Article (PDF Available)

Dissecting medial temporal lobe contributions to item and associative memory formation

Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, 6500 HB Nijmegen, The Netherlands.
NeuroImage (Impact Factor: 6.36). 04/2009; 46(3):874-81. DOI: 10.1016/j.neuroimage.2009.02.039
Source: PubMed


A fundamental and intensively discussed question is whether medial temporal lobe (MTL) processes that lead to non-associative item memories differ in their anatomical substrate from processes underlying associative memory formation. Using event-related functional magnetic resonance imaging, we implemented a novel design to dissociate brain activity related to item and associative memory formation not only by subsequent memory performance and anatomy but also in time, because the two constituents of each pair to be memorized were presented sequentially with an intra-pair delay of several seconds. Furthermore, the design enabled us to reduce potential differences in memory strength between item and associative memory by increasing task difficulty in the item recognition memory test. Confidence ratings for correct item recognition for both constituents did not differ between trials in which only item memory was correct and trials in which item and associative memory were correct. Specific subsequent memory analyses for item and associative memory formation revealed brain activity that appears selectively related to item memory formation in the posterior inferior temporal, posterior parahippocampal, and perirhinal cortices. In contrast, hippocampal and inferior prefrontal activity predicted successful retrieval of newly formed inter-item associations. Our findings therefore suggest that different MTL subregions indeed play distinct roles in the formation of item memory and inter-item associative memory as expected by several dual process models of the MTL memory system.

Full-text (PDF)

Available from: Shaozheng Qin
  • Source
    • "We interpreted this reduction to reflect a disruption of encoding processes, since numerous studies have implicated the hippocampus (e.g. Wagner et al., 1998; Eichenbaum, 2000; Qin et al., 2009; Nadel and Hardt, 2011) in successful memory encoding. Moreover, these results are in line with findings from Kensinger et al. (2003) and Uncapher and Rugg (2008); both studies reported an attenuated memory effect in the left hippocampus for the condition with a difficult secondary task compared to the control condition. "
    [Show abstract] [Hide abstract] ABSTRACT: It is a well-established finding that memory encoding is impaired if an external secondary task (e.g. tone discrimination) is performed simultaneously. Yet, while studying we are also often engaged in internal secondary tasks such as planning, ruminating, or daydreaming. It remains unclear whether such a secondary internal task has similar effects on memory and what the neural mechanisms underlying such an influence are. We therefore measured participants' blood oxygenation level dependent responses while they learned word-pairs and simultaneously performed different types of secondary tasks (i.e., internal, external, and control). Memory performance decreased in both internal and external secondary tasks compared to the easy control condition. However, while the external task reduced activity in memory-encoding related regions (hippocampus), the internal task increased neural activity in brain regions associated with self-reflection (anterior medial prefrontal cortex), as well as in regions associated with performance monitoring and the perception of salience (anterior insula, dorsal anterior cingulate cortex). Resting-state functional connectivity analyses confirmed that anterior medial prefrontal cortex and anterior insula/dorsal anterior cingulate cortex are part of the default mode network and salience network, respectively. In sum, a secondary internal task impairs memory performance just as a secondary external task, but operates through different neural mechanisms.
    Full-text · Article · Dec 2015 · NeuroImage
    • "Since both intact and recombined pairs comprise previously studied items, performance cannot be based on item recognition , and so should be driven by recognition of the previously encountered associations. Some researchers have proposed that the brain structures that support recognition memory for single items are partially distinct from those that support recognition memory for associations, and particularly, associations between previously unrelated items (e.g., Giovanello et al., 2009; Qin et al., 2009). For instance, the relational memory theory holds that the hippocampus is especially important for encoding into memory new, flexible associations between unrelated items, while the adjacent medial temporal lobe (MTL) cortex, comprising entorhinal, perirhinal, and parahippocampal cortex (PHC), is more critical for single item recognition (e.g., Eichenbaum et al., 1994; Cohen et al., 1997; Eichenbaum, 1997; see also Henke, 2010 for a related theory). "
    [Show abstract] [Hide abstract] ABSTRACT: The neural substrates of associative and item priming and recognition were investigated in a functional magnetic resonance imaging (fMRI) study over two separate sessions. In the priming session, participants decided which object of a pair was bigger during both study and test phases. In the recognition session, participants saw different object pairs and performed the same size-judgement task followed by an associative recognition memory task. Associative priming was accompanied by reduced activity in the right middle occipital gyrus as well as in bilateral hippocampus. Object item priming was accompanied by reduced activity in extensive priming-related areas in the bilateral occipitotemporofrontal cortex, as well as in the perirhinal cortex, but not in the hippocampus. Associative recognition was characterised by activity increases in regions linked to recollection, such as the hippocampus, posterior cingulate cortex, anterior medial frontal gyrus and posterior parahippocampal cortex. Item object priming and recognition recruited broadly overlapping regions (e.g., bilateral middle occipital and prefrontal cortices, left fusiform gyrus), even though the BOLD response was in opposite directions. These regions along with the precuneus, where both item priming and recognition were accompanied by activation, have been found to respond to object familiarity. The minimal structural overlap between object associative priming and recollection-based associative recognition suggests that they depend on largely different stimulus-related information and that the different directions of effect indicate distinct retrieval mechanisms. In contrast, item priming and familiarity-based recognition seemed mainly based on common memory information, although the extent of common processing between priming and familiarity remains unclear. Further implications of these findings are discussed. This article is protected by copyright. All rights reserved.
    No preview · Article · Sep 2015 · Hippocampus
    • "The current data do not suggest that structural differences in MTL account for individual differences in associative memory. At first glance, this stands in contrast to previous functional MRI studies, which have shown involvement of HC in between-item binding among younger adults (Chua et al., 2007; Qin et al., 2009; Rodrigue and Raz, 2004; Westerberg et al., 2012). However, the present results are in line with findings on older adults by Rajah et al. (2010a,b), who reported no relation between HC volume and context-memory performance. "
    [Show abstract] [Hide abstract] ABSTRACT: Associative memory involves binding two or more items into a coherent memory episode. Relative to memory for single items, associative memory declines greatly in aging. However, older individuals vary substantially in their ability to memorize associative information. Although functional studies link associative memory to the medial temporal lobe (MTL) and prefrontal cortex (PFC), little is known about how volumetric differences in MTL and PFC might contribute to individual differences in associative memory. We investigated regional gray-matter volumes related to individual differences in associative memory in a sample of healthy older adults (n=54; age=60years). To differentiate item from associative memory, participants intentionally learned face-scene picture pairs before performing a recognition task that included single faces, scenes, and face-scene pairs. Gray-matter volumes were analyzed using voxel-based morphometry region-of-interest (ROI) analyses. To examine volumetric differences specifically for associative memory, item memory was controlled for in the analyses. Behavioral results revealed large variability in associative memory that mainly originated from differences in false-alarm rates. Moreover, associative memory was independent of individuals' ability to remember single items. Older adults with better associative memory showed larger gray-matter volumes primarily in regions of the left and right lateral PFC. These findings provide evidence for the importance of PFC in intentional learning of associations, likely because of its involvement in organizational and strategic processes that distinguish older adults with good from those with poor associative memory. Copyright © 2015. Published by Elsevier Inc.
    No preview · Article · Jun 2015 · NeuroImage
Show more