Social Processing and Neural Plasticity

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The core operations of social perception, memory, abstraction, and behavior derive from specialized brain circuits that are shaped through abundant experience during childhood and beyond. This role of experience means that the brains of individuals differ in their capacities and, to some extent, in their organization and physiology. In the case of brain damage and diseases, the differences in the brain translate directly to changes in abilities. For example, damage to very specific parts of the temporal lobe can lead to the inability to recognize individual faces while not affecting the recognition of other objects. Damage in other areas can leave subjects with a difficulty in recognizing facial expression, voice intonation, or even prompt them to believe that their spouse is an impostor. Similarly, abnormal development of the circuits in psychiatric diseases, for example those spurring social interaction, can lead to debilitating perceptual deficits in understanding social information. While researchers have understood for approximately 50 years that the visual brain is specialized for social information, the manner in which this specialization comes about, is refined over time, and supports our fluid social behavior remains poorly understood. The brain is inherently adaptable, particularly in early life. In our laboratory, we employ methods that allow us to track neural activity patterns over time, including days, weeks, and even months. This set of tools, which includes functional magnetic resonance imaging (fMRI), single-cell recordings, and optical recordings, allows us to study how visual perceptual learning of social stimuli is expressed in the brain. We have focused much of this work on face patches, which are small, circumscribed regions of the temporal and prefrontal cortex showing greater fMRI responses to faces than to other categories of stimuli. The longitudinal nature of our studies allows us to investigate plasticity over multiple time scales. This research has been further aided by our development of an avatar face stimulus, whose animation, facial expressions, and environmental context is under complete experimental control. This stimulus toolbox has been of great use for systematically studying the factors that determine neural firing, for example in the context of the geometry of natural vision. In the past year, we have published papers related to important aspects of face perception. For example, we demonstrated that auditory and visual information are integrated among face-selective neurons during vocal behavior (Khandhadia et al, 2021). While this integration was pronounced in one face selective region concerned with facial expression, it was nearly entirely absent in a different region concerned with face identity. We also provided evidence that the recognition of facial identity utilizes learned, internal representation of the average face (Koyano et al, 2021). This normative stimulus shapes the responses of neurons across face patches, highlighting the distinctive, and hence recognizable, facial features. The brains use of norms for face recognition was originally hypothesized based on psychophysical studies. Our demonstration of a clear neural representation of the average face within the face patch system bolsters this view and suggests a more general mode by which the brain gathers and stores information through its natural experience. In a different study, which is now accepted for publication (Waidmann et al, 2022), we took an entirely different approach to understanding the determinants of neural responses to faces. In that study, we investigated critical facial elements for driving neurons in different face patches. Facial elements were randomly intermixed on different images, for example with the eyes from one individual presented randomly with the mouths, heads, and bodies from many other individuals. One striking result from this combinatorial approach was the extent to which a very small region of a given face can determine the neuron's response, and the extent to which responses to this important feature are robust to major changes to the scene. For example, neurons responding selectively to one set of eyes often continue to respond to those eyes even when they are placed within a different face, which is attached to a different body and placed in a different scene. The local domination of such features was surprising, particularly as they were measured from the same neural populations as the norm-based coding findings mentioned above. In another study , we are investigating the role of natural geometry in the encoding of faces. The role of physical geometry, such as the metric size of a face and distance to the observer in centimeters, has not been studied. We used our avatar face to establish that neurons in face selective patches are highly sensitive to factors such as face size. Moreover, in using different size/distance combinations, we were able to determine that the critical variable shaping size responses was the physical size in centimeters, rather than the retinal angle in degrees. This study suggests that the encoding of objects in the ventral visual pathway incorporates information about the natural geometry of objects, as well as its physical location within a scene. In a final study, we have been tracing the cellular Ca++ fluorescence responses following the presentation of faces and other image stimuli. Similar to the microelectrode recordings, these recordings also permit longitudinal tracking over weeks and months. The present study aims to understand the nature of cellular selectivity, as well as the similarity of preference among neighboring neurons. In the future, our Ca++ fluorescence work will also be used to investigate whether neurons in face selective areas modify their response profiles as the subjects learn new faces.