The dorsolateral prefrontal cortex contributes to successful relational memory encoding

Abstract

Results from neuroimaging studies of long-term memory (LTM) encoding have contributed to the view that the ventrolateral prefrontal cortex (VLPFC) contributes to successful LTM formation, whereas the dorsolateral prefrontal cortex (DLPFC) does not. We hypothesized that the DLPFC does contribute to LTM, but under specific circumstances. That is, the DLPFC may be critical for building relationships between items during on-line processing, and this may promote LTM for associations between items. We used event-related functional magnetic resonance imaging (fMRI) to test this hypothesis by examining brain activity during sequential encoding of unrelated word pairs. During presentation of the second ("target") word in each pair, subjects either made a semantic judgment specific to the target word ("item-specific" trials), or a semantic judgment that involved a comparison between the target word and the first word in the pair ("relational" trials). Behaviorally, recognition memory for target words was equivalent between the two trial types but associative recognition of studied word pairs was significantly greater for relational trials. fMRI results showed that DLPFC activity was greater during relational compared with item-specific encoding and that DLPFC activity predicted successful memory for associations but not successful item memory. Activity in the VLPFC was also greater for relational compared with item-specific encoding, but VLPFC activation predicted successful memory for both associations and items. These results support the view that the DLPFC may contribute to LTM through its role in active processing of relationships during encoding, whereas the VLPFC may have a more general role in promoting successful LTM formation.

Figure 1.

Example stimuli and task timing for encoding phase.

Figure 2.

A, Mean percentage of remember and familiar responses to target words for item-specific (open bars) and relational (shaded bars) trials. B, Mean percentage of remember and familiar responses to first words for item-specific and relational trials. Error bars indicate SEM. *p < 0.001.

Figure 3.

Regions showing greater target word activation on relational than on item-specific trials. These include the bilateral DLPFC (BA 46) and VLPFC (BA 44, 45 and 47) as well as the left PHC and fusiform gyrus.

Figure 4.

Time courses of activation in prefrontal ROIs during processing of the target word as a function of subsequent memory (SM) for associations and items. Left, Time courses are separately averaged for trials in which the first word, target word association was remembered with high confidence and trials in which an incorrect or a low-confidence response was given. Right, Time courses are separately averaged for trials in which the target word was subsequently recollected and for trials in which the target word was subsequently recognized as familiar or forgotten. A, Activation in the left DLPFC (BA 46) ROI was correlated with subsequent LTM for associations but not significantly correlated with subsequent item memory. B, Activation in the left aVLPFC (BA 45/47) ROI was correlated with subsequent LTM for items and associations. Results in the pVLPFC (BA 44) were similar to those shown for the aVLPFC. Error bars indicate SEM.