Neural correlates of successful encoding identified using functional magnetic resonance imaging

Abstract

Neural activity that occurs during the creation of a new memory trace can be observed using functional magnetic resonance imaging (fMRI). Event-related designs have been used to demonstrate that activity in prefrontal and medial temporal lobe areas is associated with successful memory storage. Here we contrasted activity associated with encoding success and encoding effort. Participants viewed a series of 150 words but attempted to remember only half of them. Encoding effort was manipulated using a cue in the form of a letter (R or F) presented after each word to instruct participants either to remember or to forget that word. Increased activity in left inferior prefrontal cortex was observed when words were followed by the cue to remember. In contrast, increased left medial temporal lobe activity was observed for words that were successfully recalled later. These results show that fMRI correlates of the intention to encode a word are different from fMRI correlates of whether that encoding is successful. Prefrontal activation was strongly associated with intentional verbal encoding, whereas left medial temporal activation was crucial for the encoding that actually led to successful memory on the subsequent test.

Fig. 1.

Recognition performance for word and face stimuli that had been studied while fMRI data were collected. Three types of items were included on the recognition test: stimuli that had been cued to be remembered (R), stimuli that had been cued to be forgotten (F), and novel stimuli (N). Endorsing the items as old is the correct response for the R and F stimuli and reflects the false alarm rate for the N stimuli. Error bars indicate the SEM.

Fig. 2.

A, Brain areas in which increased activity was observed during word stimuli cued to be remembered (R-words) compared with word stimuli cued to be forgotten (F-words). Regions showing a reliable increase in activity across the group are shown in color overlaid on axial slices from the averaged high-resolution structural images. Regions shown are those for which the difference in peak activity between R words and F words was consistently greater than zero across the group of participants (t₍₁₁₎ > 3.5 in a cluster >500 mm³ in volume). Color intensity (red/orange/yellow) indicates the magnitude of the average signal change between the two conditions. The level of the images within the standard atlas is noted.B, Time course of observed activity in the left inferior prefrontal cortical region indicated within the green circle on A for remember and forget trials. The time course shown reflects averaged estimates of activity for each time point across all voxels in the region for all participants (with slight temporal smoothing for display purposes).

Fig. 3.

A, Brain areas in which increased activity was observed during word stimuli that were subsequently remembered on the recognition test compared with word stimuli that were not. Regions showing a reliable increase in activity across the group are shown in color overlaid on axial slices from the averaged high-resolution structural images. Regions shown are those for which the difference in peak activity between remembered and forgotten was consistently greater than zero across the group of participants (t₍₁₁₎ > 3.5 in a cluster >500 mm³ in volume). Color intensity (red/orange/yellow) indicates the magnitude of the average signal change between the two conditions. The level of the images within the standard atlas is noted.B, Time course of observed activity in the left posterior hippocampus and parahippocampal cortex region indicated with the blue circle on A for successful and unsuccessful memory trials. The time course shown reflects averaged estimates of activity for each time point across all voxels in the region for all participants (with slight temporal smoothing for display purposes).

Fig. 4.

Comparison of encoding effort and success in the left inferior prefrontal cortex and medial temporal lobe.A, The LIPFC region in which encoding effort was more predictive of activity than encoding success (for words).B, Time courses of observed activity for the four trial types: successfully remembered R-words (SM-R), unsuccessfully remembered R-words (UM-R), successfully remembered F-words (SM-F), and unsuccessfully remembered F-words (UM-F). Of particular note is the fact that this area exhibits a strong response to R-words, even when this effort does not produce successful memory (UM-R > SM-F). C, The left MTL region in which encoding success was more predictive of activity than encoding effort (for words).D, Time courses of observed activity in the MTL region for the four trial types. In this region, successful encoding is associated with an increase in activity, even after the forget cue, whereas an unsuccessful encoding attempt is not associated with increased activity (SM-F > UM-R).

Fig. 5.

Brain areas in which increased activity was observed during face stimuli cued to be remembered (R-faces) compared with face stimuli cued to be forgotten (F-faces). Regions showing a reliable increase in activity across the group are shown incolor overlaid on axial slices from the averaged high-resolution structural images. Regions shown are those for which the difference in peak activity between R-faces and F-faces was consistently different from zero across the group of participants (t₍₁₁₎ > 3.5 in a cluster >500 mm³ in volume). Warm colors (red/orange/yellow) indicate areas in which increased activity was observed for R-faces. Cool colors (blue/cyan) indicate areas in which increased activity was observed during F-face trials. The level of the images within the standard atlas is noted.