The neural correlates of recollection: transient versus sustained FMRI effects

Abstract

Prior research has identified several regions where neural activity is enhanced when recollection of episodic information is successful. Here, we investigated whether these regions dissociate according to whether recollection-related activity is transient or sustained across the time that recollected information must be maintained before a behavioral judgment. Human subjects studied a series of word-picture pairs under the requirement to judge which of the denoted objects was smaller. Following each of 4 study sessions, a scanned test phase occurred in which a series of studied and unstudied words was presented. The requirement at test was to judge whether each word was old or new and, if judged old, to retrieve the associated study picture and hold it in mind until a cue appeared. The delay interval varied between two and eight seconds. The cue instructed subjects which of three different judgments should be applied to the retrieved picture. Separate responses were required when words were either deemed new or the associated image was not retrieved. Relative to studied words for which the associated picture could not be retrieved, words giving rise to successful recollection elicited transient responses in the hippocampus/parahippocampal cortex and retrosplenial cortex, and to sustained activity in prefrontal cortex, the intraparietal sulcus, the left angular gyrus and the inferior temporal gyrus. The finding that recollection-related activity in the angular gyrus tracked the period over which recollected information was maintained is consistent with the proposal that this region contributes to the online representation of recollected information.

Figure 1.

Trial schematics are shown for a single retrieval trial (top) and a single encoding trial (bottom).

Figure 2.

Top, Regions showing transient recollection effects identified by the standard GLM analysis are displayed on sections of the mean across-subjects anatomical image (N = 18), thresholded at p < 0.005 for display purposes. Bottom, Mean parameter estimates derived from an FIR analysis applied to the peaks of the clusters identified above, as well as to a voxel falling within the hippocampus proper, are plotted across time from 2 s before word onset. The coordinates of the peak voxels from which time courses were derived are −12, −58, 16 (A), −27, −34, −20 (B), and −24, −34, −8 (C). The time courses were truncated as described in Materials and Methods before averaging. SEs are displayed for each estimate.

Figure 3.

Top, Parameter estimates from the peak voxels of sustained effects in the left prefrontal, left inferior temporal, and left superior parietal cortex are shown across time from 2 s before word onset. The coordinates of the peak voxels shown are −48, 32, 13 (A); −57, −46, −14 (B); and −33, −55, 46 (C). Middle, Locations of the plotted recollection effects. The effects are projected onto SPM's single subject-rendered brain and are also displayed on a section of the mean across-subjects anatomical image. Bottom, Parameter estimates from the peak voxel of each effect are displayed separately for the 2 and 8 s delay interval associative hit trials. Asterisks indicate time points at which the two conditions differ at p < 0.01.

Figure 4.

Left anterior (PGa; red) and posterior (PGp; yellow) angular gyrus ROIs are depicted on sections of the mean across-subjects anatomical image. Top, Parameter estimates averaged across all voxels within each ROI are shown from 2 s before word onset. Asterisks indicate time points at which associative hits and item hits differed: **p < 0.005 and *p < 0.05. Bottom, Parameter estimates are displayed separately for 2 and 8 s delay interval associative hit trials. Single asterisks indicate time points at which the two conditions differed at p < 0.05.

Figure 5.

Left, Sustained novelty effect in the left hippocampus (−24, −10, −17). Right, Peak parameter estimates for correct rejections and item hits are displayed from 2 s before word onset.