Making memories without trying: medial temporal lobe activity associated with incidental memory formation during recognition

Abstract

Structures in the medial portions of the human temporal lobes (MTL) play a vital role in the ability to learn new facts and events, whether such learning is intentional or incidental. We examined neural activity in the MTL both while participants studied pictures of novel scenes and while they attempted to recognize which scenes had been previously presented. In a second surprise test we assessed participants' memory for items that were presented only during the previous recognition memory test. We present a novel approach to cross-participant alignment of neuroimaging data that provides more precise localization and enhanced statistical power within regions such as the MTL. Using this technique, we observed that the amount of MTL activity predicted participants' ability to subsequently remember scenes not only during the intentional study task, but also during the first memory retrieval test when only incidental encoding occurred. This encoding-related activity during memory retrieval was in the same subregions of the MTL as encoding-related activity during intentional study and is hypothesized to be one of the primary reasons why retrieval-related activity is often difficult to observe with neuroimaging techniques.

Figure 1.

Diagram of the three tasks and the contrasts used to assess subsequent memory effects. Behavioral performance in test 1 (hits vs misses) for the items presented at study (list A) is used to contrast activity at study for subsequently remembered (study-R) versus subsequently forgotten (study-F) items. Behavioral performance in test 2 (list B, hits vs misses) is used to contrast activity during test 1 for the novel foil items (list B) that are remembered in test 2 (CR-R) versus forgotten in test 2 (CR-F).

Figure 2.

ROI-AL versus Talairach alignment. Comparison between average structural images (20 brains, coronal slices, cropped to show the MTL) aligned to the Talairach atlas (a) and aligned using the anatomically based ROI-AL technique (b). Arrows indicate the locations of the collateral sulcus. c, Comparison of the distribution of absolute t values within the MTL for the study-R versus study-F contrast using ROI-AL and using Talairach, plotted as the difference between histograms. In each bin, a positive value indicates more numerous voxels using ROI-AL.

Figure 3.

Activity during study and test 1. Results of ANOVAs showing regions whose activity varied by trial type at study (left) and at test 1 (right) are shown in coronal sections, cropped to show the MTL (the left side of image is the left side of the brain, the number indicates the approximate location of the slice in Talairach coordinates). Individual regions are coded by color based on location: orange, left perirhinal cortex (L PRC); red, right perirhinal cortex (R PRC); green, left hippocampus (L H); yellow, right hippocampus (R H); blue, left parahippocampal cortex (L PHC); purple, right parahippocampal cortex (R PHC); and cyan, non-MTL. Hemodynamic responses from each cluster of activity are shown adjacent to the coronal images and are the result of the deconvolution analysis. In each hemodynamic response, time is on the x-axis (seconds) and β fit coefficient (scanner units) is on the y-axis. At study, the hemodynamic responses for items recognized in test 1 (study-R) are shown in red, items subsequently forgotten in test 1 (study-F) are shown in blue, and the subsequent memory effect is shown in gray. In all six regions, the subsequent memory effect is statistically reliable. In test 1, target items recognized (hit) are shown in green, foil items correctly rejected and later remembered in test 2 (CR-R) are shown in red, foil items correctly rejected and later forgotten in test 2 (CR-F) are shown in blue, and the subsequent memory effect is shown in black. In all six regions, both the subsequent memory effect and the contrast between hit and CR-F trials are significantly reliable.