Dissociable networks for the expectancy and perception of emotional stimuli in the human brain

Abstract

William James posited that comparable brain regions were implicated in the anticipation and perception of a stimulus; however, dissociable networks (at least in part) may also underlie these processes. Recent functional neuroimaging studies have addressed this issue by comparing brain systems associated with the expectancy and perception of visual, tactile, nociceptive, and reward stimuli. In the present fMRI study, we addressed this issue in the domain of pictorial emotional stimuli (IAPS). Our paradigm involved the experimental conditions emotional expectancy, neutral expectancy, emotional picture perception, and neutral picture perception. Specifically, the emotional expectancy cue was uncertain in that it did not provide additional information regarding the positive or negative valence of the subsequent picture. Neutral expectancy and neutral picture perception served as control conditions, allowing the identification of expectancy and perception effects specific for emotion processing. To avoid contamination of the perception conditions by the preceding expectancy periods, 50% of the pictorial stimuli were presented without preceding expectancy cues. We found that the emotional expectancy cue specifically produced activation in the supracallosal anterior cingulate, cingulate motor area, and parieto-occipital sulcus. These regions were not significantly activated by emotional picture perception which recruited a different neuronal network, including the amygdala, insula, medial and lateral prefrontal cortex, cerebellum, and occipitotemporal areas. This dissociation may reflect a distinction between anticipatory and perceptive components of emotional stimulus processing.