The relationship between level of processing and hippocampal-cortical functional connectivity during episodic memory formation in humans

Abstract

New episodic memory traces represent a record of the ongoing neocortical processing engaged during memory formation (encoding). Thus, during encoding, deep (semantic) processing typically establishes more distinctive and retrievable memory traces than does shallow (perceptual) processing, as assessed by later episodic memory tests. By contrast, the hippocampus appears to play a processing-independent role in encoding, because hippocampal lesions impair encoding regardless of level of processing. Here, we clarified the neural relationship between processing and encoding by examining hippocampal-cortical connectivity during deep and shallow encoding. Participants studied words during functional magnetic resonance imaging and freely recalled these words after distraction. Deep study processing led to better recall than shallow study processing. For both levels of processing, successful encoding elicited activations of bilateral hippocampus and left prefrontal cortex, and increased functional connectivity between left hippocampus and bilateral medial prefrontal, cingulate and extrastriate cortices. Successful encoding during deep processing was additionally associated with increased functional connectivity between left hippocampus and bilateral ventrolateral prefrontal cortex and right temporoparietal junction. In the shallow encoding condition, on the other hand, pronounced functional connectivity increases were observed between the right hippocampus and the frontoparietal attention network activated during shallow study processing. Our results further specify how the hippocampus coordinates recording of ongoing neocortical activity into long-term memory, and begin to provide a neural explanation for the typical advantage of deep over shallow study processing for later episodic memory.

Figure 1

Experimental session and trial structure. Top: Session structure. A total of three fMRI sessions with the structure displayed were performed by each participant. For each participant, each session consisted of three study lists with deep study processing and three study lists with shallow study processing (making a total of six lists per fMRI session, and a total of 18 lists over the three sessions). Order of study condition was counterbalanced across participants (i.e., deep‐shallow‐deep vs. shallow‐deep‐shallow, etc.). Bottom: Structure of a single study trial. Each study list comprised 20 such study trials, followed by a 20 s distractor task and a 90 s oral recall period.

Figure 2

Level‐of‐processing effect. Regions with increased activity during deep versus shallow study included medial and left inferior prefrontal cortex and the left temporoparietal junction (orange‐yellow), whereas shallow study processing was associated with activation of dorsolateral prefrontal and posterior lateral brain structures (blue‐cyan). Activations above a threshold of T₂₅₀ = 4.75 (P < 0.05, FWE‐corrected; minimal cluster size k = 20 voxels) are displayed. The scale bars display the T value.

Figure 3

Activations related to successful episodic memory encoding (DM effects: later recalled > later forgotten) in the deep and shallow study conditions. A: The bilateral hippocampus (arrows) showed robust activations for later recalled relative to later forgotten words during both deep and shallow study processing. Bar plots depict contrasts of parameter estimates ± standard errors in the left (L) and right (R) hippocampus (x, y, z = peak voxel coordinates in Talairach reference space). B: Bilateral prefrontal and parietal cortices showed extensive activations for later recalled relative to later forgotten words during both deep and shallow study processing. Activations above a threshold of T₂₅₀ = 4.75 (P < 0.05, whole‐brain FWE‐corrected; minimal cluster size k = 20 voxels) are displayed.

Figure 4

Functional connectivity of the left and right hippocampus related to successful episodic memory encoding in the deep and shallow study conditions. A: Left panel: Representative volume of interest (VOI) from the left hippocampus of a single participant. VOIs were spheres with a radius of 6 mm and contained between 20 and 33 voxels. Right panel: In the deep study condition, the left hippocampus showed increased functional connectivity with the dorsolateral and ventrolateral prefrontal cortex as well with an extensive midline and parietal network, largely overlapping with the default mode network. These connectivity changes were less pronounced in the shallow condition. B: Left panel: Representative volume of interest (VOI) from the right hippocampus of a single participant. Right panel: The right hippocampus showed increased functional connectivity with the dorsal and ventral attention networks of the right hemisphere the shallow study condition, whereas connectivity increases of the right hippocampus during deep study were sparse. All displayed activations are thresholded at P < 0.05, whole‐brain FWE‐corrected.

Figure 5

Preferential increases in functional connectivity with the left hippocampus related to successful episodic memory encoding in the deep study condition. Brain regions that showed increased connectivity with the hippocampus in the deep study condition, exclusively masked with the PPI contrast from the shallow study condition (P < 0.01, uncorrected), are displayed. A: Preferential functional connectivity of the bilateral ventrolateral prefrontal cortex (VLPFC; arrows) with the left hippocampus during deep study processing. B: Left: Preferential functional connectivity of the right temporoparietal junction (TPJ; arrow) with the left hippocampus during deep study processing. The local maximum was at the intersection of previously reported positive (yellow) and negative (green) DM effects (Uncapher and Wagner, 2009). PPC: posterior parietal cortex DM effect. Right: Increased functional connectivity of these brain regions during deep study processing was positively correlated with the behavioral LOP effect. X‐axis: contrasts of parameter estimates in the TPJ for individual participants. Y‐axis: behavioral LOP effect on later recall for individual participants [(later remembered_deep ‐ later remembered_shallow)/later remembered_shallow]. plots display contrasts of parameter estimates ± standard error (x, y, z = peak voxel coordinates in Talairach reference space).

Figure 6

Right temporoparietal connectivity changes during deep and shallow encoding. The right hippocampus showed increased functional connectivity with a region in the right TPJ that was more superiorly located relative to the region that showed increased functional connectivity with the left hippocampus during deep encoding. All displayed activations are thresholded at P < 0.05, whole‐brain FWE‐corrected.