Excitation-Neurogenesis Coupling in Adult Neural Stem/Progenitor Cells
Open accessAbstract
A wide variety of in vivo manipulations influence neurogenesis in the adult hippocampus. It is not known, however, if adult neural stem/progenitor cells (NPCs) can intrinsically sense excitatory neural activity and thereby implement a direct coupling between excitation and neurogenesis. Moreover, the theoretical significance of activity-dependent neurogenesis in hippocampal-type memory processing networks has not been explored. Here we demonstrate that excitatory stimuli act directly on adult hippocampal NPCs to favor neuron production. The excitation is sensed via Ca(v)1.2/1.3 (L-type) Ca(2+) channels and NMDA receptors on the proliferating precursors. Excitation through this pathway acts to inhibit expression of the glial fate genes Hes1 and Id2 and increase expression of NeuroD, a positive regulator of neuronal differentiation. These activity-sensing properties of the adult NPCs, when applied as an "excitation-neurogenesis coupling rule" within a Hebbian neural network, predict significant advantages for both the temporary storage and the clearance of memories.
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The dynamic networks method mirrors the way the hippocampus in the human brain stores new memory through the formation of new neurons.
“The dynamic networks method mirrors the way the hippocampus in the human brain stores new memory through the formation of new neurons [93].”
From Human-inspired Perspectives: A Survey on AI Long-term Memory (2024) · cites this paper as [93]
Compared to non-parametric memory, the characteristics of parametric memory storing information implicitly within AI models are more akin to how the human brain produces new neurons or undergoes chemical changes.
“Furthermore, compared to non-parametric memory, the characteristics of parametric memory storing information implicitly within AI models are more akin to how the human brain produces new neurons or undergoes chemical changes [91, 93, 293, 94].”
From Human-inspired Perspectives: A Survey on AI Long-term Memory (2024) · cites this paper as [93]
Cites
The Medial Temporal Lobe Memory System
Squire, L. R., & Zola-Morgan, S. (1991) · Science · doi:10.1126/science.1896849 · Cited by 3,282 · see citing works
Long-Term Potentiation--A Decade of Progress?
Malenka, R. C., & Nicoll, A. R. A. (1999) · Science · doi:10.1126/science.285.5435.1870 · Cited by 2,729 · see citing works
Self-citationAstrocytes give rise to new neurons in the adult mammalian hippocampus
Seri, B., Garcı́a-Verdugo, J. M., McEwen, B. S., & Alvarez-Buylla, A. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-18-07153.2001 · Cited by 1,495 · see citing works
Irradiation induces neural precursor-cell dysfunction
Monje, M. L., Mizumatsu, S., Fike, J. R., & Palmer, T. D. (2002) · Nature Medicine · doi:10.1038/nm749 · Cited by 1,271 · see citing works
Self-citationCoordinated Interaction of Neurogenesis and Angiogenesis in the Adult Songbird Brain
Louissaint, A., Rao, S., Leventhal, C., & Goldman, S. A. (2002) · Neuron · doi:10.1016/s0896-6273(02)00722-5 · Cited by 735 · see citing works
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New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory?
Deng, W., Aimone, J. B., & Gage, F. H. (2010) · Nature reviews. Neuroscience · doi:10.1038/nrn2822 · Cited by 2,120 · see citing works
Stress, Depression, and Neuroplasticity: A Convergence of Mechanisms
Pittenger, C., & Duman, R. S. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301574 · Cited by 1,795 · see citing works
Electrical and synaptic integration of glioma into neural circuits
Venkatesh, H. S., Morishita, W., Geraghty, A. C., Silverbush, D., Gillespie, S. M., Arzt, M., Tam, L. T., Espenel, C., Ponnuswami, A., Ni, L., et al. (2019) · Nature · doi:10.1038/s41586-019-1563-y · Cited by 1,366 · see citing works
Self-citationAdult hippocampal neurogenesis in depression
Sahay, A., & Hen, R. (2007) · Nature Neuroscience · doi:10.1038/nn1969 · Cited by 1,206 · see citing works
Adult neurogenesis: from precursors to network and physiology
Abrous, D. N., Koehl, M., & Le Moal, M. (2005) · Physiological Reviews · doi:10.1152/physrev.00055.2003 · Cited by 971 · see citing works
Hippocampal Neurogenesis Regulates Forgetting During Adulthood and Infancy
Akers, K. G., Martinez-Canabal, A., Restivo, L., Yiu, A. P., De Cristofaro, A., Hsiang, H.-L. (., Wheeler, A. L., Guskjolen, A., Niibori, Y., Shoji, H., et al. (2014) · Science · doi:10.1126/science.1248903 · Cited by 761 · see citing works
The role of adult hippocampal neurogenesis in brain health and disease
Toda, T., Parylak, S. L., Linker, S. B., & Gage, F. H. (2019) · Molecular Psychiatry · doi:10.1038/s41380-018-0036-2 · Cited by 719 · see citing works
Hippocampal Neurogenesis: Regulation by Stress and Antidepressants
Dranovsky, A., & Hen, R. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.03.082 · Cited by 663 · see citing works
Regulation and function of adult neurogenesis: from genes to cognition.
Aimone, J. B., Li, Y., Lee, S. W., Clemenson, G. D., Deng, W., & Gage, F. H. (2014) · Physiological Reviews · doi:10.1152/physrev.00004.2014 · Cited by 635 · see citing works
Physical exercise prevents age-related decline in precursor cell activity in the mouse dentate gyrus
Kronenberg, G., Bick-Sander, A., Bunk, E., Wolf, C., Ehninger, D., & Kempermann, G. (2006) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2005.09.016 · Cited by 477 · see citing works
Excitatory GABA Action Is Essential for Morphological Maturation of Cortical Neurons <i>In Vivo</i>
Cancedda, L., Fiumelli, H., Chen, K., & Poo, M.-M. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.5169-06.2007 · Cited by 392 · see citing works
Boldrini, M., Santiago, A. N., Hen, R., Dwork, A. J., Rosoklija, G. B., Tamir, H., Arango, V., & John Mann, J. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.5 · Cited by 361 · see citing works
Boldrini, M., Hen, R., Underwood, M. D., Rosoklija, G. B., Dwork, A. J., Mann, J. J., & Arango, V. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.04.024 · Cited by 348 · see citing works
Why and how physical activity promotes experience-induced brain plasticity.
Kempermann, G., Fabel, K., Ehninger, D., Babu, H., Leal-Galicia, P., Garthe, A., & Wolf, S. A. (2010) · Frontiers in Neuroscience · doi:10.3389/fnins.2010.00189 · Cited by 334 · see citing works
Adult neurogenesis: integrating theories and separating functions
Aimone, J. B., Deng, W., & Gage, F. H. (2010) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2010.04.003 · Cited by 303 · see citing works
Seizures accelerate functional integration of adult-generated granule cells
Overstreet-Wadiche, L. S., Bromberg, D. A., Bensen, A. L., & Westbrook, G. L. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.5508-05.2006 · Cited by 266 · see citing works
Parvalbumin interneurons mediate neuronal circuitry-neurogenesis coupling in the adult hippocampus
Song, J., Sun, J., Moss, J., Wen, Z., Sun, G. J., Hsu, D., Zhong, C., Davoudi, H., Christian, K. M., Toni, N., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3572 · Cited by 223 · see citing works
Speisman, R. B., Kumar, A., Rani, A., Foster, T. C., & Ormerod, B. K. (2013) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2012.09.013 · Cited by 187 · see citing works
Forgetting as a form of adaptive engram cell plasticity
Ryan, T. J., & Frankland, P. W. (2022) · Nature reviews. Neuroscience · doi:10.1038/s41583-021-00548-3 · Cited by 182 · see citing works
Cognitive disorders and neurogenesis deficits in Huntington’s disease mice are rescued by fluoxetine
Grote, H. E., Bull, N. D., Howard, M. L., Van Dellen, A., Blakemore, C., Bartlett, P. F., & Hannan, A. J. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04365.x · Cited by 179 · see citing works
Adult neurogenesis and cellular brain repair with neural progenitors, precursors and stem cells
Shivraj Sohur, U., Emsley, J. G., Mitchell, B. D., & Macklis, J. D. (2006) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2006.1887 · Cited by 170 · see citing works
Steiner, B., Zurborg, S., Hörster, H., Fabel, K., & Kempermann, G. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.04.023 · Cited by 165 · see citing works
The effects of physical exercise and cognitive training on memory and neurotrophic factors.
Heisz, J. J., Clark, I. B., Bonin, K., Paolucci, E. M., Michalski, B., Becker, S., & Fahnestock, M. (2017) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01164 · Cited by 144 · see citing works
Hsieh, J., & Eisch, A. J. (2010) · Neurobiology of Disease · doi:10.1016/j.nbd.2010.01.008 · Cited by 144 · see citing works
Running Changes the Brain: the Long and the Short of It
Vivar, C., & van Praag, H. (2017) · Physiology · doi:10.1152/physiol.00017.2017 · Cited by 114 · see citing works
Ontogeny of memory: an update on 40 years of work on infantile amnesia
Madsen, H. B., & Kim, J. H. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.07.030 · Cited by 92 · see citing works
Adult hippocampal neurogenesis and its role in cognition.
Oomen, C. A., Bekinschtein, P., Kent, B. A., Saksida, L. M., & Bussey, T. J. (2014) · WIREs Cognitive Science · doi:10.1002/wcs.1304 · Cited by 93 · see citing works
Lopatina, O. L., Malinovskaya, N. A., Komleva, Y. K., Gorina, Y. V., Shuvaev, A. N., Olovyannikova, R. Y., Belozor, O. S., Belova, O. A., Higashida, H., & Salmina, A. B. (2019) · Reviews in the Neurosciences · doi:10.1515/revneuro-2019-0014 · Cited by 74 · see citing works
Neuropeptides and hippocampal neurogenesis
Zaben, M. J., & Gray, W. P. (2013) · Neuropeptides · doi:10.1016/j.npep.2013.10.002 · Cited by 75 · see citing works
Running reorganizes the circuitry of one-week-old adult-born hippocampal neurons
Sah, N., Peterson, B. D., Lubejko, S. T., Vivar, C., & van Praag, H. (2017) · Scientific Reports · doi:10.1038/s41598-017-11268-z · Cited by 63 · see citing works
The dose makes the poison: From glutamate-mediated neurogenesis to neuronal atrophy and depression
Rubio-Casillas, A., & Fernández-Guasti, A. (2016) · Reviews in the Neurosciences · doi:10.1515/revneuro-2015-0066 · Cited by 49 · see citing works
Human-inspired Perspectives: A Survey on AI Long-term Memory
He, Z., Lin, W., Zheng, H., Zhang, F., Jones, M. W., Aitchison, L., Xu, X., Liu, M., Kristensson, P. O., & Shen, J. (2024) · arXiv · doi:10.48550/arxiv.2411.00489 · Cited by 3 · see citing works
“The dynamic networks method mirrors the way the hippocampus in the human brain stores new memory through the formation of new neurons [86].”
- Authors
- Deisseroth, K., Singla, S., Toda, H., Monje, M., Palmer, T. D., & Malenka, R. C.
- Affiliations
- Stanford Medicine (US)
- Corresponding author
- Deisseroth, Karl
- Malenka, Robert C
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2004-05
- Volume
- 42
- Issue
- 4
- Pages
- 535-552
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2007095775
- Cited by
- 674
- References
- 5
- Citations by year
- 2026: 5 · 2025: 13 · 2024: 13 · 2023: 24 · 2022: 20 · 2021: 27 · 2020: 20 · 2019: 20 · 2018: 26 · 2017: 28 · 2016: 31 · 2015: 32 · 2014: 31 · 2013: 47 · 2012: 42
- FWCI
- 10.54
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 3364 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Stanford Bio-X
- 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 neurogenesis, neural stem/progenitor cells, hippocampus, L-type calcium channels, NMDA receptor, Hes1, Id2, neurogenic differentiation, neuronal differentiation, Hebbian learning, memory storage, activity-dependent gene expression
- MeSH terms
- Transcription Factor HES-1, Animals, Animals, Newborn, Cell Differentiation, Cells, Cultured, DNA-Binding Proteins, Female, Hippocampus, Microtubule-Associated Proteins, Nerve Net, Nerve Tissue Proteins, Synaptic Transmission, Neuronal Plasticity, Neurons, Rats, Inbred F344, Repressor Proteins, Stem Cells, Transcription Factors, Receptors, N-Methyl-D-Aspartate, Rats, Sprague-Dawley, Homeodomain Proteins, Gene Expression Regulation, Developmental, Excitatory Postsynaptic Potentials, Calcium Channels, L-Type, Rats, Basic Helix-Loop-Helix Proteins, Basic Helix-Loop-Helix Transcription Factors, Inhibitor of Differentiation Protein 2
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