The Privileged Brain Representation of First Olfactory Associations

Authors, poets, and scientists have been fascinated by the strength of childhood olfactory memories. Indeed, in long-term memory, the first odor-to-object association was stronger than subsequent associations of the same odor with other objects. Here we tested the hypothesis that first odor associations enjoy a privileged brain representation. Because emotion impacts memory, we further asked whether the pleasantness of an odor would influence such a representation. On day 1, we associated the same visual objects initially with one, and subsequently with a second, set of pleasant and unpleasant olfactory and auditory stimuli. One week later, we presented the same visual objects and tested odor-associative memory concurrent with functional magnetic resonance brain imaging. We found that the power (% remembered) of early associations was enhanced when they were unpleasant, regardless of whether they were olfactory or auditory. Brain imaging, however, revealed a unique hippocampal activation for early olfactory but not auditory associations, regardless of whether they were pleasant or unpleasant. Activity within the hippocampus on day 1 predicted the olfactory but not auditory associations that would be remembered one week later. These findings confirmed the hypothesis of a privileged brain representation for first olfactory associations.