Neural substrates of long-term item and source memory for emotional associates: An fMRI study

Since Tulving's influential work on the distinction between familiarity and recollection-based retrieval, numerous studies have found evidence for differential contribution of these retrieval mechanisms on emotional episodic memory. Particularly, retrieval advantage for emotional, compared to neutral, information has been related to recollection-, but not familiarity-mediated processes. Neuroimaging studies suggest that this recollection-based retrieval for emotional information is related to stronger engagement of regions in the medial temporal lobe (MTL), posterior parietal cortex (PPC), and prefrontal cortex (PFC). In the present study, we investigated neural correlates related to long-term memory of neutral information that has been associated with emotional and neutral contexts, using functional magnetic resonance imaging (fMRI). During encoding, different neutral objects integrated with emotional or neutral scenes were presented. One week later, the encoded objects were intermixed with new ones and participants had to indicate whether the objects were previously seen or not, using the Remember/Know procedure (item memory). Furthermore, memory for the correct scene background category was also tested (contextual source memory). First, replicating previous findings, we observed a preference for recollection-dependent memory retrieval versus familiarity-dependent memory retrieval for those neutral objects encoded in emotional compared to neutral contexts. Second, consistent with these behavioral effects, objects encoded with emotional, compared to neutral, scenes produced larger memory-related activity in recollection-sensitive brain regions, including PPC and PFC regions. Third, correctly retrieved emotional compared to neutral contextual information was associated with increased activity in these brain areas. Together, these results suggest that memory for information encoded in emotional contexts is remarkably robust over time and mediated by recollection-based processes.