Associative retrieval processes in the human medial temporal lobe: Hippocampal retrieval success and CA1 mismatch detection

Chen, Janice; Olsen, Rosanna K.; Preston, Alison R.; Glover, Gary H.; Wagner, Anthony D.

doi:10.1101/lm.2135211

Cited by 112 publications

(119 citation statements)

References 49 publications

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“…This result converges with electrophysiological data from rodents (Montgomery and Buzsaki, 2007) showing greater coherence between local field potentials generated by areas CA3 and CA1 when rats paused at decision points on a maze, potentially reflecting the retrieval of past trial outcomes. Additionally, synchronous firing between areas CA3 and CA1 has been related to replay during sharp wave ripples (Carr et al, 2012). Although this previous work demonstrates that CA1-CA3 connectivity increases during periods when retrieval may be more likely to occur, our results link this effect directly to memory retrieval by demonstrating that functional connectivity between DG/CA3 and area CA1 correlates with retrieval success.…”

Section: Discussionmentioning

confidence: 43%

“…More broadly, this study serves as an example of how the development of high-resolution fMRI has served as a critical bridge between hippocampal research performed in humans and animals (Carr et al, 2010). In recent years, high-resolution hippocampal imaging has been used to determine how BOLD activation in distinct hippocampal subregions is related to episodic encoding and retrieval (Zeineh et al, 2003;Eldridge et al, 2005;Preston et al, 2010), computational processes such as pattern separation and novelty detection (Kirwan and Stark, 2007;Bakker et al, 2008;Chen et al, 2011;Duncan et al, 2012a;Lacy et al, 2011), and reward modulation of memory (Wolosin et al, 2012).…”

Section: Discussionmentioning

confidence: 99%

“…In recent years, high-resolution hippocampal imaging has been used to determine how BOLD activation in distinct hippocampal subregions is related to episodic encoding and retrieval (Zeineh et al, 2003;Eldridge et al, 2005;Preston et al, 2010), computational processes such as pattern separation and novelty detection (Kirwan and Stark, 2007;Bakker et al, 2008;Chen et al, 2011;Duncan et al, 2012a;Lacy et al, 2011), and reward modulation of memory (Wolosin et al, 2012). The current study builds off of this foundation to investigate a question that had previously only been explored in animal models: How do interactions between hippocampal subregions differentially support memory encoding and retrieval?…”

Section: Discussionmentioning

confidence: 99%

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Associative Encoding and Retrieval Are Predicted by Functional Connectivity in Distinct Hippocampal Area CA1 Pathways

Tompary²,

2014

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Determining how the hippocampus supports the unique demands of memory encoding and retrieval is fundamental for understanding the biological basis of episodic memory. One possibility proposed by theoretical models is that the distinct computational demands of encoding and retrieval are accommodated by shifts in the functional interaction between the hippocampal CA1 subregion and its input structures. However, empirical tests of this hypothesis are lacking. To test this in humans, we used high-resolution fMRI to measure functional connectivity between hippocampal area CA1 and regions of the medial temporal lobe and midbrain during extended blocks of associative encoding and retrieval tasks. We found evidence for a double dissociation between the pathways supporting successful encoding and retrieval. Specifically, during the associative encoding task, but not the retrieval task, functional connectivity only between area CA1 and the ventral tegmental area predicted associative long-term memory. In contrast, connectivity between area CA1 and DG/CA3 was greater, on average, during the retrieval task compared with the encoding task, and, importantly, the strength of this connectivity significantly correlated with retrieval success. Together, these findings serve as an important first step toward understanding how the demands of fundamental memory processes may be met by changes in the relative strength of connectivity within hippocampal pathways.Key words: CA1; CA3; functional connectivity; high-resolution fMRI; hippocampus; VTA IntroductionIn everyday experience, memory encoding and retrieval appear seamlessly intertwined; encoding provides material that will later be retrieved, whereas retrieval supplies context to facilitate meaningful encoding. However, the neural mechanisms thought to underlie these processes have been hypothesized to place opposing demands on the episodic memory system (Marr, 1971;O'Reilly and McClelland, 1994). Specifically, the rapid formation of memory traces representing single episodes requires high levels of synaptic plasticity that, during retrieval, could lead to the overwriting of stored memories. Conversely, successful associative retrieval requires that cues reactivate related memory traces and thus benefits from a low threshold for memory reinstatement, but reinstating related memories at the time of encoding could lead to proactive interference (O'Reilly and McClelland, 1994).Although it is generally agreed that the hippocampus is critical for both encoding and retrieval (Scoville and Milner, 1957;Eichenbaum et al., 2007; Squire et al., 2007), it remains unknown how the hippocampus supports the complex demands of both processes. However, the unique pattern of afferent projections converging on area CA1, the major hippocampal output subregion, may provide an answer. On the one hand, inputs to CA1 might differentially support long-term memory encoding. Specifically, both late-phase long-term potentiation (LTP) at CA1 synapses and long-term memory formation have been demonstrated to be...

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Section: Discussionmentioning

confidence: 43%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Associative Encoding and Retrieval Are Predicted by Functional Connectivity in Distinct Hippocampal Area CA1 Pathways

Tompary²,

2014

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“…Evidence from lesion and neuroimaging studies suggests that discrete hippocampal substructures carry out discrete functions. For example, CA1 is proposed to act as a comparator, detecting mismatch between previously stored memory traces and currently perceived stimuli (Chen, Olsen, Preston, Glover, & Wagner, 2011;Duncan, Ketz, Inati, & Davachi, 2012). The dentate gyrus and CA3 are thought to subserve two complementary processes: pattern separation, the process of transforming neural representations that code our memories of related events, items or locations into more dissimilar, non-overlapping neural representations; and pattern completion which facilitates recall when a memory is cued by a noisy or incomplete set of cues (Bakker, Kirwan, Miller, & Stark, 2008;Gilbert, Kesner, & DeCoteau, 1998;Gold & Kesner, 2005;Leutgeb, Leutgeb, Moser, & Moser, 2007;Nakazawa et al, 2002;Neunuebel & Knierim, 2014).…”

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confidence: 99%

Improvement of allocentric spatial memory resolution in children from 2 to 4 years of age

Lambert

Lavenex

2015

International Journal of Behavioral Development

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Allocentric spatial memory, the memory for locations coded in relation to objects comprising our environment, is a fundamental component of episodic memory and is dependent on the integrity of the hippocampal formation in adulthood. Previous research from different laboratories reported that basic allocentric spatial memory abilities are reliably observed in children after 2 years of age. Based on work performed in monkeys and rats, we had proposed that the functional maturation of direct entorhinal cortex projections to the CA1 field of the hippocampus might underlie the emergence of basic allocentric spatial memory. We also proposed that the protracted development of the dentate gyrus and its projections to the CA3 field of the hippocampus might underlie the development of high-resolution allocentric spatial memory capacities, based on the essential contribution of these structures to the process known as pattern separation. Here, we present an experiment designed to assess the development of spatial pattern separation capacities and its impact on allocentric spatial memory performance in children from 18 to 48 months of age. We found that: (1) allocentric spatial memory performance improved with age, (2) as compared to younger children, a greater number of children older than 36 months advanced to the final stage requiring the highest degree of spatial resolution, and (3) children that failed at different stages exhibited difficulties in discriminating locations that required higher spatial resolution abilities. These results are consistent with the hypothesis that improvements in human spatial memory performance might be linked to improvements in pattern separation capacities.

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“…The DG and CA3 are thought to play a crucial role in rapid acquisition of context memory, with the DG imposing a distinct firing pattern on the CA3 and the latter forming an auto-associative network through the extensive collaterals present in that region (Marr 1971;O'Reilly and Rudy 2001;Krasne et al 2015). The CA1, on the other hand, is not completely understood, but is thought to play a role in a variety of both essential and modulatory functions including memory consolidation (Remondes and Schuman 2004), generalization (Basu et al 2016), comparison (Chen et al 2011;Duncan et al 2012), and encoding of specific items and their inter-relation within the context (Lee et al 2005;Griffin et al 2007;Greene et al 2013). Our findings that the DG/CA3 is more rapidly engaged than the CA1 therefore agree with previous work (Miyashita et al 2009, Pevzner et al 2012 and are consistent with the idea that the DG and CA3 lay down the initial memory framework that supports rapid conditioning (McHugh et al 2007, McHugh andTonegawa 2009) and that all regions subsequently expand upon this framework to create a more comprehensive representation as the session continues.…”

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confidence: 99%

Dissociation between complete hippocampal context memory formation and context fear acquisition

et al. 2017

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Rodents require a minimal time period to explore a context prior to footshock to display plateau-level context fear at test. To investigate whether this rapid fear plateau reflects complete memory formation within that short time-frame, we used the immediate-early gene product Arc as an indicator of hippocampal context memory formation-related activity. We found that hippocampal Arc expression continued to increase well past the minimal time required for plateau-level fear. This raises the possibility that context fear conditioning occurs more rapidly than complete memory formation. Thus, animals may be able to condition robustly to both complete and incomplete contextual representations.

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Associative retrieval processes in the human medial temporal lobe: Hippocampal retrieval success and CA1 mismatch detection

Cited by 112 publications

References 49 publications

Associative Encoding and Retrieval Are Predicted by Functional Connectivity in Distinct Hippocampal Area CA1 Pathways

Associative Encoding and Retrieval Are Predicted by Functional Connectivity in Distinct Hippocampal Area CA1 Pathways

Improvement of allocentric spatial memory resolution in children from 2 to 4 years of age

Dissociation between complete hippocampal context memory formation and context fear acquisition

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