Persistence of parahippocampal representation in the absence of stimulus input enhances long-term encoding: a functional magnetic resonance imaging study of subsequent memory after a delayed match-to-sample task

Abstract

Recent theoretical models based on cellular processes in parahippocampal structures show that persistent neuronal spiking in the absence of stimulus input is important for encoding. The goal of this study was to examine in humans how sustained activity in the parahippocampal gyrus may underlie long-term encoding as well as active maintenance of novel information. The relationship between long-term encoding and active maintenance of novel information during brief memory delays was studied using functional magnetic resonance imaging (fMRI) in humans performing a delayed matching-to-sample (DMS) task and a post-scan subsequent recognition memory task of items encountered during DMS task performance. Multiple regression analyses revealed fMRI activity in parahippocampal structures associated with the active maintenance of trial-unique visual information during a brief memory delay. In addition to a role in active maintenance, we found that the subsequent memory for the sample stimuli as measured by the post-scan subsequent recognition memory task correlated with activity in the parahippocampal gyrus during the delay period. The results provide direct evidence that encoding mechanisms are engaged during brief memory delays when novel information is actively maintained. The relationship between active maintenance during the delay period and long-term subsequent memory is consistent with current theoretical models and experimental data that suggest that long-term encoding is enhanced by sustained parahippocampal activity.

Figure 1.

Tasks and statistical analyses of fMRI data. A, DMS and CON. In both tasks, a trial consisted of three time-locked events: a 2 sec visual scene presentation (sample), followed by a 10 sec delay period, followed by a 2 sec visual scene presentation (test), followed by a variable-length intertrial interval. Tasks differed only in instruction. B, Contrasts for active maintenance analysis. C, Contrasts for subsequent memory analysis. Regressors were created by convolving the six orthogonal contrasts of interest (depicted on the left) with a gamma-variate function (HRF; depicted on the right) (Boynton et al., 1996). Vertical bars represent positioning of the HRF. S, Sample; D, delay; T, test. For details, see Materials and Methods.

Figure 2.

Behavioral results of subsequent memory rating. Mean ± SE proportion responses is depicted on y-axes, and confidence rating (5, high-confidence old; 4, low-confidence old; 3, unsure; 2, low-confidence new; 1, high-confidence new) is depicted on x-axes. A, DMS samples versus new stimuli (lures; gray bars). B, CON samples versus new stimuli. C, DMS tests versus new stimuli. D, CON tests versus new stimuli. E, DMS samples (match trials only) versus new stimuli. F, DMS samples (nonmatch trials only) versus new stimuli.

Figure 3.

fMRI results from active maintenance analysis. Please note that only activation within ROIs is superimposed on canonical average T1-weighted ICBM/MNI brain. A, Right mid-FG/PHG, x = 34, y = -34, z = -20 (arrows). B, Corrected signal intensities during sample presentation (S), delay period (DELAY), and test presentation (T) from right mid-FG/PHG; DMS > CON. C, Corrected signal intensities from right mid-FG/PHG; SMT5 > SMT1-4. D, Left mid-FG/PHG, x = -32, y = -48, z = -12 (arrows). E, Corrected signal intensities from left mid-FG/PHG; DMS > CON. F, Corrected signal intensities from left mid-FG/PHG; SMT5 > SMT1-4. y-Axes, signal intensity grand mean scaled to 100 and global calculation using mean voxel value (within per image full mean/eight mask). R, Right; L, left.

Figure 4.

fMRI results from subsequent memory analysis across match and nonmatch trials (double or single stimulus presentations). Please note that only activation within ROIs is superimposed on canonical average T1-weighted ICBM/MNI brain. A, Right PHG/mid-FG, x = 26, y = -32, z = -14 (arrows). B, Corrected signal intensities during sample presentation (S), delay period (DELAY), and test presentation (T) from right PHG/mid-FG for DMS trials (across match and nonmatch trials, double or single stimulus presentations); SMT5 > SMT1-4. C, Corrected signal intensities from right PHG/mid-FG for DMS trials that were nonmatches (single stimulus presentations); SMT5 > SMT1-4. D, Right PRC/ERC, x = 38, y = -12, z = -26 (white arrows); and left PRC/ERC, x = -28, y = -8, z = -34 (black arrow). E, Corrected signal intensities from right PRC/ERC for DMS trials (across match and nonmatch trials, double or single stimulus presentations). F, Corrected signal intensities from left PRC/ERC for DMS trials (across match and nonmatch trials). y-Axes, Signal intensity grand mean scaled to 100 and global calculation using mean voxel value (within per image full mean/eight mask). R, Right; L, left.

Figure 5.

fMRI results from subsequent memory analysis of nonmatch trials (single stimulus presentations). Please note that only activation within ROIs is superimposed on canonical average T1-weighted ICBM/MNI brain. A, Right PRC/ERC, x = 34, y = -10, z = -28 (white arrows); left PRC/ERC, x = -34, y = -12, z = -26 (black arrow). B, Corrected signal intensities during sample presentation (S), delay period (DELAY), and test presentation (T) from right PRC/ERC for DMS trials (nonmatch trials, single stimulus presentations); SMT5 > SMT1-4. C, Corrected signal intensities during sample, delay, and test presentation periods from left PRC/ERC for DMS nonmatch trials. D, Right hippocampal (HIPP.) body, x = 34, y = -26, z = -14 (white arrows); left hippocampal body, x = -30, y = 30, z = -12 (black arrow). E, Corrected signal intensities from right hippocampal body for DMS nonmatch trials (single stimulus presentations); SMT5 > SMT1-4. F, Corrected signal intensities from left hippocampal body for DMS nonmatch trials. y-Axes, Signal intensity grand mean scaled to 100 and global calculation using mean voxel value (within per image full mean/eight mask). R, Right; L, left.