed region in healthy adults. These findings suggest that cortical atrophy in semantic variant primary progressive aphasia may follow connectional pathways within a large-scale network that converges on the temporal pole.

Variation in White Matter Connectivity Predicts the Ability to Remember Faces and Discriminate Their Emotions

OBJECTIVES The extended face network contains clusters of neurons that perform distinct functions on facial stimuli. Regions in the posterior ventral visual stream appear to perform basic perceptual functions on faces, while more anterior regions, such as the ventral anterior temporal lobe and amygdala, function to link mnemonic and affective information to faces. Anterior and posterior regions are interconnected by a long-range white matter tracts; however, it is not known if variation in connectivity of these pathways explains cognitive performance. METHODS Here, we used diffusion imaging and deterministic tractography in a cohort of 28 neurologically normal adults ages 18-28 to examine microstructural properties of visual fiber pathways and their relationship to certain mnemonic and affective functions involved in face processing. We investigated how inter-individual variability in two tracts, the inferior longitudinal fasciculus (ILF) and the inferior fronto-occipital fasciculus (IFOF), related to performance on tests of facial emotion recognition and face memory. RESULTS Results revealed that microstructure of both tracts predicted variability in behavioral performance indexed by both tasks, suggesting that the ILF and IFOF play a role in facilitating our ability to discriminate emotional expressions in faces, as well as to remember unique faces. Variation in a control tract, the uncinate fasciculus, did not predict performance on these tasks. CONCLUSIONS These results corroborate and extend the findings of previous neuropsychology studies investigating the effects of damage to the ILF and IFOF, and demonstrate that differences in face processing abilities are related to white matter microstructure, even in healthy individuals.

Dynamic neural architecture for social knowledge retrieval

Significance Knowledge about other people is critical for group survival and may have unique cognitive processing demands. Here, we investigate how person knowledge is represented, organized, and retrieved in the brain. We show that the anterior temporal lobe (ATL) stores abstract person identity representation that is commonly embedded in multiple sources (e.g. face, name, scene, and personal object). We also found the ATL serves as a “neural switchboard,” coordinating with a network of other brain regions in a rapid and need-specific way to retrieve different aspects of biographical information (e.g., occupation and personality traits). Our findings endorse the ATL as a central hub for representing and retrieving person knowledge. 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.

Flortaucipir tau PET imaging in semantic variant primary progressive aphasia

Objective The semantic variant of primary progressive aphasia (svPPA) is typically associated with frontotemporal lobar degeneration (FTLD) with longTAR DNA-binding protein (TDP)-43-positive neuropil threads and dystrophic neurites (type C), and is only rarely due to a primary tauopathy or Alzheimer’s disease. We undertook this study to investigate the localisation and magnitude of the presumed tau Positron Emission Tomography (PET) tracer [18F]Flortaucipir (FTP; also known as T807 or AV1451) in patients with svPPA, hypothesising that most patients would not show tracer uptake different from controls. Methods FTP and [11C]Pittsburgh compound B PET imaging as well as MRI were performed in seven patients with svPPA and in 20 controls. FTP signal was analysed by visual inspection and by quantitative comparison to controls, with and without partial volume correction. Results All seven patients showed elevated FTP uptake in the anterior temporal lobe with a leftward asymmetry that was not observed in healthy controls. This elevated FTP signal, largely co-localised with atrophy, was evident on both visual inspection and quantitative cortical surface-based analysis. Five patients were amyloid negative, one was amyloid positive and one has an unknown amyloid status. Conclusions In this series of patients with clinical profiles, structural MRI and amyloid PET imaging typical for svPPA, FTP signal was unexpectedly elevated with a spatial pattern localised to areas of atrophy. This raises questions about the possible off-target binding of this tracer to non-tau molecules associated with neurodegeneration. Further investigation with autopsy analysis will help illuminate the binding target(s) of FTP in cases of suspected FTLD-TDP neuropathology.

More Than Meets the Eye: The Merging of Perceptual and Conceptual Knowledge in the Anterior Temporal Face Area.

An emerging body of research has supported the existence of a small face sensitive region in the ventral anterior temporal lobe (ATL), referred to here as the “anterior temporal face area”. The contribution of this region in the greater face-processing network remains poorly understood. The goal of the present study was to test the relative sensitivity of this region to perceptual as well as conceptual information about people and objects. We contrasted the sensitivity of this region to that of two highly-studied face-sensitive regions, the fusiform face area (FFA) and the occipital face area (OFA), as well as a control region in early visual cortex (EVC). Our findings revealed that multivoxel activity patterns in the anterior temporal face area contain information about facial identity, as well as conceptual attributes such as one’s occupation. The sensitivity of this region to the conceptual attributes of people was greater than that of posterior face processing regions. In addition, the anterior temporal face area overlaps with voxels that contain information about the conceptual attributes of concrete objects, supporting a generalized role of the ventral ATLs in the identification and conceptual processing of multiple stimulus classes.

Conceptual knowledge attenuates viewpoint dependency in visual object recognition

Learning verbal semantic knowledge for objects has been shown to attenuate recognition costs incurred by changes in view from a learned viewpoint. Such findings were attributed to the semantic or meaningful nature of the learned verbal associations. However, recent findings demonstrate surprising benefits to visual perception after learning even noninformative verbal labels for stimuli. Here we test whether learning verbal information for novel objects, independent of its semantic nature, can facilitate a reduction in viewpoint-dependent recognition. To dissociate more general effects of verbal associations from those stemming from the semantic nature of the associations, participants learned to associate semantically meaningful (adjectives) or nonmeaningful (number codes) verbal information with novel objects. Consistent with a role of semantic representations in attenuating the viewpoint-dependent nature of object recognition, the costs incurred by a change in viewpoint were attenuated for stimuli with learned semantic associations relative to those associated with nonmeaningful verbal information. This finding is discussed in terms of its implications for understanding basic mechanisms of object perception as well as the classic viewpoint-dependent nature of object recognition.

The neural representation of social status in the extended face-processing network

Social status is a salient cue that shapes our perceptions of other people and ultimately guides our social interactions. Despite the pervasive influence of status on social behavior, how information about the status of others is represented in the brain remains unclear. Here, we tested the hypothesis that social status information is embedded in our neural representations of other individuals. Participants learned to associate faces with names, job titles that varied in associated status, and explicit markers of reputational status (star ratings). Trained stimuli were presented in an functional magnetic resonance imaging experiment where participants performed a target detection task orthogonal to the variable of interest. A network of face‐selective brain regions extending from the occipital lobe to the orbitofrontal cortex was localized and served as regions of interest. Using multivoxel pattern analysis, we found that face‐selective voxels in the lateral orbitofrontal cortex – a region involved in social and nonsocial valuation, could decode faces based on their status. Similar effects were observed with two different status manipulations – one based on stored semantic knowledge (e.g., different careers) and one based on learned reputation (e.g., star ranking). These data suggest that a face‐selective region of the lateral orbitofrontal cortex may contribute to the perception of social status, potentially underlying the preferential attention and favorable biases humans display toward high‐status individuals.

Functional connectivity in category-selective brain networks after encoding predicts subsequent memory

Activity in category selective regions of the temporal and parietal lobes during encoding has been associated with subsequent memory for face and scene stimuli. Reactivation theories of memory consolidation predict that after encoding connectivity between these category‐selective regions and the hippocampus should be modulated and predict recognition memory. However, support for this proposal has been limited in humans. Here, participants completed a resting‐state functional MRI (fMRI) scan, followed by face‐ and place‐encoding tasks, followed by another resting‐state fMRI scan during which they were asked to think about the stimuli they had previously encountered. Individual differences in face recognition memory were predicted by the degree to which connectivity between face‐responsive regions of the fusiform gyrus and perirhinal cortex increased following the face‐encoding task. In contrast, individual differences in scene recognition were predicted by connectivity between the hippocampus and a scene‐selective region of the retrosplenial cortex before and after the place‐encoding task. Our results provide novel evidence for category specificity in the neural mechanisms supporting memory consolidation.