Functional dissociation of hippocampal subregions corresponding to memory types and stages

Abstract

Background: The hippocampus reportedly plays a crucial role in memory. However, examining individual human hippocampal-subfield function remains challenging because of their small sizes and convoluted structures. Here, we identified hippocampal subregions involved in memory types (implicit and explicit memory) and stages (encoding and retrieval).

Methods: We modified the serial reaction time task to examine four memory types, i.e. implicit encoding, explicit encoding, implicit retrieval, and explicit retrieval. During this task, 7-T functional magnetic resonance imaging was used to compare brain activity evoked by these memory types.

Results: We found hippocampal activation according to all memory types and stages and identified that the hippocampus subserves both implicit and explicit memory processing. Moreover, we confirmed that cornu ammonis (CA) regions 1-3 were implicated in both memory encoding and retrieval, whereas the subiculum was implicated only in memory retrieval. We also found that CA 1-3 was activated more for explicit than implicit memory.

Conclusions: These results elucidate human hippocampal-subfield functioning underlying memory and may support future investigations into hippocampal-subfield functioning in health and neurodegenerative disease.

Keywords: CA 1–3; Encoding; Explicit memory; Hippocampus; Implicit memory; Retrieval; Subiculum; Ultra-high field fMRI.

Fig. 1

The block-designed fMRI paradigm. Explicit memory and implicit memory tasks comprise three conditions: encoding sequence (ES); retrieval sequence (RTS); and random sequence (RS). The three conditions were repeated three times for each task

Fig. 2

Hippocampal activation corresponding to each memory type and stage. All kinds of memories, such as explicit encoding, explicit retrieval, implicit encoding, and implicit retrieval, evoke hippocampal activation (p < 0.05, FDR-corrected). MNI coordinates: explicit encoding (− 38, − 18, − 14), explicit retrieval (− 18, − 14, − 22), implicit encoding (− 36, − 36, − 4), implicit retrieval (− 18, − 22, − 18)

Fig. 3

Conjunction analysis results. a Activation in the CA 1–3 is shown during encoding. b Retrieval has evoked activation of the subiculum (yellow: CA 1–3 area, green: subiculum, red: activated area). MNI coordinates: encoding (− 36, − 14, − 16), retrieval (− 18, − 10, − 24)

Fig. 4

Time course of hemodynamic responses in subiculum and in the CA1–3 areas. a subiculum and b CA1–3 areas. Blue and red represent explicit encoding and implicit encoding, and green and violet indicate explicit retrieval and implicit retrieval, respectively. The y-axis and x-axis display percent signal change and number of scans each, and the error bars represents SEM

Fig. 5

The number of significantly activated voxel in the subiculum and in the CA1–3 areas during each memory type and stage. Blue represents explicit memory, and red indicates implicit memory. a In the subiculum, the main effect of memory stage on the number of significantly activated voxel was found. b There are significant main effects of memory type and stage in the CA1–3 areas