Neurons in the human medial temporal lobe (MTL) that are selective for the identity of specific people are classically thought to encode identity invariant to visual features. However, it remains largely unknown how visual information from higher visual cortex is translated into a semantic representation of an individual person. Here, we show that some MTL neurons are selective to multiple different face identities on the basis of shared features that form clusters in the representation of a deep neural network trained to recognize faces. Contrary to prevailing views, we find that these neurons represent an individual’s face with feature-based encoding, rather than through association with concepts. The response of feature neurons did not depend on face identity nor face familiarity, and the region of feature space to which they are tuned predicted their response to new face stimuli. Our results provide critical evidence bridging the perception-driven representation of facial features in the higher visual cortex and the memory-driven representation of semantics in the MTL, which may form the basis for declarative memory.

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.

Autism spectrum disorder (ASD) is characterized by difficulties in social processes, interactions, and communication. Yet, the neurocognitive bases underlying these difficulties are unclear. Here, we triangulated the ‘trans-diagnostic’ approach to personality, social trait judgments of faces, and neurophysiology to investigate (1) the relative position of autistic traits in a comprehensive social-affective personality space, and (2) the distinct associations between the social-affective personality dimensions and social trait judgment from faces in individuals with ASD and neurotypical individuals. We collected personality and facial judgment data from a large sample of online participants (N = 89 self-identified ASD; N = 307 neurotypical controls). Factor analysis with 33 subscales of 10 social-affective personality questionnaires identified a 4-dimensional personality space. This analysis revealed that ASD and control participants did not differ significantly along the personality dimensions of empathy and prosociality, antisociality, or social agreeableness. However, the ASD participants exhibited a weaker association between prosocial personality dimensions and judgments of facial trustworthiness and warmth than the control participants. Neurophysiological data also indicated that ASD participants had a weaker association with neuronal representations for trustworthiness and warmth from faces. These results suggest that the atypical association between social-affective personality and social trait judgment from faces may contribute to the social and affective difficulties associated with ASD.

An important question in human face perception research is to understand whether neural representation of faces is dynamically modulated by context. In particular, although there is a plethora of neuroimaging literature that has probed the neural representation of faces, few studies have investigated what low-level structural and textural facial features parametrically drive neural responses to faces and whether the representation of these features is modulated by the task. To answer these questions, we employed two task instructions when participants viewed the same faces. We first identified brain regions that parametrically encoded high-level social traits such as perceived facial trustworthiness and dominance, and we showed that these brain regions were modulated by task instructions. We then employed a data-driven computational face model with parametrically generated faces and identified brain regions that encoded low-level variation in the faces (shape and skin texture) that drove neural responses. We further analyzed the evolution of the neural feature vectors along the visual processing stream and visualized and explained these feature vectors. Together, our results showed a flexible neural representation of faces for both low-level features and high-level social traits in the human brain.

People instantaneously evaluate faces with significant agreement on evaluations of social traits.However, the neural basis for such rapid spontaneous face evaluation remains largely unknown.Here, we recorded from 490 neurons in the amygdala and hippocampus in 5 neurosurgical patients and show that amygdala and hippocampal neurons encode a social trait space. We further investigated the temporal evolution and modulation on the social trait representation, and we employed encoding and decoding models to reveal the critical social traits for the trait space.We also recorded from another 259 neurons and replicated our findings using different social traits. Lastly, the neuronal social trait space may have a behavioral consequence likely involved in the abnormal processing of social information in autism. Together, our results suggest that there exists a neuronal population code for a comprehensive social trait space in the human amygdala and hippocampus that underlie spontaneous first impressions.

Investigations into how individual neurons encode behavioral variables of interest have revealed specific representations in single neurons, such as place and object cells, as well as a wide range of cells with conjunctive encodings or mixed selectivity. However, as most experiments examine neural activity within individual tasks, it is currently unclear if and how neural representations change across different task contexts. Within this discussion, the medial temporal lobe is particularly salient, as it is known to be important for multiple behaviors including spatial navigation and memory, however the relationship between these functions is currently unclear. Here, to investigate how representations in single neurons vary across different task contexts in the MTL, we collected and analyzed single-neuron activity from human participants as they completed a paired-task session consisting of a passive-viewing visual working memory and a spatial navigation and memory task. Five patients contributed 22 paired-task sessions, which were spike sorted together to allow for the same putative single neurons to be compared between the different tasks. Within each task, we replicated concept-related activations in the working memory task, as well as target-location and serial-position responsive cells in the navigation task. When comparing neuronal activity between tasks, we first established that a significant number of neurons maintained the same kind of representation, responding to stimuli presentations across tasks. Further, we found cells that changed the nature of their representation across tasks, including a significant number of cells that were stimulus responsive in the working memory task that responded to serial position in the spatial task. Overall, our results support a flexible encoding of multiple, distinct aspects of different tasks by single neurons in the human MTL, whereby some individual neurons change the nature of their feature coding between task contexts.

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.

The human amygdala and hippocampus are critically involved in various processes in face perception. However, it remains unclear how task demands or evaluative contexts modulate processes underlying face perception. In this study, we employed two task instructions when participants viewed the same faces and recorded single-neuron activity from the human amygdala and hippocampus. We comprehensively analyzed task modulation for three key aspects of face processing and we found that neurons in the amygdala and hippocampus (1) encoded high-level social traits such as perceived facial trustworthiness and dominance and this response was modulated by task instructions; (2) encoded low-level facial features and demonstrated region-based feature coding, which was not modulated by task instructions; and (3) encoded fixations on salient face parts such as the eyes and mouth, which was not modulated by task instructions. Together, our results provide a comprehensive survey of task modulation of neural processes underlying face perception at the single-neuron level in the human amygdala and hippocampus.