Flexible visual recognition, such as that required for social perception, is a notoriously difficult problem for the brain to solve. Ultimately, visual recognition is based on the decoding of the retinal imaging. However, the retinal image cast by a given person's face is never the same twice, and the brain therefore needs to categorize very different images as corresponding to the same person. For example, each time a friend or relative is seen, they are illuminated differently, are seen from a different angle, and are wearing different clothes. Moreover, the internal features of the face will have a different, as the expression-producing muscles give rise to an infinite number of different poses. Nonetheless, the recognition of a familiar individual is immediate and effortless. We are interested in how the brain accomplishes this task, and how social information such as emotional or attentional state, can be extracted based on facial features. Central to understanding the remarkable flexibility in face recognition is plasticity and learning. To this end, we are presently using two approaches to understand how complex stimuli are learned, encoded and stored in high-level visual cortex. In one approach, we are using implanted microwire bundle electrodes to longitudinally track neural responses to faces and other objects during periods of focused learning. We previously demonstrated that in the absence of learning pressures, neurons in the macaque inferotemporal cortex exhibited near-complete stability in their responses over periods exceeding two weeks. This finding raised the question whether learning new stimuli would give rise to changes in neural tuning when monkeys learned new faces, either as individuals, categories, or artificial races. We are presently investigating this issue, with initial results suggesting that training can significantly affect the tuning of inferotemporal neurons. This was shown most clearly using a paradigm the monkey learned positive or negative reward values for a large number of face and non-face stimuli, after which the responses of the learned stimuli differed markedly and the difference lasted for the remaining week of recording. A second paradigm examines the effect of visual priming, or previous exposure, on fMRI responses to stimuli throughout the brain. In priming, previously viewed stimuli generate faster responses than those seen for the first time. As a first step toward investigating the neurobiological basis of priming the macaque prefrontal and temporal cortices, we have recently implemented a novel event-related design in awake monkeys. These findings demonstrate that fMRI responses to previously viewed stimuli are significantly lower in several patches of cortex. We are presently investigating the relationship between these cortical sites and areas known to show selective responses for social stimuli such as faces and bodies. Both longitudinal single-cell recordings and event-related fMRI recordings during priming tap into the cortical plasticity in the brain that characterizes adult learning of social stimuli. Deficits in social learning are characteristic of a number of psychiatric disorders, whose origins are thought to be developmental. However, since cortical learning of social stimuli remains malleable in the adult, gaining a deeper understanding of the cortical changes involved is an important step toward developing interventions to help individuals that have specific difficulty with visual social cognition.
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