Top-down modulation of hippocampal encoding activity as measured by high-resolution functional MRI

Abstract

Memory formation is known to be critically dependent upon the medial temporal lobe (MTL). Despite this well-characterized role, it remains unclear whether and how MTL encoding processes are affected by top-down goal states. Here, we examined the manner in which task demands at encoding affect MTL activity and its relation to subsequent memory performance. Participants were scanned using high-resolution neuroimaging of the MTL while engaging in two incidental encoding tasks: one that directed participants' attention to stimulus distinctiveness, and the other requiring evaluation of similarities across stimuli. We hypothesized that attending to distinctiveness would lead to the formation of more detailed memories and would more effectively engage the hippocampal circuit than attending to similarity. In line with our hypotheses, higher rates of subsequent recollection were observed for stimuli studied under the Distinctiveness than Similarity task. Critically, within the hippocampus, CA1 and the subiculum demonstrated an interaction between memory performance and task such that a significant subsequent memory effect was found only when task goals required attention to stimulus distinctiveness. To this end, robust engagement of the hippocampal circuit may underlie the observed behavioral benefits of attending to distinctiveness. Taken together, these findings advance understanding of the effects of top-down intentional information on successful memory formation across subregions of the MTL.

Keywords: Encoding; Functional MRI; Goal states; Hippocampus; Medial temporal lobe; Memory.

Figure 1

Distinctiveness and Similarity tasks. During the Distinctiveness task (A), participants imagined themselves as chauffeurs and rated how easily a given “customer” could be picked out of a crowded airport on a scale from 1 to 4, ranging from 1 = hard to 4 = easy. During the Similarity task (B), participants imagined themselves as casting agents and rated how well each “actor” matched the director’s desired look on a scale from 1 to 4, ranging from 1 = poor match to 4 = excellent match. For Experiment 2, a variable inter-trial interval (ITI) was included during which participants made odd/even judgments.

Figure 2

Distinctiveness and similarity ratings during encoding. In the Distinctiveness task, ratings ranged from 1 = hard to pick out of a crowd (not distinctive) to 4 = easy to pick out of a crowd (very distinctive). For the Similarity task, ratings ranged from 1 = poor match (dissimilar) to 4 = excellent match (very similar). A significant two-way interaction between encoding task and response option was found for both Experiment 1 and 2, suggesting that participants processed faces differently in each of the two encoding tasks.

Figure 3

Effect of encoding task on subsequent memory performance. Experiment 1: A significant main effect of encoding task was found (p = .038) such that the subsequent hit rate for the Distinctiveness task was higher than that of the Similarity task. Analyses further revealed a significant interaction between encoding task and subsequent memory quality (p = .032), with a higher percentage of subsequent remember hits for the Distinctiveness than Similarity task (p = .007). Experiment 2: A trend toward a significant interaction between encoding task and subsequent memory quality was found (p = .10), with a higher percentage of subsequent remember hits for faces studied under the Distinctiveness than Similarity task (p < .05).

Figure 4

Effect of task ratings on subsequent rates of recollection. For each task and for each rating bin, the proportion of subsequently recollected trials was calculated. Experiment 1: A significant interaction was found between encoding task and rating (p = .012) such that subsequent rates of recollection increased with increasing ratings in the Distinctiveness task but not the Similarity task. Experiment 2: No main effects of rating nor interaction between encoding task and rating was found.

Figure 5

Main effect of subsequent memory. Timecourses represent encoding activity associated with subsequent hits and misses for the Distinctiveness and Similarity tasks. Bar graphs represent integrated percent signal change from 3–12 sec. Encoding activity in left DG/CA_2/3 (A) and right parahippocampal cortex (B) revealed a main effect of subsequent memory such that collapsed across task, activity associated with subsequent hits was greater than that for misses (left DG/CA_2/3, p = .004; right parahippocampal cortex, p = .002). DG: dentate gyrus. PHC: parahippocampal cortex.

Figure 6

Encoding task by subsequent memory interaction. Timecourses represent encoding activity associated with subsequent hits and misses for the Distinctiveness and Similarity tasks. Bar graphs represent integrated percent signal change from 9–12 sec. Encoding activity in right CA1 (A) and left subiculum (B) revealed a significant interaction between encoding task and subsequent memory late in the timecourse, such that greater subsequent memory effects were observed for the Distinctiveness than the Similarity task (right CA1, p = .016; left subiculum, p = .047).