Social Processing and Neural Plasticity

National Institute Of Mental Health

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Abstract

Neuroscientists studying the brain use stimuli with different levels of complexity to study the neural mechanism of sight. These stimuli range from dots and lines, to faces and bodies. Decades of investigation using electrophysiological and functional imaging methods have revealed that the brains of humans and animals are replete with neurons that respond selectively to particular visual features. These favored features are of many types, with brain areas organized in an apparent cascade of simpler features identified early in the pipeline, and more complex ones identified later. Selectively responding neurons are often said to represent individual visual features. The normal interplay between primates does not much resemble the contrived and controlled experiments that have given rise to our theories about brain function. A logical question, then, is whether a neuron that represents a feature, say a face, in one context will also represent that face in a different context. Humans are a particularly large primate species, but are typical of primates in some ways, such as the abundant use of vision to mediate interaction with others. The primate brain has a significant fraction of its billions of neurons dedicated to the processing of social stimuli. An exciting challenge for neuroscientists is to understand how the neural representation of stimuli gleaned from conventional testing paradigms bears on perception and behavior under more natural conditions. Over the past year, we have used extensively a microwire bundle array developed and modified in the laboratory to longitudinally track the activity of cells in the brain that reside in so-called face patches, which are small, circumscribed regions showing greater fMRI responses to faces than to other categories of stimuli. We recently investigated fMRI responses in the face patches of both macaques (Russ et al.,2015) and marmosets (Hung et al., 2015). Within the last year, we have continued this line of research in both species, with new results published in the macaque. In one free-viewing study in the macaque, we tracked the relative contribution of motion caused by the subjects own eye movements to the fMRI signals in the brain (Russ et al., 2016). In this study, we showed that the brain areas responding to the motion in a movie video were very different than those responsive to an animals own eye movements. In another study (Park et al., 2017) which is a follow up to a previous electrophysiology study (McMahon et al., 2015), we developed a new method for understanding the surprising functional diversity of neurons within <1mm3 area in the cerebral cortex. That study tracked the time course of both neuron activity and fMRI activity in monkeys watching 5-minute movies. By comparing the time courses of voxels throughout the brain to each neurons response, we obtained whole-brain activity maps for each neuron. This method then allowed us to classify neurons based on their affiliation with other areas throughout the brain. Multiple other studies are underway in the laboratory, in both macaques and marmosets. In the macaques, for example, we are presently preparing a manuscript that describes the way in which neurons in face patches respond to the facial identity of monkey and human faces (Koyano et al., in preparation). This study is in many ways a follow up to a study published more than a decade ago (Leopold et al., 2006), and is closely related to recent work published by Doris Tsao and colleagues. This work highlights the important role of the average face, which serves as a learned norm to steer the brains perception of individual identity. In the marmoset, we are setting up to investigate the developmental plasticity of face identity learning, using a combination of microelectrode and optical imaging methods. A common theme in these projects is an ethological and evolutionary perspective as they shape theories of brain function. To that end, in the last year we have published three reviews and commentaries on the topic of social neuroscience and evolution. One of these, published in Jon Kaass 4-volume set Evolution of Nervous Systems, focuses on the evolution of high-level visual specialization in primates (Leopold et al., 2017). Another is a discussion of the use of marmosets as a model to study issues in social neuroscience (Miller et al., Neuron, 2016). The last of these is a highlight of a recent study in human patients, where naturalistic viewing was combined with intracranial ECoG recordings (Leopold and Russ, 2017).