Elsevier

Neuropsychologia

Volume 51, Issue 12, October 2013, Pages 2322-2332
Neuropsychologia

Medial temporal lobe contributions to cued retrieval of items and contexts

https://doi.org/10.1016/j.neuropsychologia.2013.02.011Get rights and content

Abstract

Several models have proposed that different regions of the medial temporal lobes contribute to different aspects of episodic memory. For instance, according to one view, the perirhinal cortex represents specific items, parahippocampal cortex represents information regarding the context in which these items were encountered, and the hippocampus represents item–context bindings. Here, we used event-related functional magnetic resonance imaging (fMRI) to test a specific prediction of this model—namely, that successful retrieval of items from context cues will elicit perirhinal recruitment and that successful retrieval of contexts from item cues will elicit parahippocampal cortex recruitment. Retrieval of the bound representation in either case was expected to elicit hippocampal engagement. To test these predictions, we had participants study several item–context pairs (i.e., pictures of objects and scenes, respectively), and then had them attempt to recall items from associated context cues and contexts from associated item cues during a scanned retrieval session. Results based on both univariate and multivariate analyses confirmed a role for hippocampus in content-general relational memory retrieval, and a role for parahippocampal cortex in successful retrieval of contexts from item cues. However, we also found that activity differences in perirhinal cortex were correlated with successful cued recall for both items and contexts. These findings provide partial support for the above predictions and are discussed with respect to several models of medial temporal lobe function.

Highlights

► A prediction of the Binding of Items and Contexts (or BIC) model was tested. ► Contributions of MTL structures to cued recall of items and contexts were examined. ► Parahippocampal cortex supports successful retrieval of contexts from item cues. ► Perirhinal cortex supports item and context retrieval from associated cues. ► Hippocampus supports flexible content-general relational memory retrieval.

Introduction

It is not an uncommon experience to come across an item that triggers memory for related contextual information or a context that calls to mind a particular item. For example, while rummaging through a junk drawer, you might encounter a shell amongst the rubble and immediately recall the beach where you enjoyed your first surfing lesson. Conversely, you might happen upon that beach sometime later, and be reminded of the shell you kept from your surfing experience. While both of these examples illustrate the act of retrieving additional information from a particular cue (i.e., either context from item or item from context), they may differentially engage brain regions known to play a critical role in successful encoding and subsequent retrieval of episodic memories.

There is broad consensus that the medial temporal lobes (MTL) are critical for long-term memory, and several models have proposed that the hippocampus and adjacent MTL cortical structures (e.g., the perirhinal and parahippocampal cortices) contribute in different ways (e.g., Brown and Aggleton, 2001, Cohen and Eichenbaum, 1993, Davachi, 2006, Eichenbaum et al., 2007, Graham et al., 2010). According to one influential model, perirhinal cortex supports the process of familiarity-based recognition, and the hippocampus supports successful recollection (Brown & Aggleton, 2001). Competing models have stressed differences in the representational characteristics of MTL structures, emphasizing a role for the hippocampus in relational memory (e.g., memory for relationships among items and the contexts in which they were initially encountered; Cohen & Eichenbaum, 1993) and roles for the perirhinal and parahippocampal cortices in representation of information about items and contexts, respectively (e.g., Davachi, 2006, Diana et al., 2007, Eacott and Gaffan, 2005, Eichenbaum et al., 2007, Montaldi and Mayes, 2010).

As emphasized in one of these models – the Binding of Items and Context (or BIC) model (Diana et al., 2007, Eichenbaum et al., 2007) – process-based and representational views are not necessarily incompatible because hippocampus-mediated relational memory representations may support the experience of recollection (i.e., item recognition accompanied by successful retrieval of additional details about the encoding context) and item-specific perirhinal representations may support a subjective sense of familiarity (i.e., item recognition absent any associated information about the encoding experience). Importantly, however, the BIC model does not rule out possible contributions of perirhinal cortex to recollection, which is consistent with results of recent functional magnetic resonance imaging (fMRI ) investigations showing that perirhinal cortex contributes to successful source recollection when source (in this example, a particular color) has been encoded as an item detail (e.g., a red elephant; Staresina & Davachi, 2008). The BIC model also predicts that activity differences in the parahippocampal cortex will be associated with successful recollection to the extent that contextual representations have been recovered.

The fMRI experiment described here was designed to test a specific prediction of the BIC model—namely that cued recall of items from contexts will elicit perirhinal recruitment and that cued recall of contexts from items will elicit parahippocampal recruitment. To test this prediction, we had participants encode trial unique item–context pairs where items were pictures of common objects and contexts were pictures of indoor and outdoor scenes. During a scanned retrieval phase, participants attempted to recall contexts (i.e., studied scenes) from associated item cues and to recall items (i.e., studied objects) from associated context cues. Univariate and multivariate (i.e., pattern similarity) approaches were used to identify BOLD signal changes correlated with successful cued retrieval of items and contexts. These effects were evaluated in contrasts that compared studied cues for which the associate was successfully recalled to studied cues that were merely endorsed as familiar. In addition to predicted effects for the perirhinal and the parahippocampal cortices, we expected that successful cued recall in either condition, both of which required recovery of item–context relationships, would be supported by BOLD signal changes in the hippocampus.

Section snippets

Participants

Twenty-nine individuals (20 females) from the UC Davis community participated in this experiment and were compensated at a rate of 20 dollars per hour for their time. Data from 11 of these individuals were excluded because the number of trials (i.e., at least 8 per bin) associated with conditions of interest was insufficient for fMRI analyses or because of technical difficulties; therefore, the reported results reflect data from 18 participants (12 females). Informed consent was obtained from

Behavioral performance

Results based on behavioral performance indicated that participants could successfully distinguish old from new pictures during the scanned retrieval phase, and that performance was marginally better for item cues (d′=2.35) than for context cues (d′=1.99; t(17)=2.02, p=.06). Importantly, there were no significant differences in the proportion of studied pictures endorsed with familiar responses or with recollect-associate responses as a function of cue type, though participants did make their

Discussion

The present study investigated the sensitivity of areas along the longitudinal extent of the hippocampus and parahippocampal gyrus to recollection of items and contexts. Consistent with expectations, hippocampal activation magnitude and pattern similarity measures were sensitive to successful content-general relational memory retrieval; notable differences in recruitment along the length of the hippocampus were evident as well, and are discussed in more detail below. Findings from the

Acknowledgements

This work was supported by National Institutes of Health Grant R01MH083734 (to C.R. and A.P.Y). This article does not necessarily represent the official views of the National Institutes of Health.

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