Changes in human brain dynamics during behavioral priming and repetition suppression

Behavioral responses to a perceptual stimulus are typically faster with repeated exposure to the stimulus (behavioral priming). This implicit learning mechanism is critical for survival but impaired in a variety of neurological disorders, including Alzheimer's disease. Many studies of the neural bases for behavioral priming have encountered an interesting paradox: in spite of faster behavioral responses, repeated stimuli usually elicit weaker neural responses (repetition suppression). Several neurophysiological models have been proposed to resolve this paradox, but noninvasive techniques for human studies have had insufficient spatial-temporal precision for testing their predictions. Here, we used the unparalleled precision of electrocorticography (ECoG) to analyze the timing and magnitude of task-related changes in neural activation and propagation while patients named novel vs repeated visual objects. Stimulus repetition was associated with faster verbal responses and decreased neural activation (repetition suppression) in ventral occipito-temporal cortex (VOTC) and left prefrontal cortex (LPFC). Interestingly, we also observed increased neural activation (repetition enhancement) in LPFC and other recording sites. Moreover, with analysis of high gamma propagation we observed increased top-down propagation from LPFC into VOTC, preceding repetition suppression. The latter results indicate that repetition suppression and behavioral priming are associated with strengthening of top-down network influences on perceptual processing, consistent with predictive coding models of repetition suppression, and they support a central role for changes in large-scale cortical dynamics in achieving more efficient and rapid behavioral responses.