Pre-stimulus neural activity predicts successful encoding of inter-item associations

Abstract

fMRI was employed to investigate the relationship between pre-stimulus neural activity and associative encoding of words and pictures in humans. While undergoing scanning, subjects studied randomly interleaved word or picture pairs. A pre-stimulus cue preceded the presentation of each study pair and signaled whether it would comprise words or pictures. Memory for the study pairs was later tested with an associative recognition test, which comprised word or picture pairs presented either in the same (intact) or a different (rearranged) pairing as at study, along with pairs of new items. The critical fMRI contrast was between study activity associated with pairs later correctly judged intact and pairs incorrectly judged as rearranged. A key question was whether material-selective pre-stimulus encoding effects could be identified which overlapped regions selectively activated by the respective study material. Picture-selective pre-stimulus effects were identified in bilateral fusiform and the intraparietal sulcus (IPS), whereas word-selective effects could not be identified. Material-invariant pre-stimulus subsequent memory effects were also identified in several neocortical regions as well as in the hippocampus. Whereas the loci of the neocortical effects suggest that they reflect the benefit to encoding that accrues from engagement of cognitive control processes, their magnitude was negatively correlated across subjects with associative recognition performance and positively related to false alarm rate. Conversely, the hippocampal effects also predicted unique variance in associative memory and were negatively related to hit rate. It is suggested that the neocortical pre-stimulus effects may reflect encoding processes that increase familiarity of single items, whereas the hippocampal pre-stimulus effects are proposed to reflect either the encoding of task-irrelevant features or the retrieval of task-relevant information associated with the pre-stimulus cues. Overall, the results provide evidence that pre-stimulus processes may be deleterious, rather than beneficial, to associative encoding.

Keywords: Associative memory; Hippocampus; Neocortex; Pre-stimulus; fMRI.

Figure 1. Schematic of the study task

Figure 2. Material-invariant pre-stimulus subsequent memory effects

Left: regions where pre-stimulus activity was greater for study pairs that were later correctly judged intact than for pairs that were later incorrectly judged as re-arranged. Results are rendered onto the PALS-B12 atlas of the visualization program Caret, using mean fiducial mapping (see Methods section 2.6.2). Right: estimated time courses from two representative regions. Y-axis represents mean parameter estimates derived from an FIR analysis of activity from the two indicated loci, and are plotted in 2 s intervals relative to stimulus onset. Error bars represent estimated standard errors of the difference between conditions. The coordinates of the voxels from which timecourses were derived are (A) 42, 14, 22; (B) -3 -31, 25.

Figure 3. Material-invariant hippocampal subsequent memory effects

Top left: pre-stimulus subsequent memory effects projected onto a section of the across-subjects mean normalized structural image. Top right: estimated time courses of activity for the right hippocampus (18, -13, -20); see figure 3 legend for details. Bottom left: stimulus-related subsequent memory effects; right: estimated time courses of activity the left hippocampus (-33, -25, -14).

Figure 4. Across-subjects correlation between pre-stimulus subsequent memory effects and later associative recognition performance

Figure 5. Picture-selective pre-stimulus subsequent memory effects

Top: regions where pre-stimulus activity was greater for picture pairs that were later remembered than for picture pairs that were later incorrectly judged as re-arranged. Bottom: estimated time courses from the loci indicated above; see Figure 3 legend for details. The coordinates from which timecourses were derived are (A) −33, -82, 16; (B) -42, -61, -35.

Figure 6. Stimulus-related subsequent memory effects

Top: Material-invariant subsequent memory effects. Middle: picture-selective effects. Bottom: word-selective effects. Right: estimated time courses from representative regions, taken from the indicated regions; see figure 3 legend for details. Coordinates for each time course are (from top to bottom) −39, 8, 28; 54, -55, 14; -51, -37, -8, respectively.

Figure 7. Overlap between pre- and post-stimulus picture-selective subsequent memory effects

Post-stimulus picture selective subsequent memory effects masked within regions demonstrating pre-stimulus picture selective subsequent memory effects (see Methods section 2.7.4). Blue: pre-stimulus effects; Yellow: post-stimulus picture effects; Red: Overlap. Right: Estimated time courses of activity for the center of mass of the cluster demonstrating overlap (24,-61, 39); see Figure 3 legend for details. Error bars represent estimated standard errors of the difference between conditions.