Hippocampal Neurogenesis Regulates Forgetting During Adulthood and Infancy
Abstract
Forget It!: When examining the relationship between the production of new neurons in the hippocampus and memory, studies have generally first manipulated hippocampal neurogenesis and afterward investigated memory formation and found that new neurons help to encode new memories. However, when investigating how similar manipulations of neurogenesis impact established hippocampus-dependent memories, Akers et al. (p. 598 ; see the Perspective by Mongiat and Schinder ) uncovered a role for neurogenesis in memory clearance. Thus, the continuous addition of new neurons both degrades existing information stored in hippocampal circuits and simultaneously provides substrates for new learning.
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Such alterations promote an increased participation of these cells during learning and memory tasks and a reconfiguration of DG-CA3 circuits that degrade stored memories.
“Consequently, such alterations promote an increased participation of these cells during learning and memory tasks35 and a reconfiguration of DG-CA3 circuits that degrade stored memories.36”
From Adult hippocampal neuroplasticity triggers susceptibility to recurrent depression (2017) · cites this paper as [36]
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Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus
van Praag, H., Kempermann, G., & Gage, F. H. (1999) · Nature Neuroscience · doi:10.1038/6368 · Cited by 3,880 · see citing works
Kuhn, H., Dickinson-Anson, H., & Gage, F. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-06-02027.1996 · Cited by 3,139 · see citing works
Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus
Malberg, J. E., Eisch, A. J., Nestler, E. J., & Duman, R. S. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-24-09104.2000 · Cited by 3,111 · see citing works
Mechanisms and Functional Implications of Adult Neurogenesis
Zhao, C., Deng, W., & Gage, F. H. (2008) · Cell · doi:10.1016/j.cell.2008.01.033 · Cited by 3,007 · see citing works
Modality-Specific Retrograde Amnesia of Fear
Kim, J. J., & Fanselow, M. S. (1992) · Science · doi:10.1126/science.1585183 · Cited by 2,483 · see citing works
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
ADULT NEUROGENESIS IN THE MAMMALIAN CENTRAL NERVOUS SYSTEM
Ming, G., & Song, H. (2005) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.28.051804.101459 · Cited by 1,829 · see citing works
Optogenetic stimulation of a hippocampal engram activates fear memory recall
Liu, X., Ramirez, S., Pang, P. T., Puryear, C. B., Govindarajan, A., Deisseroth, K. A., & Tonegawa, S. (2012) · Nature · doi:10.1038/nature11028 · Cited by 1,669 · see citing works
Microglia Shape Adult Hippocampal Neurogenesis through Apoptosis-Coupled Phagocytosis
Sierra, A., Encinas, J. M., Deudero, J. J. P., Chancey, J. H., Enikolopov, G., Overstreet-Wadiche, L. S., Tsirka, S. E., & Maletic-Savatic, M. (2010) · Cell Stem Cell · doi:10.1016/j.stem.2010.08.014 · Cited by 1,622 · see citing works
Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation
Sahay, A., Scobie, K. N., Hill, A. S., O'Carroll, C. M., Kheirbek, M. A., Burghardt, N. S., Fenton, A. A., Dranovsky, A., & Hen, R. (2011) · Nature · doi:10.1038/nature09817 · Cited by 1,567 · see citing works
Eichenbaum (2004) · doi:10.1016/j.neuron.2004.08.028 · Cited by 1,464 · see citing works
The efficiency of systematic sampling in stereology—reconsidered
GUNDERSEN, H. J. G., JENSEN, E. B. V., KIÊU, K., & NIELSEN, J. (1999) · Journal of Microscopy · doi:10.1046/j.1365-2818.1999.00457.x · Cited by 1,317 · see citing works
Computational analysis of the role of the hippocampus in memory
Treves, A., & Rolls, E. T. (1994) · Hippocampus · doi:10.1002/hipo.450040319 · Cited by 1,272 · see citing works
GABA regulates synaptic integration of newly generated neurons in the adult brain
Ge, S., Goh, E. L. K., Sailor, K. A., Kitabatake, Y., Ming, G., & Song, H. (2005) · Nature · doi:10.1038/nature04404 · Cited by 1,261 · see citing works
Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus
Zhao, C., Teng, E. M., Summers, R. G., Ming, G.-L., & Gage, F. H. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.3648-05.2006 · Cited by 1,257 · see citing works
Marino, S., Vooijs, M., van der Gulden, H., Jonkers, J., & Berns, A. (2000) · Genes & Development · doi:10.1101/gad.14.8.994 · Cited by 920 · see citing works
Localization of a Stable Neural Correlate of Associative Memory
Reijmers, L. G. J. E., Perkins, B. L., Matsuo, N., & Mayford, M. R. (2007) · Science · doi:10.1126/science.1143839 · Cited by 853 · see citing works
Zambrowicz, B., Imamoto, A., Fiering, S., Herzenberg, L. A., Kerr, W. G., & Soriano, P. M. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.8.3789 · Cited by 850 · see citing works
Making memories last: the synaptic tagging and capture hypothesis
Redondo, R. L., & Morris, R. G. M. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn2963 · Cited by 792 · see citing works
GABAergic Cells Are the Major Postsynaptic Targets of Mossy Fibers in the Rat Hippocampus
Acsády, L., Kamondi, A., Sı́k, A., Freund, T., & Buzsáki, G. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-09-03386.1998 · Cited by 741 · see citing works
Neurons born in the adult dentate gyrus form functional synapses with target cells
Toni, N., Laplagne, D. A., Zhao, C., Lombardi, G., Ribak, C. E., Gage, F. H., & Schinder, A. F. (2008) · Nature Neuroscience · doi:10.1038/nn.2156 · Cited by 741 · see citing works
Excitation-Neurogenesis Coupling in Adult Neural Stem/Progenitor Cells
Deisseroth, K., Singla, S., Toda, H., Monje, M., Palmer, T. D., & Malenka, R. C. (2004) · Neuron · doi:10.1016/s0896-6273(04)00266-1 · Cited by 674 · see citing works
Short‐term and long‐term survival of new neurons in the rat dentate gyrus
Dayer, A. G., Ford, A. A., Cleaver, K. M., Yassaee, M., & Cameron, H. A. (2003) · Journal of Comparative Neurology · doi:10.1002/cne.10675 · Cited by 628 · see citing works
Amaral, D. G., & Dent, J. A. (1981) · The Journal of Comparative Neurology · doi:10.1002/cne.901950106 · Cited by 606 · see citing works
Exercise and the brain: something to chew on
van Praag, H. (2009) · Trends in Neurosciences · doi:10.1016/j.tins.2008.12.007 · Cited by 599 · see citing works
Adult-Generated Hippocampal Neurons Allow the Flexible Use of Spatially Precise Learning Strategies
Garthe, A., Behr, J., & Kempermann, G. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005464 · Cited by 597 · see citing works
Synapse formation on neurons born in the adult hippocampus
Toni, N., Teng, E. M., Bushong, E. A., Aimone, J. B., Zhao, C., Consiglio, A., van Praag, H., Martone, M. E., Ellisman, M. H., & Gage, F. H. (2007) · Nature Neuroscience · doi:10.1038/nn1908 · Cited by 579 · see citing works
Optical controlling reveals time-dependent roles for adult-born dentate granule cells
Gu, Y., Arruda-Carvalho, M., Wang, J., Janoschka, S., Josselyn, S. A., Frankland, P. W., & Ge, S. (2012) · Nature Neuroscience · doi:10.1038/nn.3260 · Cited by 423 · see citing works
Self-citationp53 suppresses the self-renewal of adult neural stem cells
Meletis, K., Wirta, V., Hede, S., Nistér, M., Lundeberg, J., & Frisén, J. (2005) · Development · doi:10.1242/dev.02208 · Cited by 414 · see citing works
The ghosts of brain states past: Remembering reactivates the brain regions engaged during encoding.
Danker, J. F., & Anderson, J. R. (2010) · Psychological Bulletin · doi:10.1037/a0017937 · Cited by 400 · see citing works
The multifarious hippocampal mossy fiber pathway: a review
Henze, D. A., Urban, N. N., & Barrionuevo, G. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00146-9 · Cited by 389 · see citing works
Age-related production of new granule cells in the adult dentate gyrus
Seki, T., & Arai, Y. (1995) · Neuroreport · doi:10.1097/00001756-199512150-00010 · Cited by 386 · see citing works
Stimulation of entorhinal cortex promotes adult neurogenesis and facilitates spatial memory
Stone, S. S. D., Teixeira, C. M., DeVito, L. M., Zaslavsky, K., Josselyn, S. A., Lozano, A. M., & Frankland, P. W. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3100-11.2011 · Cited by 384 · see citing works
Self-citationFear erasure in mice requires synergy between antidepressant drugs and extinction training
Karpova, N. N., Pickenhagen, A., Lindholm, J., Tiraboschi, E., Kulesskaya, N., Ágústsdóttir, A., Antila, H., Popova, D., Akamine, Y., Sullivan, R., et al. (2011) · Science · doi:10.1126/science.1214592 · Cited by 382 · see citing works
Functional Convergence of Neurons Generated in the Developing and Adult Hippocampus
Laplagne, D. A., Esposito, M. S., Piatti, V. C., Morgenstern, N. A., Zhao, C., van Praag, H., Gage, F. H., & Schinder, A. F. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040409 · Cited by 359 · see citing works
Memory retention – the synaptic stability versus plasticity dilemma
Abraham, W. C., & Robins, A. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2004.12.003 · Cited by 353 · see citing works
Campbell, B. A., & Spear, N. E. (1972) · Psychological Review · doi:10.1037/h0032690 · Cited by 351 · see citing works
Discovery of a Proneurogenic, Neuroprotective Chemical
Pieper, A. A., Xie, S., Capota, E., Estill, S. J., Zhong, J., Long, J. M., Becker, G. L., Huntington, P. J., Goldman, S. E., Shen, C.-H., et al. (2010) · Cell · doi:10.1016/j.cell.2010.06.018 · Cited by 350 · see citing works
Hippocampal neurogenesis and forgetting
Frankland, P. W., Köhler, S., & Josselyn, S. A. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.05.002 · Cited by 261 · see citing works
Self-citationThe distribution of early childhood memories
Rubin, D. C. (2000) · Memory · doi:10.1080/096582100406810 · Cited by 220 · see citing works
Niibori, Y., Yu, T., Epp, J. R., Akers, K. G., Josselyn, S. A., & Frankland, P. W. (2012) · Nature Communications · doi:10.1038/ncomms2261 · Cited by 195 · see citing works
Self-citationYu, T., Zhang, G., Liebl, D. J., & Kernie, S. G. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.4629-08.2008 · Cited by 180 · see citing works
Genetic influence on phenotypic differentiation in adult hippocampal neurogenesis
Kempermann, G., & Gage, F. H. (2002) · Developmental Brain Research · doi:10.1016/s0165-3806(01)00224-3 · Cited by 177 · see citing works
Infantile amnesia: A neurogenic hypothesisPreprint
Josselyn, S. A., & Frankland, P. W. (2012) · Learning & Memory · doi:10.1101/lm.021311.110 · Cited by 149 · see citing works
Self-citationInducible repression of CREB function disrupts amygdala-dependent memory
Josselyn, S. A. (2004) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.05.008 · Cited by 136 · see citing works
Self-citationA role for circuit homeostasis in adult neurogenesis
Meltzer, L. A., Yabaluri, R., & Deisseroth, K. A. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.09.007 · Cited by 124 · see citing works
Multiple Forms of Activity-Dependent Competition Refine Hippocampal Circuits In Vivo
Yasuda, M., Johnson‐Venkatesh, E., Zhang, H., Parent, J. M., Sutton, M. A., & Umemori, H. (2011) · Neuron · doi:10.1016/j.neuron.2011.04.027 · Cited by 100 · see citing works
Design-based estimation of neuronal number and individual neuronal volume in the rat hippocampus
Sharifabad, M. H., & Nyengaard, J. R. (2007) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2007.01.009 · Cited by 90 · see citing works
Ontogeny of contextual fear memory formation, specificity, and persistence in micePreprint
Akers, K. G., Arruda-Carvalho, M., Josselyn, S. A., & Frankland, P. W. (2012) · Learning & Memory · doi:10.1101/lm.027581.112 · Cited by 88 · see citing works
Self-citationMaekawa, M., Namba, T., Suzuki, E., Yuasa, S., Kohsaka, S., & Uchino, S. (2009) · Neuroscience Research · doi:10.1016/j.neures.2008.12.006 · Cited by 85 · see citing works
Weisz, V. I., & Argibay, P. F. (2012) · Cognition · doi:10.1016/j.cognition.2012.07.002 · Cited by 73 · see citing works
Postnatal neurogenesis in the dentate gyrus of the guinea pig
Guidi, S., Ciani, E., Severi, S., Contestabile, A., & Bartesaghi, R. (2004) · Hippocampus · doi:10.1002/hipo.20050 · Cited by 58 · see citing works
Ohira, K., & Miyakawa, T. (2011) · Molecular Brain · doi:10.1186/1756-6606-4-10 · Cited by 53 · see citing works
Self-citationImpact of early adverse experience on complexity of adult-generated neurons
Leslie, A. T., Akers, K. G., Krakowski, A. D., Stone, S. S. D., Sakaguchi, M., Arruda-Carvalho, M., & Frankland, P. W. (2011) · Translational Psychiatry · doi:10.1038/tp.2011.38 · Cited by 30 · see citing works
Self-citationRichards, B. A., & Frankland, P. W. (2013) · Hippocampus · doi:10.1002/hipo.22089 · Cited by 26 · see citing works
Self-citationChildhood and concealing memories.
Freud, S. (2004) · doi:10.1037/10012-004 · Cited by 20 · see citing works
McGonigal, R., Tabatadze, N., & Routtenberg, A. (2011) · Hippocampus · doi:10.1002/hipo.20998 · Cited by 17 · see citing works
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Salter, M. W., & Stevens, B. (2017) · Nature Medicine · doi:10.1038/nm.4397 · Cited by 1,767 · see citing works
Adult Neurogenesis in the Hippocampus: From Stem Cells to Behavior
Gonçalves, J. T., Schafer, S. T., & Gage, F. H. (2016) · Cell · doi:10.1016/j.cell.2016.10.021 · Cited by 1,122 · see citing works
Adult hippocampal neurogenesis and cognitive flexibility — linking memory and mood
Anacker, C., & Hen, R. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2017.45 · Cited by 1,014 · see citing works
Adult Mammalian Neural Stem Cells and Neurogenesis: Five Decades Later
Bond, A. M., Ming, G.-L., & Song, H. (2015) · Cell Stem Cell · doi:10.1016/j.stem.2015.09.003 · Cited by 791 · 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
Microglia mediate forgetting via complement-dependent synaptic elimination
Wang, C., Yue, H., Hu, Z., Shen, Y., Ma, J., Li, J., Wang, X.-D., Wang, L., Sun, B., Shi, P., et al. (2020) · Science · doi:10.1126/science.aaz2288 · Cited by 629 · see citing works
Microglia regulation of synaptic plasticity and learning and memory
Zhou, M., Cornell, J., Salinas, S., & Huang, H.-Y. (2022) · Neural Regeneration Research · doi:10.4103/1673-5374.322423 · Cited by 548 · see citing works
The role of engram cells in the systems consolidation of memory
Tonegawa, S., Morrissey, M. D., & 北村, 貴. (2018) · Nature reviews. Neuroscience · doi:10.1038/s41583-018-0031-2 · Cited by 454 · see citing works
Mitochondria as central regulators of neural stem cell fate and cognitive function
Khacho, M., Harris, R., & Slack, R. S. (2018) · Nature reviews. Neuroscience · doi:10.1038/s41583-018-0091-3 · Cited by 396 · see citing works
He, X.-F., Liu, D.-X., Zhang, Q., Liang, F.-Y., Dai, G.-Y., Zeng, J.-S., Pei, Z., Xu, G.-Q., & Lan, Y. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00144 · Cited by 371 · see citing works
“The 12 C57BL/6J mice in each group performed the water-maze task, according to the protocol of van Praag et al. (1999) and Akers et al. (2014).”
MethodSex differences in hippocampal cognition and neurogenesis
Yagi, S., & Galea, L. A. M. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0208-4 · Cited by 340 · see citing works
The slow forgetting of emotional episodic memories: An emotional binding account
Yonelinas, A., & Ritchey, M. (2015) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2015.02.009 · Cited by 313 · see citing works
The Biology of Forgetting—A Perspective
Davis, R. L., & Zhong, Y. (2017) · Neuron · doi:10.1016/j.neuron.2017.05.039 · Cited by 324 · see citing works
Knierim, J. J., & Neunuebel, J. P. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.10.008 · Cited by 305 · see citing works
The Persistence and Transience of Memory
Richards, B. A., & Frankland, P. W. (2017) · Neuron · doi:10.1016/j.neuron.2017.04.037 · Cited by 304 · see citing works
Self-citationKol, A., Adamsky, A., Groysman, M., Kreisel, T., London, M., & Goshen, I. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0679-6 · Cited by 283 · see citing works
Naninck, E. F. G., Hoeijmakers, L., Kakava-Georgiadou, N., Meesters, A., Lazic, S. E., Lucassen, P. J., & Kőrösi, A. (2014) · Hippocampus · doi:10.1002/hipo.22374 · Cited by 281 · see citing works
Hippocampal neurogenesis: Learning to remember
Lazarov, O., & Hollands, C. (2016) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.12.006 · Cited by 281 · see citing works
Formation and integration of new neurons in the adult hippocampus
Denoth‐Lippuner, A., & Jessberger, S. (2021) · Nature reviews. Neuroscience · doi:10.1038/s41583-021-00433-z · Cited by 274 · see citing works
Evidences for Adult Hippocampal Neurogenesis in Humans
Moreno-Jiménez, E. P., Terreros-Roncal, J., Flor-García, M., Rábano, A., & Llorens-Martín, M. (2021) · The Journal of Neuroscience · doi:10.1523/jneurosci.0675-20.2020 · Cited by 272 · see citing works
Human adult neurogenesis across the ages: An immunohistochemical study
Dennis, C. V., Suh, L. S., Rodriguez, M. L., Kril, J. J., & Sutherland, G. T. (2016) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12337 · Cited by 265 · see citing works
Hippocampal neurogenesis and forgetting
Frankland, P. W., Köhler, S., & Josselyn, S. A. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.05.002 · Cited by 261 · see citing works
Self-citationReview: adult neurogenesis contributes to hippocampal plasticity
Toda, T., & Gage, F. H. (2017) · Cell and Tissue Research · doi:10.1007/s00441-017-2735-4 · Cited by 262 · see citing works
Astrocyte activation and reactive gliosis—A new target in stroke?
Pekny, M., Wilhelmsson, U., Tatlisumak, T., & Pekna, M. (2018) · Neuroscience Letters · doi:10.1016/j.neulet.2018.07.021 · Cited by 231 · see citing works
Neurogenesis-mediated forgetting minimizes proactive interference
Epp, J. R., Mera, R. S., Köhler, S., Josselyn, S. A., & Frankland, P. W. (2016) · Nature Communications · doi:10.1038/ncomms10838 · Cited by 229 · see citing works
Self-citationAdult Hippocampal Neurogenesis, Fear Generalization, and Stress
Besnard, A., & Sahay, A. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.167 · Cited by 226 · see citing works
Mice in an enriched environment learn more flexibly because of adult hippocampal neurogenesis
Garthe, A., Roeder, I., & Kempermann, G. (2015) · Hippocampus · doi:10.1002/hipo.22520 · Cited by 223 · see citing works
REST and neural gene network dysregulation in iPSC models of Alzheimer’s disease
Meyer, K., Feldman, H. M., Lu, T., Drake, D., Lim, E. T., Ling, K.-H., Bishop, N. A., Pan, Y., Seo, J., Lin, Y.-T., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.01.023 · Cited by 216 · see citing works
Gage, F. H. (2019) · Science · doi:10.1126/science.aav6885 · Cited by 216 · see citing works
O’Leary, O. F., & Cryan, J. F. (2014) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2014.09.011 · Cited by 212 · see citing works
Infantile Amnesia: A Critical Period of Learning to Learn and Remember
Alberini, C. M., & Travaglia, A. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0324-17.2017 · Cited by 209 · see citing works
Remote Memory and the Hippocampus: A Constructive Critique
Barry, D. N., & Maguire, E. A. (2018) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2018.11.005 · Cited by 196 · see citing works
Sex hormones and adult hippocampal neurogenesis: Regulation, implications, and potential mechanisms
Mahmoud, R., Wainwright, S. R., & Galea, L. A. M. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2016.03.002 · Cited by 201 · see citing works
Adult neurogenesis: a substrate for experience-dependent change
Opendak, M., & Gould, E. (2015) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2015.01.001 · Cited by 200 · see citing works
Duarte-Guterman, P., Yagi, S., Chow, C., & Galea, L. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.05.024 · Cited by 194 · see citing works
Exercise augmentation of exposure therapy for PTSD: rationale and pilot efficacy data
Powers, M. B., Medina, J. L., Burns, S., Kauffman, B. Y., Monfils, M., Asmundson, G. J. G., Diamond, A., McIntyre, C., & Smits, J. A. J. (2015) · Cognitive Behaviour Therapy · doi:10.1080/16506073.2015.1012740 · Cited by 194 · see citing works
Sex Hormones and Cognition: Neuroendocrine Influences on Memory and Learning
Hamson, D. K., Roes, M., & Galea, L. A. M. (2016) · Comprehensive physiology · doi:10.1002/cphy.c150031 · Cited by 205 · 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
Self-citationRecalibrating the Relevance of Adult Neurogenesis
Snyder, J. S. (2019) · Trends in Neurosciences · doi:10.1016/j.tins.2018.12.001 · Cited by 183 · see citing works
Kida, S. (2018) · Psychopharmacology · doi:10.1007/s00213-018-5086-2 · Cited by 183 · see citing works
Neuroinflammation and neurogenesis in Alzheimer's disease and potential therapeutic approaches
Sung, P.-S., Lin, P.-Y., Liu, C.-H., Su, H.-C., & Tsai, K.-J. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21030701 · Cited by 193 · see citing works
Modulating Neuronal Competition Dynamics in the Dentate Gyrus to Rejuvenate Aging Memory Circuits
McAvoy, K. M., Scobie, K. N., Berger, S. M., Russo, C., Guo, N., Decharatanachart, P., Vega-Ramirez, H., Miake-Lye, S., Whalen, M. J., Nelson, M., et al. (2016) · Neuron · doi:10.1016/j.neuron.2016.08.009 · Cited by 175 · see citing works
An expanded particle swarm optimization based on multi-exemplar and forgetting ability
Xia, X., Gui, L., He, G., Wei, B., Zhang, Y., Yu, F., Wu, H., & Zhan, Z. (2019) · Information Sciences · doi:10.1016/j.ins.2019.08.065 · Cited by 175 · see citing works
Klune, C. B., Jin, B., & DeNardo, L. A. (2021) · eLife · doi:10.7554/elife.64567 · Cited by 171 · see citing works
Stress and adolescent hippocampal neurogenesis: diet and exercise as cognitive modulators
Hueston, C. M., Cryan, J. F., & Nolan, Y. M. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.48 · Cited by 171 · see citing works
Involvement of Adult Hippocampal Neurogenesis in Learning and Forgetting
Yau, S., Li, A., & So, K. (2015) · Neural Plasticity · doi:10.1155/2015/717958 · Cited by 165 · see citing works
Adult hippocampal neurogenesis in Alzheimer’s disease: A roadmap to clinical relevance
Salta, E., Lazarov, O., Fitzsimons, C. P., Tanzi, R. E., Lucassen, P. J., & Choi, S. H. (2023) · Cell stem cell · doi:10.1016/j.stem.2023.01.002 · Cited by 165 · see citing works
Adult Hippocampal Neurogenesis: Regulation and Possible Functional and Clinical Correlates
Baptista, P., & Andrade, J. P. (2018) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2018.00044 · Cited by 162 · see citing works
On the Run for Hippocampal PlasticityPreprint
Cooper, C. P., Moon, H. Y., & van Praag, H. (2017) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a029736 · Cited by 160 · see citing works
Infantile amnesia reflects a developmental critical period for hippocampal learning
Travaglia, A., Bisaz, R., Sweet, E. S., Blitzer, R. D., & Alberini, C. M. (2016) · Nature Neuroscience · doi:10.1038/nn.4348 · Cited by 160 · see citing works
Blood-to-brain communication in aging and rejuvenation
Bieri, G., Schroer, A. B., & Villeda, S. A. (2023) · Nature Neuroscience · doi:10.1038/s41593-022-01238-8 · Cited by 156 · see citing works
Recovery of “Lost” Infant Memories in Mice
Guskjolen, A. J., Kenney, J. W., de la Parra, J., Yeung, B.-R. A., Josselyn, S. A., & Frankland, P. W. (2018) · Current Biology · doi:10.1016/j.cub.2018.05.059 · Cited by 160 · see citing works
Self-citationA complementary processes account of the development of childhood amnesia and a personal past.
Bauer, P. (2015) · Psychology Review · doi:10.1037/a0038939 · Cited by 134 · see citing works
Functions of adult-born neurons in hippocampal memory interference and indexing
Miller, S. M., & Sahay, A. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0484-2 · Cited by 146 · 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
Born this way: Hippocampal neurogenesis across the lifespan
Kozareva, D. A., Cryan, J. F., & Nolan, Y. M. (2019) · Aging Cell · doi:10.1111/acel.13007 · Cited by 146 · see citing works
Kumar, D., Koyanagi, I., Carrier‐Ruiz, A., Vergara, P., Srinivasan, S., Sugaya, Y., Kasuya, M., Yu, T., Vogt, K. E., Muratani, M., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.05.008 · Cited by 144 · see citing works
Brain size and limits to adult neurogenesis
Paredes, M. F., Sorrells, S. F., García‐Verdugo, J. M., & Álvarez-Buylla, A. (2015) · The Journal of Comparative Neurology · doi:10.1002/cne.23896 · Cited by 142 · see citing works
Engram neurons: Encoding, consolidation, retrieval, and forgetting of memory
Guskjolen, A. J., & Cembrowski, M. S. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02137-5 · Cited by 148 · see citing works
Self-citationNeural Progenitor Cell Terminology
Martínez‐Cerdeño, V., & Noctor, S. C. (2018) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2018.00104 · Cited by 141 · see citing works
Assessments of dentate gyrus function: discoveries and debates
Borzello, M., Ramirez, S., Treves, A., Lee, I., Scharfman, H. E., Stark, C. E. L., Knierim, J. J., & Rangel, L. M. (2023) · Nature reviews. Neuroscience · doi:10.1038/s41583-023-00710-z · Cited by 138 · see citing works
Cognitive Function and the Microbiome
Gareau, M. G. (2016) · International review of neurobiology · doi:10.1016/bs.irn.2016.08.001 · Cited by 131 · see citing works
The long and short term effects of motherhood on the brain
Duarte‐Guterman, P., Leuner, B., & Galea, L. A. M. (2019) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.02.004 · Cited by 127 · see citing works
Adult Neurogenesis and the Future of the Rejuvenating Brain Circuits
Lepousez, G., Nissant, A., & Lledo, P. (2015) · Neuron · doi:10.1016/j.neuron.2015.01.002 · Cited by 129 · see citing works
Re-evaluating the link between neuropsychiatric disorders and dysregulated adult neurogenesis
Yun, S., Reynolds, R. P., Masiulis, I., & Eisch, A. J. (2016) · Nature Medicine · doi:10.1038/nm.4218 · Cited by 127 · see citing works
Abolition of aberrant neurogenesis ameliorates cognitive impairment after stroke in mice
Cuartero, M. I., de la Parra, J., Pérez-Ruiz, A., Bravo-Ferrer, I., Durán-Laforet, V., García-Culebras, A., García-Segura, J. M., Dhaliwal, J., Frankland, P. W., Lizasoain, I., et al. (2019) · Journal of Clinical Investigation · doi:10.1172/jci120412 · Cited by 128 · see citing works
Self-citationNuninga, J. O., Mandl, R. C. W., Boks, M. P., Bakker, S. C., Somers, M., Heringa, S. M., Nieuwdorp, W., Hoogduin, H. M., Kahn, R. S., Luijten, P. R., et al. (2019) · Molecular Psychiatry · doi:10.1038/s41380-019-0392-6 · Cited by 126 · see citing works
Mechanisms of Hippocampal Aging and the Potential for Rejuvenation
Fan, X., Wheatley, E., & Villeda, S. (2017) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-072116-031357 · Cited by 124 · see citing works
Adusumilli, V. S., Walker, T. L., Overall, R. W., Klatt, G. M., Zeidan, S. A., Zocher, S., Kirova, D. G., Ntitsias, K., Fischer, T. J., Sykes, A. M., et al. (2020) · Cell stem cell · doi:10.1016/j.stem.2020.10.019 · Cited by 119 · see citing works
Surget, A., & Belzung, C. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01136-8 · Cited by 122 · see citing works
Cognition in the Chronic Pain Experience: Preclinical Insights
Phelps, C. E., Navratilova, E., & Porreca, F. (2021) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2021.01.001 · Cited by 120 · see citing works
Wilkins, H., Harris, J. L., Carl, S. M., Lezi, E., Lu, J., Selfridge, J. E., Roy, N., Hutfles, L. J., Koppel, S. J., Morris, J. K., et al. (2014) · Human Molecular Genetics · doi:10.1093/hmg/ddu371 · Cited by 116 · see citing works
Adult neurogenesis: bridging the gap between mice and humans
Jessberger, S., & Gage, F. H. (2014) · Trends in Cell Biology · doi:10.1016/j.tcb.2014.07.003 · Cited by 116 · see citing works
Hippocampal activation of Rac1 regulates the forgetting of object recognition memory
Liu, Y., Du, S., Lv, L., Lei, B., Shi, W., Tang, Y., Wang, L., & Zhong, Y. (2016) · Current Biology · doi:10.1016/j.cub.2016.06.056 · Cited by 114 · see citing works
Ishikawa, R., Fukushima, H., Frankland, P. W., & Kida, S. (2016) · eLife · doi:10.7554/elife.17464 · Cited by 112 · see citing works
Self-citationThe development of spatial and memory circuits in the rat
Tan, H. M., Wills, T. J., & Cacucci, F. (2017) · WIREs Cognitive Science · doi:10.1002/wcs.1424 · Cited by 113 · see citing works
Tello-Ramos, M. C., Branch, C. L., Kozlovsky, D. Y., Pitera, A. M., & Витальевич, П. В. (2018) · Animal Behaviour · doi:10.1016/j.anbehav.2018.02.019 · Cited by 111 · see citing works
Scribble Scaffolds a Signalosome for Active Forgetting
Cervantes-Sandoval, I., Chakraborty, M., MacMullen, C., & Davis, R. L. (2016) · Neuron · doi:10.1016/j.neuron.2016.05.010 · Cited by 100 · see citing works
RNA-binding proteins balance brain function in health and disease
Schieweck, R., Ninkovic, J., & Kiebler, M. A. (2020) · Physiological Reviews · doi:10.1152/physrev.00047.2019 · Cited by 104 · see citing works
Adult hippocampal neurogenesis and its impairment in Alzheimer’s disease
Kim, T. A., Syty, M. D., Wu, K., & Ge, S. (2022) · 动物学研究 · doi:10.24272/j.issn.2095-8137.2021.479 · Cited by 114 · see citing works
The Nuclear Receptor REV-ERBα Regulates Fabp7 and Modulates Adult Hippocampal Neurogenesis
Schnell, A., Chappuis, S., Schmutz, I., Brai, E., Ripperger, J. A., Schaad, O., Welzl, H., Descombes, P., Alberi, L. A., & Albrecht, U. (2014) · PLoS ONE · doi:10.1371/journal.pone.0099883 · Cited by 104 · see citing works
Szulc, K. U., Timmons, B. W., Bouffet, É., Laughlin, S., de Medeiros, C. B., Skocic, J., Lerch, J. P., & Mabbott, D. (2018) · NeuroImage Clinical · doi:10.1016/j.nicl.2018.02.021 · Cited by 99 · see citing works
Hippocampal adult neurogenesis: Does the immune system matter?
de Miranda, A. S., Zhang, C., Katsumoto, A., & Teixeira, A. L. (2016) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2016.10.052 · Cited by 100 · see citing works
Rewiring the connectome: Evidence and effects
Bennett, S. H., Kirby, A. J., & Finnerty, G. T. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.03.001 · Cited by 104 · see citing works
Characterization of the role of adult neurogenesis in touch‐screen discrimination learning
Swan, A. A., Clutton, J. E., Chary, P. K., Cook, S. G., Liu, G. G., & Drew, M. R. (2014) · Hippocampus · doi:10.1002/hipo.22337 · Cited by 101 · see citing works
Castilla‐Ortega, E., Serrano, A., Blanco, E., Araos, P. F., Suárez, J., Pavón, F. J., de Fonseca, F. R., & Santín, L. J. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.03.030 · Cited by 100 · see citing works
Gengatharan, A., Malvaut, S., Marymonchyk, A., Ghareghani, M., Snapyan, M., Fischer-Sternjak, J., Ninkovic, J., Götz, M., & Saghatelyan, A. (2021) · Cell · doi:10.1016/j.cell.2020.12.026 · Cited by 97 · see citing works
Neurogenesis in the Normal Ageing Hippocampus: A Mini-Review
Seib, D. R., & Martín-Villalba, A. (2014) · Gerontology · doi:10.1159/000368575 · Cited by 96 · see citing works
Johnston, S. T., Shtrahman, M., Parylak, S., Gonçalves, J. T., & Gage, F. H. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.10.013 · Cited by 98 · see citing works
Sekeres, M. J., Bradley-Garcia, M., Martínez-Canabal, A., & Winocur, G. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222312697 · Cited by 99 · see citing works
Adult-born neurons modify excitatory synaptic transmission to existing neurons
Adlaf, E. W., Vaden, R. J., Niver, A. J., Manuel, A. F., Onyilo, V. C., Araujo, M. T., Dieni, C. V., Vo, H. T., King, G. D., Wadiche, J. I., et al. (2017) · eLife · doi:10.7554/elife.19886 · Cited by 93 · see citing works
Gao, A., Xia, F., Guskjolen, A. J., Ramsaran, A. I., Santoro, A., Josselyn, S. A., & Frankland, P. W. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.3126-17.2018 · Cited by 91 · see citing works
Self-citationAdult neurogenesis, human after all (again): Classic, optimized, and future approaches
Lucassen, P. J., Fitzsimons, C. P., Salta, E., & Maletić‐Savatić, M. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112458 · Cited by 93 · see citing works
Novel Galectin-3 Roles in Neurogenesis, Inflammation and Neurological Diseases
Soares, L. C., Al‐Dalahmah, O., Hillis, J. M., Young, C. C., Asbed, I., Sakaguchi, M., O’Neill, E. E., & Szele, F. G. (2021) · Cells · doi:10.3390/cells10113047 · Cited by 94 · see citing works
Transformation of cortical and hippocampal neural circuit by environmental enrichment
Hirase, H., & Shinohara, Y. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.09.031 · Cited by 91 · 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
Dumitru, I., Neitz, A., Alfonso, J., & Monyer, H. (2017) · Neuron · doi:10.1016/j.neuron.2017.03.003 · Cited by 88 · see citing works
AAV ablates neurogenesis in the adult murine hippocampus
Johnston, S., Parylak, S. L., Kim, S., Mac, N., Lim, C., Gallina, I., Bloyd, C., Newberry, A., Saavedra, C. D., Novak, O., et al. (2021) · eLife · doi:10.7554/elife.59291 · Cited by 87 · see citing works
Radial glial cells in the adult dentate gyrus: what are they and where do they come from?
Berg, D. A., Bond, A. M., Ming, G.-L., & Song, H. (2018) · F1000Research · doi:10.12688/f1000research.12684.1 · Cited by 89 · see citing works
- Authors
- 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., Ohira, K., Richards, B. A., Miyakawa, T., Josselyn, S. A., & Frankland, P. W.
- Affiliations
- Hospital for Sick Children (CA)
- Program in Neurosciences and Mental Health, The Hospital for Sick Children, Toronto, M5G 1X8, Canada.
- University of Toronto (CA)
- Fujita Health University (JP)
- Corresponding author
- Akers, Katherine G.
- Restivo, Leonardo
- Josselyn, Sheena A.
- Frankland, Paul W.
- ORCID
- Venue
- Science
- Published
- 2014-05-09
- Volume
- 344
- Issue
- 6184
- Pages
- 598-602
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2130169724
- Cited by
- 761
- References
- 57
- Citations by year
- 2026: 34 · 2025: 71 · 2024: 47 · 2023: 50 · 2022: 49 · 2021: 68 · 2020: 72 · 2019: 81 · 2018: 66 · 2017: 56 · 2016: 75 · 2015: 57 · 2014: 33 · 2013: 1
- FWCI
- 25.59
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Canadian Institutes of Health Research (MOP74650, MOP- 86762)
- Japan Society for the Promotion of Science (25116526, 25242078)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- hippocampal neurogenesis, forgetting, infantile amnesia, dentate gyrus, memory consolidation, adult neurogenesis, guinea pig, degu, computational model of memory
- MeSH terms
- Amnesia, Animals, Female, Guinea Pigs, Hippocampus, Male, Memory, Mice, Inbred C57BL, Neurons, Dentate Gyrus, Mice, Neurogenesis
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