Conditional reduction of adult born doublecortin-positive neurons reversibly impairs selective behaviors
Open accessAbstract
Adult neurogenesis occurs in the adult mammalian subventricular zone (SVZ) along the walls of the lateral ventricles and the subgranular zone (SGZ) of the hippocampal dentate gyrus. While a burgeoning body of research implicates adult neurogenesis in olfactory bulb (OB)- and hippocampal-related behaviors, the precise function continues to elude. To further assess the behavioral importance of adult neurogenesis, we herein generated a novel inducible transgenic mouse model of adult neurogenesis reduction where mice with CreER(T2) under doublecortin (DCX) promoter control were crossed with mice where diphtheria toxin A (DTA) was driven by the Rosa26 promoter. Activation of DTA, through the administration of tamoxifen (TAM), results in a specific reduction of DCX+ immature neurons in both the hippocampal dentate gyrus and OB. We show that the decrease of DCX+ cells causes impaired social discrimination ability in both young adult (from 3 months) and middle aged (from 10 months) mice. Furthermore, these animals showed an age-independent altered coping behavior in the Forced Swim Test without clear changes in anxiety-related behavior. Notably, these behavior changes were reversible on repopulating the neurogenic zones with DCX+ cells on cessation of the TAM treatment, demonstrating the specificity of this effect. Overall, these results support the notion that adult neurogenesis plays a role in social memory and in stress coping but not necessarily in anxiety-related behavior.
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Adult neurogenesis in the hippocampus is necessary for stress-induced social avoidance and social cognition.
“Adult neurogenesis in the hippocampus has been shown to be necessary for stress-induced social avoidance (Lagace et al., 2010), as well as in social cognition (Garrett et al., 2015) (Figure 1C).”
From Adult neurogenesis, glia, and the extracellular matrix (2019) · cites this paper as Garrett et al., 2015
Mice with fewer new neurons were unable to discriminate between novel and previously encountered mice.
“Mice with fewer new neurons were unable to discriminate between novel and previously encountered mice (Garrett et al., 2015).”
From Adult neurogenesis, glia, and the extracellular matrix (2019) · cites this paper as Garrett et al., 2015
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Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation
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“, 2011), pattern separation (Sahay et al., 2011), emotion-related behavior (Revest et al.”
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“At variance with the only other genetic study to date that analyzed adult social recognition memory independent of mating behavior (Sakamoto et al., 2011), our results indicate an involvement of adult neurogenesis in social discrimination ability.”
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“However, OB neurogenesis is necessary for olfactory learning and memory (Breton-Provencher et al., 2009; Arruda-Carvalho et al., 2014; Sakamoto et al., 2014) and mating behavior (Feierstein et al.”
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“Our model is based on the human DCX promoter (shown to drive expression with a similar pattern to mouse endogenous DCX (Couillard-Despres et al., 2006; Zhang et al., 2010).”
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“, 2006) and Nestin (Deng et al., 2009; Singer et al., 2009) with the consequent necessity to develop ever-more complex genetic constructs and elaborate mouse line crossing to increase specificity (Imayoshi et al.”
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MethodA powerful transgenic tool for fate mapping and functional analysis of newly generated neurons
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“We observed previously that a portion of EGFP+ cells (as an index of DCX+ cells) in the DCX CreERT2: CAG-CAT-EGFP mice were incorporating BrdU as proliferation marker (Zhang et al., 2010), but there was no co-localization between the EGFP signal and expression of GFAP (astrocyte marker), CNPase (oligodendrocyte marker…”
BackgroundMethodInfluentialLinking adult olfactory neurogenesis to social behavior
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Is there a role for young hippocampal neurons in adaptation to stress?
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“However, OB neurogenesis is necessary for olfactory learning and memory (Breton-Provencher et al., 2009; Arruda-Carvalho et al., 2014; Sakamoto et al., 2014) and mating behavior (Feierstein et al.”
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“While there were exceptions (Revest et al., 2009; Onksen et al., 2011), the consensus appears to be that without exposing mice with reduced neurogenesis to an additional challenge, there may not be changes in ‘‘baseline’’ levels of anxiety (Petrik et al.”
BackgroundcGMP-dependent protein kinase I, the circadian clock, sleep and learning
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“30 days), tapering off with the appearance of mature neuronal markers largely confined to areas of continuous neurogenesis and rarely outside (Brown et al., 2003; Keays, 2007; von Bohlen und Halbach, 2011).”
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Adult neurogenesis, glia, and the extracellular matrix
Cope, E. C., & Gould, E. (2019) · Cell Stem Cell · doi:10.1016/j.stem.2019.03.023 · Cited by 236 · see citing works
“That is, mice with fewer new neurons seem unable to discriminate between novel and previously encountered mice (Garrett et al., 2015).”
Adult hippocampal neurogenesis and its impairment in Alzheimer’s disease
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“In animals, experimental disruption of neurogenesis impairs social memory and coping with stress (Clelland et al., 2009; Garrett et al., 2015; Alam et al., 2018).”
BackgroundAdult-born neurons boost odor-reward association
Grelat, A., Benoit, L., Wagner, S., Moigneu, C., Lledo, P.-M., & Alonso, M. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1716400115 · Cited by 72 · see citing works
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“The lack of effect on object location memory and anxiety-like behavior with reduced adult neurogenesis is consistent with data from naive mice lacking immature neurons (Garrett et al., 2015; Seo et al., 2015).”
ResultA fin-loop-like structure in GPX4 underlies neuroprotection from ferroptosis
Lorenz, S., Wahida, A., Bostock, M. J., Seibt, T., Mourão, A., Levkina, A., Trümbach, D., Soudy, M., Emler, D., Rothammer, N., et al. (2025) · Cell · doi:10.1016/j.cell.2025.11.014 · Cited by 51 · see citing works
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“ories, is particularly sensitive to neurogenesis levels (Garrett et al., 2015; Monteiro et al., 2014; Pereira-Caixeta et al., 2017).”
BackgroundAbrous, D. N., Koehl, M., & Lemoine, M. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01172-4 · Cited by 45 · see citing works
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“…with a number of previous studies that also showed no effect of neurogenesis ablation on anxiety-related behavior (Shors et al., 2002; Saxe et al., 2006; Schloesser et al., 2010; Garrett et al., 2015), thus supporting the hypothesis that neurogenesis does not regulate emotional behavior directly.”
ResultRivera, P. D., Hanamsagar, R. M., Kan, M. J., Tran, P. K., Stewart, D. A., Jo, Y. C., Gunn, M. D., & Bilbo, S. D. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2018.11.010 · Cited by 39 · see citing works
“These data agree with previously published data that correlate deficits in spatial memory, social memory, and in stress coping with modest reductions of DCX in rodents (Garrett et al. 2015; Lagace et al. 2010; Jessberger et al. 2009).”
ResultSocial behavior, hormones and adult neurogenesis
Opendak, M. M., Briones, B. A., & Gould, E. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2016.02.002 · Cited by 35 · see citing works
“A few studies have pinpointed new neurons in the dentate gyrus as important mediators of social avoidance (Lagace et al., 2010), social recognition (Garrett et al., 2015) and social preference (Opendak et al., 2015), but the extent to which general principles exist about modulation of new neuron…”
Meis1 effects on motor phenotypes and the sensorimotor system in mice
Salminen, A. V., Garrett, L., Schormair, B., Rozman, J., Giesert, F., Niedermeier, K. M., Becker, L., Rathkolb, B., Rácz, I., Klingenspor, M., et al. (2017) · Disease Models & Mechanisms · doi:10.1242/dmm.030080 · Cited by 36 · see citing works
“We have shown previously that decreased social memory can be due to decreased adult neurogenesis in mice (Garrett et al., 2015).”
BackgroundMastrodonato, A., Barbati, S. A., Leone, L., Colussi, C., Gironi, K., Rinaudo, M., Piacentini, R., Denny, C. A., & Grassi, C. (2018) · Scientific Reports · doi:10.1038/s41598-017-18676-1 · Cited by 31 · see citing works
“Moreover, there was no interaction (Group × Time, F(3,36) = 1.”
Disruption of adult olfactory neurogenesis induces deficits in maternal behavior in sheep
Corona, R., Meurisse, M., Cornilleau, F., Moussu, C., Keller, M., & Lévy, F. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.02.043 · Cited by 24 · see citing works
A comprehensive phenotypic characterization of a whole-body Wdr45 knock-out mouse
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“The Social Discrimination test was conducted as described previously (Garrett et al. 2015).”
Crybb2 Mutations Consistently Affect Schizophrenia Endophenotypes in Mice
Heermann, T., Garrett, L., Wurst, W., Fuchs, H., Gailus‐Durner, V., de Angelis, M. H., Graw, J., & Hölter, S. M. (2018) · Molecular Neurobiology · doi:10.1007/s12035-018-1365-5 · Cited by 18 · see citing works
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Fgf9 Y162C Mutation Alters Information Processing and Social Memory in Mice
Garrett, L., Becker, L., Rozman, J., Puk, O., Stoeger, T., Yildirim, A. Ö., Bohla, A., Eickelberg, O., Hans, W., Prehn, C. P., et al. (2017) · Molecular Neurobiology · doi:10.1007/s12035-017-0659-3 · Cited by 11 · see citing works
“We have shown previously the involvement of adult neurogenesis in social recognition memory in the DCXCreER; DTA model where decreased neurogenesis (both olfactory bulb and hippocampal) reversibly impaired social recognition memory [28].”
BackgroundMethodInfluentialRuitenberg, M. J., Wells, J. E., Bartlett, P. F., Harvey, A. R., & Vukovic, J. (2017) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2017.05.013 · Cited by 10 · see citing works
Waters, R. C., Worth, H. M., Vasquez, B., & Gould, E. (2022) · Neurobiology of Stress · doi:10.1016/j.ynstr.2022.100436 · Cited by 8 · see citing works
“, 2020) and others (Monteiro et al., 2014; Garrett et al., 2015) and may reflect changes in social memory or social novelty detection.”
In the pursuit of new social neurons. Neurogenesis and social behavior in mice: A systematic review
García-Gómez, L., Castillo-Fernández, I., & Pérez‐Villalba, A. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.1011657 · Cited by 8 · see citing works
“Instead, when genetic modifications were specifically guided with inducible and reversible genetic models to reduce neurogenesis, social discrimination between a familiar and a new mouse could be correlated with the number of DCX in the DG (Garrett et al., 2015) without altering other behaviors.”
BackgroundGrieco, F., Balla, A., Larrieu, T., & Toni, N. (2025) · EMBO Reports · doi:10.1038/s44319-025-00367-y · Cited by 4 · see citing works
“2G and corresponding legend do not show a neurogenesis difference between Control dominant and submissive mice (there is no posthoc test that would indicate a difference).”
Sinks, M. R., Morrison, D. E., Ramdev, R. A., Lentzou, S., & Spritzer, M. D. (2023) · Neuroscience · doi:10.1016/j.neuroscience.2023.05.018 · Cited by 3 · see citing works
Analysis of Neuropsychiatric Disease‐Related Functional Neuroanatomical Markers in Mice
Garrett, L., Ung, M., Heermann, T., Niedermeier, K. M., & Hölter, S. M. (2018) · Current Protocols in Mouse Biology · doi:10.1002/cpmo.37 · Cited by 3 · see citing works
“9A and B; see Garrett et al., 2015; Garrett, Lie, Hrabé de Angelis, Wurst, & Hölter, 2012 for example analyses), Ki67 (Fig.”
Transcriptional regulation of neonatal neural stem cells is a determinant of social behaviorPreprint
Hiramoto, T., Boku, S., Kang, G., Abe, S., Silva, M. B. E., Tanigaki, K., Nagashima, M., Ye, K. Q., Yamauchi, T., Michurina, T. V., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.11.12.468452 · Cited by 3 · see citing works
Complex Long-term Effects of Radiation on Adult Mouse Behavior
Garrett, L., Ung, M.-C., Einicke, J., Zimprich, A., Fenzl, F. Q., Pawliczek, D., Graw, J., Dalke, C., & Hölter, S. M. (2021) · Radiation Research · doi:10.1667/rade-20-00281.1 · Cited by 2 · see citing works
“Rodents rely heavily on olfaction in social interactions and have a strong olfactory bulb neurogenesis, therefore alterations in social investigation behavior can also indicate altered olfactory capacities (31, 32).”
BackgroundMethodInfluentialNatural variations of adult neurogenesis and anxiety predict hierarchical status of inbred micePreprint
Grieco, F., Balla, A., Larrieu, T., & Toni, N. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.09.21.614232 · Cited by 1 · see citing works
Orechio, D. (2016) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/d.10.2016.tde-29092016-112302
Li, R., Xiong, W., & Sun, C. (2025) · International Journal of Neuroscience · doi:10.1080/00207454.2025.2540989
“AHN is also related to social behavior, affecting social recognition and avoidance [38,39]. early Alzheimer’s symptoms include emotional changes preceding cognitive decline [40]. in summary, AHN promotes cognitive flexibility, memory precision, emotional resilience, and adaptability in the face of…”
Rôle et connectivité des néo-neurones formés à l’âge adulte dans le bulbe olfactif
Grelat, A. (2018) · theses.fr (ABES) · doi:10.70675/c01c4ec0zba51z466aza2f1z09fdd6310b8f
Olfactory learning potentiates long-range cortical GABAergic inputs onto adult-born neuronsPreprint
Peroni, E., Badts, C.-H. D., Lepousez, G., Hiridjee, A., Renvoise, J., Lafosse, I., Wagner, S., Jacquemet, E., Lledo, P., Alonso, M., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.05.29.728424
“…odorant detection (Breton-Provencher et al. , 2016) and discrimination (Enwere et al. , 2004), olfactory innate behaviors (Sakamoto et al. , 2011; Garrett et al. , 2015; Muthusamy et al. , 2017), perceptual learning (Moreno et al. , 2009), olfactory learning (Alonso et al. , 2012; Grelat et al.…”
- Authors
- Garrett, L., Zhang, J., Zimprich, A., Niedermeier, K. M., Fuchs, H., Gailus-Durner, V., Hrabě de Angelis, M., Vogt Weisenhorn, D., Wurst, W., & Hölter, S. M.
- Affiliations
- Helmholtz Munich (DE)
- Max Delbrück Center (DE)
- Corresponding author
- Hölter, Sabine M.
- ORCID
- Venue
- Frontiers in Behavioral Neuroscience
- Publisher
- Frontiers Media SA
- Published
- 2015-11-12
- Volume
- 9
- Pages
- 302-302
- ISSN
- 1662-5153 (ISSN-L)
- PMC
- PMC4642364
- OpenAlex
- W2142710879
- Cited by
- 37
- References
- 49
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 1 · 2023: 2 · 2022: 3 · 2021: 6 · 2020: 2 · 2019: 2 · 2018: 8 · 2017: 4 · 2016: 5
- FWCI
- 2.30
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Behavioral Neuroscience (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (acceptedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- mediaTUM (Technical University of Munich) (submittedVersion, cc-by)
- Site cant be reached (submittedVersion, cc-by)
- DZNE Pub (submittedVersion, cc-by)
- PuSH - Publication Server of Helmholtz Zentrum München (submittedVersion)
- Funders
- Bundesministerium für Bildung und Forschung (EO 0901, 01EO0901)
- Bayerisches Staatsministerium für Bildung und Kultus, Wissenschaft und Kunst
- Deutschen Schwindel- und Gleichgewichtszentrum (01 EO 0901, EO 0901)
- 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, doublecortin, subventricular zone, dentate gyrus, olfactory bulb, social discrimination, social memory, stress coping, anxiety
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