Contextually Mediated Spontaneous Retrieval Is Specific to the Hippocampus

Abstract

SUMMARY Although it is now well established that the hippocampus supports memory encoding [1, 2], little is known about hippocampal activity during spontaneous memory retrieval. Recent intracranial electroencephalographic (iEEG) work has shown that hippocampal activity during encoding predicts subsequent temporal organization of memories [3], supporting a role in contextual binding. It is an open question, however, whether the hippocampus similarly supports contextually mediated processes during retrieval. Here, we analyzed iEEG recordings obtained from 215 epilepsy patients as they performed a free recall task. To identify neural activity specifically associated with contextual retrieval, we compared correct recalls, intrusions (incorrect recall of either items from prior lists or items not previously studied), and deliberations (matched periods during recall when no items came to mind). Neural signals that differentiate correct recalls from both other retrieval classes reflect contextual retrieval, as correct recalls alone arise from the correct context. We found that in the hippocampus, high-frequency activity (HFA, 44–100 Hz), a proxy for neural activation [4], was greater prior to correct recalls relative to the other retrieval classes, with no differentiation between intrusions and deliberations. This pattern was not observed in other memory-related cortical regions, including DLPFC, thus supporting a specific hippocampal contribution to contextually mediated memory retrieval.

Spectral fingerprints or spectral tilt? Evidence for distinct oscillatory signatures of memory formation

“…While gamma power increases co-occurred with alpha/beta power decreases in occipital/posterior regions [66], no such co-localization was evident in left lateralized areas involved in semantic processing. Consequently, if the analysis in our study was limited to increases in broad band gamma power changes, a common practice in iEEG analysis [21][22][23][24][25] [9,21,22] the prominent changes in alpha/beta power related to word processing would have been missed. Our findings are exemplary in demonstrating that limiting analysis to very narrow parts of the time-frequency spectrum restricts the potential insights that can be drawn from the data.…”

Hippocampal contributions to serial‐order memory

“…An across‐subject correlation showed that greater hippocampal activity during encoding predicted increased serial recall. In a followup study, Long et al () examined both hippocampal and neocortical HFA during the retrieval phase of the same free recall task. They divided recall events into three classes: recall of items from the immediately preceding list (correct recalls), recall of items from other study lists or items not studied (intrusions) and periods of searching with no recall event (deliberations).…”

Functional wiring of the human medial temporal lobe

“…Second, we examined a memory retrieval contrast, wherein epochs of time leading up to verbalization of a recalled item are compared to matched epochs of time, from other word lists, where no recall occurs (e.g. 29,40,41; see Methods for details). We refer to these matched periods as "deliberation" intervals.…”

“…In this way, we aimed to contrast activity related to successful retrieval against activity during which subjects were liable to try, but fail, to recall a word. This paradigm has been employed in several prior studies examining the neural correlates of free recall (3,29,41,40). However, free-recall tasks inherently confound neural process responsible for episodic retrieval with processes responsible for vocalization and motor preparatory behavior.…”