How hippocampus and cortex contribute to recognition memory: Revisiting the complementary learning systems model

Norman, Kenneth A.

doi:10.1002/hipo.20855

Cited by 217 publications

(236 citation statements)

References 86 publications

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“…Entropy is a measure of the richness of information encoded in a sequence of events. Applying this concept to the neural networks , it has been demonstrated that the degree of information that is encoded in neural assemblies increases as a function of desynchronization and decreases as a function of synchronized firing patterns [94,95,96]. This hypothesis has been confirmed in clinical studies in patients with memory deficits [97], as well as during states where there is little cognitive processing (e.g.…”

Section: Discussionmentioning

confidence: 98%

Electroencephalographic Upper/Low Alpha Frequency Power Ratio Relates to Cortex Thinning in Mild Cognitive Impairment

et al. 2014

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Objective: Temporoparietal cortex thinning is associated with mild cognitive impairment (MCI) due to Alzheimer disease (AD). The increase in EEG upper/low α frequency power ratio has been associated with AD converter MCI subjects. We investigated the association of the EEG upper/low α frequency power ratio with patterns of cortical thickness in MCI. Methods: 74 adult subjects with MCI underwent clinical and neuropsychological evaluation, electroencephalography (EEG) recording and high-resolution 3-dimensional magnetic resonance imaging (MRI). The EEG upper/low α frequency power ratio as well as cortical thickness were computed for each subject. Three MCI groups were detected according to increasing tertile values of EEG upper/low α frequency power ratios, and the difference of cortical thickness among the groups was estimated. Results: The EEG high upper/low α frequency power ratio group had a total cortical grey matter volume reduction of 471 mm², greater than that of the EEG low upper/low α frequency power ratio group (p < 0.001). The EEG high upper/low α frequency power ratio group showed a similar but less marked pattern (160 mm²) of cortical thinning when compared to the EEG middle upper/low α frequency power ratio group (p < 0.001). Moreover, the EEG high upper/low α frequency power ratio group had wider cortical thinning than other groups, mapped to the supramarginal gyrus and precuneus bilaterally. No significant regional cortical thickness differences were found between middle and low EEG upper/low α frequency power ratio groups. Conclusion: A high EEG upper/low α frequency power ratio was associated with temporoparietal cortical thinning in MCI subjects. The combination of upper/low α frequency power ratio and cortical thickness measurement could be useful for identifying individuals at risk for progression to AD dementia and may be of value in the clinical context.

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Section: Discussionmentioning

confidence: 98%

Electroencephalographic Upper/Low Alpha Frequency Power Ratio Relates to Cortex Thinning in Mild Cognitive Impairment

et al. 2014

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“…Aging is associated with a decline in episodic memory formation (37), spatial memory and navigation (38), contextual source memory (39), and recollection (40,41). These functions require intact pattern separation circuitry (7,42). Here, we examined the potential neural locus for pattern separation deficits and uncovered both a functional change in the DG/CA3 network as well as a related structural change in the perforant path, both of which predicted pattern separation abilities.…”

Section: Discussionmentioning

confidence: 99%

Age-related memory deficits linked to circuit-specific disruptions in the hippocampus

Yassa

Mattfeld

Stark

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

393

406

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Converging data from rodents and humans have demonstrated an age-related decline in pattern separation abilities (the ability to discriminate among similar experiences). Several studies have proposed the dentate and CA3 subfields of the hippocampus as the potential locus of this change. Specifically, these studies identified rigidity in place cell remapping in similar environments in the CA3. We used high-resolution fMRI to examine activity profiles in the dentate gyrus and CA3 in young and older adults as stimulus similarity was incrementally varied. We report evidence for "representational rigidity" in older adults' dentate/CA3 that is linked to behavioral discrimination deficits. Using ultrahigh-resolution diffusion imaging, we quantified both the integrity of the perforant path as well as dentate/CA3 dendritic changes and found that both were correlated with dentate/CA3 functional rigidity. These results highlight structural and functional alterations in the hippocampal network that predict age-related changes in memory function and present potential targets for intervention.L ong-term memory function is commonly known to deteriorate with increasing age. One of the sites that undergo the earliest changes is the hippocampus (1, 2), which has a well-known role in learning new facts and remembering events (3). Recently, electrophysiological recording studies in aged rodents have shed light on some of the possible neural mechanisms in the hippocampus that underlie this decline (1). These studies have demonstrated "rigidity" in aged CA3 place cell firing patterns in similar environments. In contrast to young CA3 place cells, which readily remap and shift their representations in these environments, aged CA3 place cells retain their original fields despite the changes in the environment. These data strongly suggest that aging is associated with a diminished capacity for pattern separation (learning new information by decorrelating similar inputs to avoid interference) and an increased propensity for pattern completion (retrieval of previously stored information from a partial cue), and further suggest that this shift could be the result of a functional imbalance in the hippocampal dentate gyrus (DG) and CA3 network.The role of hippocampal subfields in these key processes has long been hypothesized in computational models (4-7). The models suggest that the DG granule cells are capable of performing especially strong pattern separation on the distributed representations arriving from layer II entorhinal neurons, projecting this signal onto the CA3 subfield of the hippocampus via the strong mossy fiber pathway. Empirical evidence for the involvement of the DG and CA3 in pattern separation has been demonstrated by using electrophysiological recordings (8-10), immediate-early genes (11), and high-resolution functional MRI in humans (12, 13). Ablation studies using DG-specific ibotenic acid lesions (14), as well as genetic NMDA receptor knockouts (15), have additionally shown that the DG is critical for, and the likely ...

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“…One dominant theoretical perspective on the functional contributions of different MTL subregions to memory, the "complementary learning systems" model, holds that a hippocampal "pattern separation" mechanism supports memory for events by orthogonalizing (making more distinct) neural representations during encoding, allowing later retrieval cues to trigger memory for a unique event (O'Reilly and McClelland 1994;McClelland et al 1995;O'Reilly and Rudy 2001;Norman and O'Reilly 2003;Norman 2010). Conversely, this perspective holds that the neighboring MTL cortex supports memory by gradually encoding neural representations that capture the commonalities across similar stimuli, permitting later item recognition on the basis of global similarity between the present and past.…”

Section: Multivariate Fmri Analyses and Memory Theorymentioning

confidence: 99%

Noninvasive Functional and Anatomical Imaging of the Human Medial Temporal Lobe

Brown

Staresina

Wagner

2015

Cold Spring Harb Perspect Biol

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The ability to remember life's events, and to leverage memory to guide behavior, defines who we are and is critical for everyday functioning. The neural mechanisms supporting such mnemonic experiences are multiprocess and multinetwork in nature, which creates challenges for studying them in humans and animals. Advances in noninvasive neuroimaging techniques have enabled the investigation of how specific neural structures and networks contribute to human memory at its many cognitive and mechanistic levels. In this review, we discuss how functional and anatomical imaging has provided novel insights into the types of information represented in, and the computations performed by, specific medial temporal lobe (MTL) regions, and we consider how interactions between the MTL and other cortical and subcortical structures influence what we learn and remember. By leveraging imaging, researchers have markedly advanced understanding of how the MTL subserves declarative memory and enables navigation of our physical and mental worlds.O ne of the central aims of cognitive neuroscience research is to understand how human brain function relates to the mnemonic experiences that define much of who we are as individuals. Recent advances in noninvasive human neuroimaging have given rise to novel insights about the neural foundations of human memory, and have allowed neuroscientists to draw important connections between human and nonhuman animal research. Although noninvasive imaging techniques remain limited in their spatial resolution (we cannot yet describe the behavior of individual neurons in the human brain without implanting electrodes in patients undergoing brain surgery), they also have important strengths that have allowed researchers to significantly advance mechanistic accounts of learning and memory. In this review, we begin with a historical perspective on noninvasive neuroimaging techniques and their application to the study of memory encoding. We then introduce more recent cutting-edge methodological approaches, as we discuss specific domains of memory theory that they have helped advance. Drawing on research examining the medial temporal lobe (MTL), we emphasize the power of such imaging techniques to allow scientists to make inferences about the types of mnemonic information represented by distinct brain areas, and to understand how the funcEditors: Eric R. Kandel, Yadin Dudai, and Mark R. Mayford Additional Perspectives on Learning and Memory available at

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How hippocampus and cortex contribute to recognition memory: Revisiting the complementary learning systems model

Cited by 217 publications

References 86 publications

Electroencephalographic Upper/Low Alpha Frequency Power Ratio Relates to Cortex Thinning in Mild Cognitive Impairment

Electroencephalographic Upper/Low Alpha Frequency Power Ratio Relates to Cortex Thinning in Mild Cognitive Impairment

Age-related memory deficits linked to circuit-specific disruptions in the hippocampus

Noninvasive Functional and Anatomical Imaging of the Human Medial Temporal Lobe

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