Pattern Separation and Pattern Completion Within the Hippocampal Circuit During Naturalistic Stimuli

Abstract

Pattern separation and pattern completion in the hippocampus play a critical role in episodic learning and memory. However, there is limited empirical evidence supporting the role of the hippocampal circuit in these processes during complex continuous experiences. In this study, we analyzed high-resolution fMRI data from the "Forrest Gump" open-access dataset (16 participants) using a sliding-window temporal autocorrelation approach to investigate whether the canonical hippocampal circuit (DG-CA3-CA1-SUB) shows evidence consistent with the occurrence of pattern separation or pattern completion during a naturalistic audio movie task. Our results revealed that when processing continuous naturalistic stimuli, the DG-CA3 pair exhibited evidence consistent with the occurrence of the pattern separation process, whereas both the CA3-CA1 and CA1-SUB pairs showed evidence consistent with pattern completion. Moreover, during the latter half of the audio movie, we observed evidence consistent with a reduction in pattern completion in the CA3-CA1 pair and an increase in pattern completion in the CA1-SUB pair. Overall, these findings improve our understanding of the evidence related to the occurrence of pattern separation and pattern completion processes during natural experiences.

Keywords: fMRI; hippocampal subfields; naturalistic stimuli; pattern completion; pattern separation.

FIGURE 1

Simplified schematic depiction of entorhinal cortex and hippocampal subfields circuitry (modified from Axmacher et al. 2006).

FIGURE 2

Visual representation of hippocampal subfields segmentation. (A) Sample coronal slices of hippocampal subfields in an anatomical T1‐ and T2‐weighted image from subject 03, from anterior (left) to posterior (right). (B) Sample sagittal slices of hippocampal subfields in an anatomical T1‐ and T2‐weighted image from subject 03, from medial (left) to lateral (right). Top row: T1 image. Second row: T2 image. Third row: Segmentation computed with T1 and T2 scans simultaneously, overlaid on the T2 images. Fourth row: Longitudinal segmentation computed with T1 and T2 scans simultaneously, overlaid on the T2 images.

FIGURE 3

Schematic of pattern separation and pattern completion analyses. (A) Pearson correlation coefficient (R) was calculated between successive sliding windows to assess temporal similarity in Regions A and B. R values were transformed into Fisher Z‐scores. (B) The distribution of temporal similarity within hippocampal pairs (ROI_A–ROI_B) for all window sizes (ranging from 15 to 50 TR). For each size, the pattern separation ratio value was computed as the proportion of sliding windows where Region A exhibited greater temporal similarity than Region B (Z _A > Z _B) relative to the total number of adjacent windows. Conversely, the pattern completion ratio represented the ratio of sliding windows where Region A exhibited lower temporal similarity than Region B (Z _A < Z _B) to the total number of adjacent windows. Nonparametric permutation tests (1000 times) were then conducted to evaluate the significance of the pattern separation (or completion) ratio at this window size. (C) The run‐level pattern separation (or completion) for each movie run. It was measured as the area between pattern separation (or completion) ratio values and the dividing line (y = 0.5) across all window sizes. The x‐axis corresponds to window size, and the y‐axis represented the ratio values of pattern separation (or completion). PC, pattern completion; PS, pattern separation.

FIGURE 4

Pattern separation and pattern completion analyses within the hippocampal (A) DG‐CA3, (B) CA3‐CA1, and (C) CA1‐SUB pairs during naturalistic stimuli in an example of subject 03 run 1. Three area graphs (left) presented the run‐level pattern separation or completion, which was measured as the area between the curve of pattern separation or completion ratio values (ranging from 15 to 50 TR) and the dividing line (y = 0.5). Three scatter diagrams (right) presented the distribution of adjacent sliding windows for pattern separation and completion within the corresponding hippocampal pair at one window size. Each dot represents the temporal similarity in the current hippocampal pair under a sliding window (50 TR), and then the pattern separation or completion ratio was calculated at each preselected given window size. (D) Pattern separation and pattern completion results in the whole hippocampal subfield. A two‐tailed one‐sample t‐test was performed against the chance level. Data plotted as mean ± SEM. *p < 0.05, **p < 0.01, ***p < 0.001, Bonferroni corrected. PC, pattern completion; PS, pattern separation.

FIGURE 5

The dynamic changes of pattern separation and pattern completion processes within the DG‐CA3 (left), CA3‐CA1 (middle), and CA1‐SUB pairs (right) during (A) the first half, (B) the second half, and (C) the whole of the audio movie. The x‐axis represents the sequence of movie runs, while the y‐axis represents the value of Δ pattern separation‐pattern completion. Each dot represents a subject.