Persistent schema-dependent hippocampal-neocortical connectivity during memory encoding and postencoding rest in humans

Abstract

The hippocampus is thought to promote gradual incorporation of novel information into long-term memory by binding, reactivating, and strengthening distributed cortical-cortical connections. Recent studies implicate a key role in this process for hippocampally driven crosstalk with the (ventro)medial prefrontal cortex (vmPFC), which is proposed to become a central node in such representational networks over time. The existence of a relevant prior associative network, or schema, may moreover facilitate this process. Thus, hippocampalvmPFC crosstalk may support integration of new memories, particularly in the absence of a relevant prior schema. To address this issue, we used functional magnetic resonance imaging (fMRI) and prior schema manipulation to track hippocampal-vmPFC connectivity during encoding and postencoding rest. We manipulated prior schema knowledge by exposing 30 participants to the first part of a movie that was temporally scrambled for 15 participants. The next day, participants underwent fMRI while encoding the movie's final 15 min in original order and, subsequently, while resting. Schema knowledge and item recognition performance show that prior schema was successfully and selectively manipulated. Intersubject synchronization (ISS) and interregional partial correlation analyses furthermore show that stronger prior schema was associated with more vmPFC ISS and less hippocampal-vmPFC interregional connectivity during encoding. Notably, this connectivity pattern persisted during postencoding rest. These findings suggest that additional crosstalk between hippocampus and vmPFC is required to compensate for difficulty integrating novel information during encoding and provide tentative support for the notion that functionally relevant hippocampal-neocortical crosstalk persists during off-line periods after learning.declarative memory | memory consolidation | resting state | functional connectivity | functional MRI T he formation of long-term memory traces involves a gradual integration of newly acquired information into neocortical associative networks (1, 2). The hippocampus is thought to promote this process by binding, reactivating, and strengthening connections between distributed neocortical representations, thus gradually reducing hippocampal dependence of the memory trace (3-5). Recent findings, however, show a concomitant increase in dependence on the (ventral) medial prefrontal cortex (vmPFC) (6-9) that may develop rapidly depending on contextual factors (10). These findings suggest that the binding role of the hippocampus may be transferred to the vmPFC (6, 11, 12) and implicate hippocampal-neocortical interactions in early stages of long-term memory formation (13).Several lines of animal and human research suggest that coupling between these regions occurs at different stages of long-term memory formation. During encoding, neurons in medial prefrontal cortex (PFC) have been shown to exhibit unit activity that is phase locked to hippocampal theta oscillations (14). Moreover, functional connec...

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