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. 2015 Apr;27(4):679-91.
doi: 10.1162/jocn_a_00740. Epub 2014 Oct 14.

Reinstatement of Individual Past Events Revealed by the Similarity of Distributed Activation Patterns During Encoding and Retrieval

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Free PMC article

Reinstatement of Individual Past Events Revealed by the Similarity of Distributed Activation Patterns During Encoding and Retrieval

Erik A Wing et al. J Cogn Neurosci. .
Free PMC article

Abstract

Neurobiological memory models assume memory traces are stored in neocortex, with pointers in the hippocampus, and are then reactivated during retrieval, yielding the experience of remembering. Whereas most prior neuroimaging studies on reactivation have focused on the reactivation of sets or categories of items, the current study sought to identify cortical patterns pertaining to memory for individual scenes. During encoding, participants viewed pictures of scenes paired with matching labels (e.g., "barn," "tunnel"), and, during retrieval, they recalled the scenes in response to the labels and rated the quality of their visual memories. Using representational similarity analyses, we interrogated the similarity between activation patterns during encoding and retrieval both at the item level (individual scenes) and the set level (all scenes). The study yielded four main findings. First, in occipitotemporal cortex, memory success increased with encoding-retrieval similarity (ERS) at the item level but not at the set level, indicating the reactivation of individual scenes. Second, in ventrolateral pFC, memory increased with ERS for both item and set levels, indicating the recapitulation of memory processes that benefit encoding and retrieval of all scenes. Third, in retrosplenial/posterior cingulate cortex, ERS was sensitive to individual scene information irrespective of memory success, suggesting automatic activation of scene contexts. Finally, consistent with neurobiological models, hippocampal activity during encoding predicted the subsequent reactivation of individual items. These findings show the promise of studying memory with greater specificity by isolating individual mnemonic representations and determining their relationship to factors like the detail with which past events are remembered.

Figures

Figure 1
Figure 1
(A) Experimental design. During encoding, scene pictures were presented with a descriptive label while participants judged image composition. At retrieval, descriptive labels for previously encoded scenes were presented. Participants rated how detailed their memory was for the corresponding picture on a 4-point scale. After the scan, all scenes from encoding were presented in a forced-choice recognition task that included three similar scene exemplars. Participants chose the specific image they believed was presented at encoding and then rated their confidence on a 4-point scale. (B) Overview of searchlight analysis. For item-ERS, ERS was calculated with that item’s corresponding encoding trial to produce an ERS volume for each trial. For set-ERS, ERS was calculated in the same way between each retrieval trial and all encoding trial sharing the same subsequent memory rating. These ERS values were then averaged at the voxel level to produce a single set-ERS volume for each retrieval trial that contained the mean similarity between that trial and other encoding trials of the same memory set.
Figure 2
Figure 2
Behavioral performance. Postscan forced-choice recognition performance shown as a function of cued-recall ratings given during the scanned retrieval phase. Increases in both recognition accuracy and confidence are evident at each successive cued-recall memory level.
Figure 3
Figure 3
Regions showing main findings of the factorial design. (A) Left OTC showed a Memory × ERS level interaction with a stronger impact on memory ratings for item-ERS than set-ERS. (B) Bilateral VLPFC showed a main effect of memory where both item-ERS and set-ERS had a similar impact on memory ratings. (C) RSC/PCC showed a main effect of ERS level; in this region item-ERS was greater than set-ERS, but they did not vary with memory scores. Line graphs below each brain image plot the mean item/set ERS value across memory ratings for the corresponding cluster and illustrate the specific nature of the effect within the cluster.
Figure 4
Figure 4
Relationship between univariate encoding activity and item-ERS. (A) Trialwise item-ERS in left OTC was correlated with encoding activity across the whole brain to identify regions where encoding activity predicted item-ERS. (B) In two regions trial-to-trial variability in encoding activity predicted with the degree of memory-related item-ERS: the anterior MTL and early visual cortex. (C) These two regions showed different patterns between encoding activity and subsequent memory, with typical subsequent memory effects (i.e., memory-related increase in univariate activity) evident in hippocampus (graphs shows effects at hippocampal peak, MNI −15, 18 –19) but not in early visual cortex (ROI mean, see Table 2 for subpeaks).

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