Attentional modulation of learning-related repetition attenuation effects in human parahippocampal cortex

Two of the most fundamental processes in biological vision are attention and learning. Attention actively selects and enhances visual information that is most relevant to behavior. Learning enables the visual system to benefit from perceptual experience. The amount of visual information to learn is infinite; however, top-down control mechanisms must somehow regulate learning to achieve an adaptive balance between plasticity and stability in neural circuitry. Functional magnetic resonance imaging (fMRI) can measure learning-related changes in neural activity to previously viewed perceptual stimuli. Described variably as the repetition suppression or adaptation effect, the attenuation in neural activity to repeated stimuli versus novel stimuli provides a marker for stimuli-specific perceptual processing and memory. One important issue concerns whether repetition attenuation is automatic or not, and recent work has begun to show that it is sensitive to task demands. Accordingly, the present study further examined how attention controls the attenuated response to repeated stimuli, specifically testing whether attention is important for initial encoding, for the expression of memory traces, or for both encoding and expression. To manipulate attention, we used overlapping scene and face images and asked subjects to attend to either category. fMRI revealed significant attenuation in the parahippocampal place area for only the repeated scenes that were attended both during the initial presentation and during repetition. Thus, attention actively governs when neuronal activity is attenuated to repeated perceptual input, and such attention is important during both initial encoding and subsequent expression of the learned information.