Faces are salient social stimuli that attract a stereotypical pattern of eye movement. The human amygdala and hippocampus are involved in various aspects of face processing; however, it remains unclear how they encode the content of fixations when viewing faces. To answer this question, we employed single-neuron recordings with simultaneous eye tracking when participants viewed natural face stimuli. We found a class of neurons in the human amygdala and hippocampus that encoded salient facial features such as the eyes and mouth. With a control experiment using non-face stimuli, we further showed that feature selectivity was specific to faces. We also found another population of neurons that differentiated saccades to the eyes vs. the mouth. Population decoding confirmed our results and further revealed the temporal dynamics of face feature coding. Interestingly, we found that the amygdala and hippocampus played different roles in encoding facial features. Lastly, we revealed two functional roles of feature-selective neurons: 1) they encoded the salient region for face recognition, and 2) they were related to perceived social trait judgments. Together, our results link eye movement with neural face processing and provide important mechanistic insights for human face perception.
A central challenge in face perception research is to understand how neurons encode face identities. This challenge has not been met largely due to the lack of simultaneous access to the entire face processing neural network and the lack of a comprehensive multifaceted model capable of characterizing a large number of facial features. Here, we addressed this challenge by conducting in silico experiments using a pre-trained face recognition deep neural network (DNN) with a diverse array of stimuli. We identified a subset of DNN units selective to face identities, and these identity-selective units demonstrated generalized discriminability to novel faces. Visualization and manipulation of the network revealed the importance of identity-selective units in face recognition. Importantly, using our monkey and human single-neuron recordings, we directly compared the response of artificial units with real primate neurons to the same stimuli and found that artificial units shared a similar representation of facial features as primate neurons. We also observed a region-based feature coding mechanism in DNN units as in human neurons. Together, by directly linking between artificial and primate neural systems, our results shed light on how the primate brain performs face recognition tasks.
more » « less- Award ID(s):
- 2114644
- NSF-PAR ID:
- 10368104
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- Communications Biology
- Volume:
- 5
- Issue:
- 1
- ISSN:
- 2399-3642
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract -
more » « less
According to a classical view of face perception (Bruce and Young, 1986; Haxby et al., 2000), face identity and facial expression recognition are performed by separate neural substrates (ventral and lateral temporal face-selective regions, respectively). However, recent studies challenge this view, showing that expression valence can also be decoded from ventral regions (Skerry and Saxe, 2014; Li et al., 2019), and identity from lateral regions (Anzellotti and Caramazza, 2017). These findings could be reconciled with the classical view if regions specialized for one task (either identity or expression) contain a small amount of information for the other task (that enables above-chance decoding). In this case, we would expect representations in lateral regions to be more similar to representations in deep convolutional neural networks (DCNNs) trained to recognize facial expression than to representations in DCNNs trained to recognize face identity (the converse should hold for ventral regions). We tested this hypothesis by analyzing neural responses to faces varying in identity and expression. Representational dissimilarity matrices (RDMs) computed from human intracranial recordings (
n = 11 adults; 7 females) were compared with RDMs from DCNNs trained to label either identity or expression. We found that RDMs from DCNNs trained to recognize identity correlated with intracranial recordings more strongly in all regions tested—even in regions classically hypothesized to be specialized for expression. These results deviate from the classical view, suggesting that face-selective ventral and lateral regions contribute to the representation of both identity and expression.SIGNIFICANCE STATEMENT Previous work proposed that separate brain regions are specialized for the recognition of face identity and facial expression. However, identity and expression recognition mechanisms might share common brain regions instead. We tested these alternatives using deep neural networks and intracranial recordings from face-selective brain regions. Deep neural networks trained to recognize identity and networks trained to recognize expression learned representations that correlate with neural recordings. Identity-trained representations correlated with intracranial recordings more strongly in all regions tested, including regions hypothesized to be expression specialized in the classical hypothesis. These findings support the view that identity and expression recognition rely on common brain regions. This discovery may require reevaluation of the roles that the ventral and lateral neural pathways play in processing socially relevant stimuli. -
Photo Sleuth: Combining Collective Intelligence and Computer Vision to Identify Historical PortraitsIdentifying people in photographs is a critical task in a wide variety of domains, from national security [7] to journalism [14] to human rights investigations [1]. The task is also fundamentally complex and challenging. With the world population at 7.6 billion and growing, the candidate pool is large. Studies of human face recognition ability show that the average person incorrectly identifies two people as similar 20–30% of the time, and trained police detectives do not perform significantly better [11]. Computer vision-based face recognition tools have gained considerable ground and are now widely available commercially, but comparisons to human performance show mixed results at best [2,10,16]. Automated face recognition techniques, while powerful, also have constraints that may be impractical for many real-world contexts. For example, face recognition systems tend to suffer when the target image or reference images have poor quality or resolution, as blemishes or discolorations may be incorrectly recognized as false positives for facial landmarks. Additionally, most face recognition systems ignore some salient facial features, like scars or other skin characteristics, as well as distinctive non-facial features, like ear shape or hair or facial hair styles. This project investigates how we can overcome these limitations to support person identification tasks. By adjusting confidence thresholds, users of face recognition can generally expect high recall (few false negatives) at the cost of low precision (many false positives). Therefore, we focus our work on the “last mile” of person identification, i.e., helping a user find the correct match among a large set of similarlooking candidates suggested by face recognition. Our approach leverages the powerful capabilities of the human vision system and collaborative sensemaking via crowdsourcing to augment the complementary strengths of automatic face recognition. The result is a novel technology pipeline combining collective intelligence and computer vision. We scope this project to focus on identifying soldiers in photos from the American Civil War era (1861– 1865). An estimated 4,000,000 soldiers fought in the war, and most were photographed at least once, due to decreasing costs, the increasing robustness of the format, and the critical events separating friends and family [17]. Over 150 years later, the identities of most of these portraits have been lost, but as museums and archives increasingly digitize and publish their collections online, the pool of reference photos and information has never been more accessible. Historians, genealogists, and collectors work tirelessly to connect names with faces, using largely manual identification methods [3,9]. Identifying people in historical photos is important for preserving material culture [9], correcting the historical record [13], and recognizing contributions of marginalized groups [4], among other reasons.more » « less
-
In this paper, we propose a new deep framework which predicts facial attributes and leverage it as a soft modality to improve face identification performance. Our model is an end to end framework which consists of a convolutional neural network (CNN) whose output is fanned out into two separate branches; the first branch predicts facial attributes while the second branch identifies face images. Contrary to the existing multi-task methods which only use a shared CNN feature space to train these two tasks jointly, we fuse the predicted attributes with the features from the face modality in order to improve the face identification performance. Experimental results show that our model brings benefits to both face identification as well as facial attribute prediction performance, especially in the case of identity facial attributes such as gender prediction. We tested our model on two standard datasets annotated by identities and face attributes. Experimental results indicate that the proposed model outperforms most of the current existing face identification and attribute prediction methods.more » « less
-
Recent neuroimaging evidence challenges the classical view that face identity and facial expression are processed by segregated neural pathways, showing that information about identity and expression are encoded within common brain regions. This article tests the hypothesis that integrated representations of identity and expression arise spontaneously within deep neural networks. A subset of the CelebA dataset is used to train a deep convolutional neural network (DCNN) to label face identity (chance = 0.06%, accuracy = 26.5%), and the FER2013 dataset is used to train a DCNN to label facial expression (chance = 14.2%, accuracy = 63.5%). The identity-trained and expression-trained networks each successfully transfer to labeling both face identity and facial expression on the Karolinska Directed Emotional Faces dataset. This study demonstrates that DCNNs trained to recognize face identity and DCNNs trained to recognize facial expression spontaneously develop representations of facial expression and face identity, respectively. Furthermore, a congruence coefficient analysis reveals that features distinguishing between identities and features distinguishing between expressions become increasingly orthogonal from layer to layer, suggesting that deep neural networks disentangle representational subspaces corresponding to different sources.more » « less
