Forgotten but not gone: FMRI evidence of implicit memory for negative stimuli 24 hours after the initial study episode

Abstract

Endel Tulving conducted pioneering work on the explicit and implicit memory systems and demonstrated that priming effects can be long-lasting. It is also well-established that emotion can amplify explicit and implicit memory. Prior work has utilized repetition suppression (RS) of the fMRI-BOLD signal-a reduction in the magnitude of activity over repeated presentations of stimuli-to index implicit memory. Using an explicit recognition memory paradigm, we examined emotional modulation of long-term implicit memory effects as revealed by repetition suppression (i.e., comparing second-exposure forgotten items to first-exposure correct rejections). Forty-seven participants incidentally encoded line-drawings of negative, positive, and neutral scenes followed by the full color image. Twenty-four hours later, participants underwent fMRI during a recognition memory test in which old and new line-drawings were presented. Implicit and explicit memory effects were defined by the contrasts of New-Correct Rejections > Old-Misses and Old-Hits > New-Correct Rejections, respectively. Wide-spread Negative RS was found in frontal and occipito-temporal cortex that was greater than Neutral RS in the right orbito-frontal cortex and inferior frontal gyri. Valence-specific Negative RS, compared to Positive RS, was observed in the left inferior occipital gyrus. There was no strong evidence for emotional modulation of amygdala RS, but functional connectivity analyses revealed valence-specificity: Negative and positive valence were associated with repetition suppression and repetition enhancement of amygdala-occipital connectivity, respectively. Negative implicit memory patterns in most frontal regions-but not occipital areas-overlapped with explicit memory effects. Thus, implicit memory effects for a single visual stimulus presentation are modulated by emotional valence, can be observed 24hours after initial exposure, and show some overlap with explicit memory.

Keywords: Amygdala; Emotion; Implicit memory; Neural priming; Repetition suppression; Valence.