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.

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Available from: Shaozheng Qin,
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    • "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. "
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    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.
    NeuroImage 06/2015; 118. DOI:10.1016/j.neuroimage.2015.06.002 · 6.36 Impact Factor
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    • "Several neuroimaging studies have reported that during encoding, neural activity in the frontal, occipital, and medial temporal regions differs according to whether the related source of the item was remembered in a subsequent memory test [3] [4] [5] [6] [7] [8] [9] [10] [11] [12] [13] . These differences in neural activity are often described as " subsequent source memory effects " [14] . "
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    ABSTRACT: Episodic memories are composed of various interrelated elements, including those specific to items of central interest and those pertaining to related features, such as the color, shape, size, spatial location, temporal order, and media or modalities of presentation. Memory about a core item (such as a word, object, or picture) is called item memory while memory about the context or related fea-tures of a core item is defined as source memory. What determines which sources within an episode are successfully remembered is of particular interest to researchers. Behavioral evidence suggests that the orientation of a memory task influences whether the related source of the item will be re-membered later. This study explored changes in the hippocampus and prefrontal cortex while par-ticipants completed two tasks: an item-oriented task and a source-oriented task. We used functional MRI to investigate the neural mechanisms by which task orientation influences source encoding. We found that subsequent source memory effects in the right prefrontal cortex and hippocampus were modulated by task orientation, whereas task orientation modulated item memory effects in the prefrontal cortex. These findings highlight the possibility that the hippocampus contributes to the intentional encoding of item-source associations, whereas the prefrontal cortex is biased toward processing information to which attention is directed.
    Neural Regeneration Research 09/2013; 8(26):2424-31. DOI:10.3969/j.issn.1673-5374.2013.26.003 · 0.22 Impact Factor
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    • "These findings support the view that components of the MTL perform qualitatively distinct computations and that this heterogeneity of function does not simply reflect memory strength (Montaldi & Mayes, 2010). The data are also consistent with dual-process models of the neural bases of recognition memory (Aggleton & Brown, 2006; Brown & Aggleton, 2001; Diana et al., 2007; Mayes et al., 2007; Montaldi & Mayes, 2010) and other studies distinguishing between the roles of the PRC and the hippocampus with respect to familiarity and recollection (e.g., Cohn et al., 2009; Davachi et al., 2003; Diana et al., 2010; Greve, Evans, Graham, & Wilding, 2011; Montaldi et al., 2006; Qin et al., 2009; Ranganath et al., 2004; Yonelinas et al., 2005; but see Kirwan et al., 2008; Smith, Wixted, & Squire, 2011; Song, Jeneson, & Squire, 2011). "
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    ABSTRACT: Two experiments explored eye measures (fixations and pupil response patterns) and brain responses (BOLD) accompanying the recognition of visual object stimuli based on familiarity and recollection. In both experiments, the use of a modified remember/know procedure led to high confidence and matched accuracy levels characterising strong familiarity (F3) and recollection (R) responses. In Experiment 1, visual scanning behaviour at retrieval distinguished familiarity-based from recollection-based recognition. Recollection, relative to strength-matched familiarity, involved significantly larger pupil dilations and more dispersed fixation patterns. In Experiment 2, the hippocampus was selectively activated for recollected stimuli, while no evidence of activation was observed in the hippocampus for strong familiarity of matched accuracy. Recollection also activated the parahippocampal cortex (PHC), while the adjacent perirhinal cortex (PRC) was actively engaged in response to strong familiarity (than to recollection). Activity in prefrontal and parietal areas differentiated familiarity and recollection in both the extent and the magnitude of activity they exhibited, while the dorsomedial thalamus showed selective familiarity-related activity, and the ventrolateral and anterior thalamus selective recollection-related activity. These findings are consistent with the view that the hippocampus and PRC play contrasting roles in supporting recollection and familiarity and that these differences are not a result of differences in memory strength. Overall, the combined pupil dilation, eye movement and fMRI data suggest the operation of recognition mechanisms drawing differentially on familiarity and recollection, whose neural bases are distinct within the MTL.
    Neuropsychologia 08/2012; 50(13). DOI:10.1016/j.neuropsychologia.2012.08.001 · 3.30 Impact Factor
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