Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus
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Although hippocampal neurogenesis has been described in many adult mammals, the functional impact of this process on physiology and behavior remains unclear. In the present study, we used two independent methods to ablate hippocampal neurogenesis and found that each procedure caused a limited behavioral deficit and a loss of synaptic plasticity within the dentate gyrus. Specifically, focal X irradiation of the hippocampus or genetic ablation of glial fibrillary acidic protein-positive neural progenitor cells impaired contextual fear conditioning but not cued conditioning. Hippocampal-dependent spatial learning tasks such as the Morris water maze and Y maze were unaffected. These findings show that adult-born neurons make a distinct contribution to some but not all hippocampal functions. In a parallel set of experiments, we show that long-term potentiation elicited in the dentate gyrus in the absence of GABA blockers requires the presence of new neurons, as it is eliminated by each of our ablation procedures. These data show that new hippocampal neurons can be preferentially recruited over mature granule cells in vitro and may provide a framework for how this small cell population can influence behavior.
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Contradictory studies have found either no effect of reduced neurogenesis on hippocampal cognition or only on certain types of hippocampal cognitive tests, and one study found that absence of new neurons improves cognitive function.
“On the other hand, contradictory studies have found either no effect of reduced neurogenesis on hippocampal cognition (Groves et al., 2013; Saxe et al., 2006; Shors et al., 2002) or only on certain types of hippocampal cognitive tests (Shors et al., 2002). One study has even found that the absence of new neurons improves cognitive function (Saxe et al., 2007).”
From Adult neurogenesis, glia, and the extracellular matrix (2019) · cites this paper as Saxe et al., 2006
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“BrdU and Tuj-1 immunofluorescent staining Environmental enrichment is one of the strongest enhancers of adult neurogenesis and trophic factors secretion (van Praag et al., 2000), which were implicated in memory processes (Gross, 2000; Kempermann et al., 2004; Saxe et al., 2006).”
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“and reduced by blocking neurogenesis, whereas cued (fear) learning is neurogenesisindependent (Saxe et al., 2006).”
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“This includes the possibility of influencing non-neuronal cell lineages (through targeting GFAP; Saxe et al., 2006) and Nestin (Deng et al.”
BackgroundSocial regulation of adult neurogenesis in a eusocial mammal
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Self-citation
- Authors
- Saxe, M. D., Battaglia, F., Wang, J.-W., Malleret, G., David, D. J., Monckton, J. E., Garcia, A. D. R., Sofroniew, M. V., Kandel, E. R., Santarelli, L., Hen, R., & Drew, M. R.
- Affiliations
- Columbia University (US)
- *Center For Neurobiology and Behavior,
- Université Paris-Sud (FR)
- University of California, Los Angeles (US)
- Howard Hughes Medical Institute (US)
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2006-11-14
- Volume
- 103
- Issue
- 46
- Pages
- 17501-17506
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC1859958
- OpenAlex
- W2108461283
- Cited by
- 1,020
- References
- 45
- Citations by year
- 2026: 7 · 2025: 20 · 2024: 15 · 2023: 25 · 2022: 30 · 2021: 44 · 2020: 45 · 2019: 50 · 2018: 54 · 2017: 58 · 2016: 66 · 2015: 59 · 2014: 83 · 2013: 61 · 2012: 73
- FWCI
- 14.99
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- 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
- adult hippocampal neurogenesis, contextual fear conditioning, dentate gyrus, synaptic plasticity, long-term potentiation, glial fibrillary acidic protein, neural progenitor cells, X-ray irradiation, spatial learning, granule cells, GABAergic inhibition
- MeSH terms
- Animals, Conditioning, Psychological, Electrophysiology, Fear, Glial Fibrillary Acidic Protein, Hippocampus, Male, Memory, Mice, Transgenic, Neuronal Plasticity, Neurons, Thymidine Kinase, Mice
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