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Resolving New Memories: A Critical Look at the Dentate Gyrus, Adult Neurogenesis, and Pattern Separation
Open accessAbstract
Recently, investigation of new neurons in memory formation has focused on a specific function-pattern separation. However, it has been difficult to reconcile the form of separation tested in behavioral tasks with how it is conceptualized according to computational and electrophysiology perspectives. Here, we propose a memory resolution hypothesis that considers the unique information contributions of broadly tuned young neurons and highly specific mature neurons and describe how the fidelity of memories can relate to spatial and contextual discrimination. See the related Perspective from Sahay, Wilson, and Hen, "Pattern Separation: A Common Function for New Neurons in Hippocampus and Olfactory Bulb," in this issue of Neuron.
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“Yet, hippocampal adult neurogenesis is required for learning and memory, in particular for pattern separation, i.e., the ability to disentangle similar memory patterns within the output to CA3; indeed this ability, although inherent to the dentate gyrus circuitry, is strongly enhanced from the addition of new neurons to the existing circuits (Aimone et al., 2011;Sahay et al., 2011;Tirone et al., 2”
From Depression and adult neurogenesis: Positive effects of the antidepressant fluoxetine and of physical exercise (2018) · cites this paper as Aimone et al., 2011
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“The dentate gyrus (DG) subregion of the hippocampus mediates episodic memory formation and the disambiguation of similar but discrete events, a phenomenon known as pattern separation [3], [4], [5], [6].”
From Arf4 Determines Dentate Gyrus-Mediated Pattern Separation by Regulating Dendritic Spine Development (2012) · cites this paper as [4]
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“This primarily occurs through the role that neurogenesis plays in facilitating memory formation by dictating a computational mechanism known as pattern separation (Aimone et al., 2011; Sahay et al., 2011).”
From Aerobic Exercise as a Tool to Improve Hippocampal Plasticity and Function in Humans: Practical Implications for Mental Health Treatment (2016) · cites this paper as Aimone et al., 2011
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“The finding that neurogenesis persists into adulthood has generated a great deal of enthusiasm, centering on the idea that promoting this process would benefit memory (Aimone et al. 2011; Sahay et al. 2011a).”
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“These adult-born GCs contribute to cognitive functions (Clelland et al., 2009; Aimone et al., 2011; Sahay et al., 2011; Nakashiba et al., 2012) and emotional regulation (Santarelli et al., 2003; Snyder et al., 2011) of the animal.”
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“There is also accumulating data showing that hippocampal neurogenesis is an important player for pattern separation (Aimone et al., 2010, 2011; Sahay et al., 2011a,b; Tronel et al., 2012).”
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Piatti, V. C., Ewell, L. A., & Leutgeb, J. K. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00050 · Cited by 160
“Other computational models support the involvement of immature adult-born DGCs in the pattern separation computation (Aimone et al., 2011; Nogues et al., 2012).”
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“…clearance of hippocampal memory traces, reorganization of memory to extrahippocampal substrates, and certain antidepressant-induced behavioral responses in Developmental Neurobiology specific mouse strains (Sahay and Hen, 2007; Deng et al., 2010; Aimone et al., 2011; Sahay et al., 2011).”
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“…neurons to modify the hippocampal network is at least in part the result of their specific connectivity pattern and electrophysiological properties that arise transiently during their maturation (Ge et al., 2007; Aimone et al., 2011; Sahay et al., 2011; Li et al., 2012; Marín-Burgin et al., 2012).”
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“These newborn neurons integrate into the circuity of the DG, contributing to behaviors such as pattern separation (Aimone et al. 2011) and spatial learning (Dupret et al.”
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“Neurogenesis has been implicated in cognitive performance and emotional responses in rodents (75,76).”
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“Interestingly, ablation of new neurons impairs pattern separation, whereas enhanced neurogenesis is associated with improvement (2, 27, 106).”
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“This function has not been fully elucidated and continues to be a topic of intense investigation and discussion (Gheusi et al., 2009; Aimone et al., 2011; Lazic, 2012; Gheusi et al., 2013; Cameron and Glover, 2015; Miller and Hen, 2015; Opendak and Gould, 2015).”
BackgroundBehavioral pattern separation and its link to the neural mechanisms of fear generalization
Lange, I., Goossens, L., Michielse, S., Bakker, J. M., Lissek, S. M., Papalini, S., Verhagen, S. J. W., Leibold, N. K., Marcelis, M. C., Wichers, M., et al. (2017) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsx104 · Cited by 114
“…awareness during threat processing and fear learning (Jovanovic et al., 2012; Lueken et al., 2014; Fullana et al., 2016), and is thought to contribute to fear discrimination processes due to its essential role in pattern separation (Clelland et al., 2009; Aimone et al., 2011; Sahay et al., 2011).”
BackgroundEffects of early-life stress on cognitive function and hippocampal structure in female rodents.
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“Changes in proliferation and DG structure may further affect downstream processing within the hippocampus and alterations in neurogenesis have indeed been linked to cognitive changes (Clelland et al., 2009; Creer et al., 2010; Aimone et al., 2011; Sahay et al., 2011a,b; Oomen et al., 2014).”
CBP is required for environmental enrichment‐induced neurogenesis and cognitive enhancement
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“…current theoretical models describing the role of the DG in the processing and storage of spatial informa- tion, newborn neurons in the subgranular zone (SGZ) are hypothesized to facilitate pattern separation and spatial memory resolution (Deng et al, 2010; Aimone et al, 2011; Sahay et al, 2011b).”
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“These neurons become structurally and functionally integrated into the hippocampal circuitry where they critically contribute to hippocampal-dependent learning and memory processes (Kee et al., 2007; Aimone et al., 2011; Gu et al., 2012).”
BackgroundThe subiculum: Unique hippocampal hub and more
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Replay in Deep Learning: Current Approaches and Missing Biological Elements
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“From the perspective of close association between hippocampal neurogenesis and cognitive and mood function [1,27,28,47,48], it is likely that NSC grafting mediated normal extent and pattern of neurogenesis in the injured hippocampus and enhanced neurogenesis in the contralateral”
BackgroundHow to make a hippocampal dentate gyrus granule neuron
Yu, D. X., Marchetto, M. C., & Gage, F. H. (2014) · Development · doi:10.1242/dev.096776 · Cited by 109
“…existing hippocampal circuitry, where they play a fundamental role in learning and spatial memory formation by performing pattern separation on inputs from the entorhinal cortex, an area of the brain located in the medial temporal lobe (McHugh et al., 2007; Zhao et al., 2008; Aimone et al., 2011).”
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“As such, it is to our knowledge unique in being a gene with this property of having a strong and specific role in survival and maturation of adult-born DGCs during the critical period within which they establish appropriate connectivity and have unique functional properties relevant to hippocampal information processi…”
Background
Metadata
- Authors
- Aimone, J. B., Deng, W., & Gage, F. H.
- Affiliations
- Salk Institute for Biological Studies (US)
- Corresponding author
- Gage, Fred H.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2011-05
- Volume
- 70
- Issue
- 4
- Pages
- 589-596
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC3240575
- OpenAlex
- W2069785065
- Cited by
- 663
- References
- 49
- Citations by year
- 2026: 15 · 2025: 29 · 2024: 20 · 2023: 25 · 2022: 27 · 2021: 31 · 2020: 41 · 2019: 38 · 2018: 39 · 2017: 64 · 2016: 62 · 2015: 62 · 2014: 71 · 2013: 63 · 2012: 58
- FWCI
- 5.76
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Foundation for the National Institutes of Health
- James S. McDonnell Foundation
- National Institute of Mental Health (R01MH090258)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- dentate gyrus, adult neurogenesis, pattern separation, hippocampus, spatial discrimination, contextual discrimination, memory fidelity, mature neurons, memory formation
- MeSH terms
- Adult, Age Factors, Animals, Humans, Memory, Dentate Gyrus, Neurogenesis
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