Amphetamine disrupts dopamine axon growth in adolescence by a sex-specific mechanism in mice
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Abstract
Initiating drug use during adolescence increases the risk of developing addiction or other psychopathologies later in life, with long-term outcomes varying according to sex and exact timing of use. The cellular and molecular underpinnings explaining this differential sensitivity to detrimental drug effects remain unexplained. The Netrin-1/DCC guidance cue system segregates cortical and limbic dopamine pathways in adolescence. Here we show that amphetamine, by dysregulating Netrin-1/DCC signaling, triggers ectopic growth of mesolimbic dopamine axons to the prefrontal cortex, only in early-adolescent male mice, underlying a male-specific vulnerability to enduring cognitive deficits. In adolescent females, compensatory changes in Netrin-1 protect against the deleterious consequences of amphetamine on dopamine connectivity and cognitive outcomes. Netrin-1/DCC signaling functions as a molecular switch which can be differentially regulated by the same drug experience as function of an individual’s sex and adolescent age, and lead to divergent long-term outcomes associated with vulnerable or resilient phenotypes.
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Amphetamine exposure in early adolescence has opposite sex-dependent outcomes as exposure in mid-adolescence.
“In the case of amphetamine exposure in adolescence, for example, exposure in early adolescence had opposite sex-dependent outcomes as exposure in mid-adolescence [51].”
From Adolescent nicotine exposure and persistent neurocircuitry changes: unveiling lifelong psychiatric risks (2025) · cites this paper as [51]
The Discussion reports an age-dependent reversal in which sex shows reduced Dcc expression after amphetamine: males in early adolescence and females in mid-adolescence. But it does not report opposite enduring outcomes: females exposed at either age were protected from the dopamine-innervation and cognitive deficits observed in early-exposed males. The claim is supported for the molecular response, not for long-term outcomes. (LLM, conf=0.86)
Experimental — accuracy not yet measuredStriking, age-dependent differences can be reported in the enduring effects of the same experience on neural circuitry depending on the adolescent period in which this experience occurred.
“striking, age-dependent differences can be reported in the enduring effects of the same experience on neural circuitry depending on the adolescent period in which this experience occurred [48–51].”
From Adolescent nicotine exposure and persistent neurocircuitry changes: unveiling lifelong psychiatric risks (2025) · cites this paper as [51]
Amphetamine in adolescence misroutes a subset of dopamine axons to the PFC in an age- and sex-dependent manner, leading to pathological ectopic innervation associated with cognitive deficits.
“For example, amphetamine in adolescence misroutes a subset of dopamine axons to the PFC in an age- and sex-dependent manner, leading to a pathological ectopic innervation associated with cognitive deficits [51].”
From Adolescent nicotine exposure and persistent neurocircuitry changes: unveiling lifelong psychiatric risks (2025) · cites this paper as [51]
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Self-citationGrant, A., Hoops, D., Labelle‐Dumais, C., Prévost, M., Rajabi, H., Kolb, B. E., Stewart, J., Arvanitogiannis, A., & Flores, C. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05888.x · Cited by 65 · see citing works
Self-citationThe Netrin-1/DCC Guidance Cue Pathway as a Molecular Target in Depression: Translational Evidence
Torres‐Berrío, A., Hernández, G., Nestler, E. J., & Flores, C. (2020) · Biological Psychiatry · doi:10.1016/j.biopsych.2020.04.025 · Cited by 64 · see citing works
Self-citationVerney, C. (1999) · Microscopy Research and Technique · doi:10.1002/(sici)1097-0029(19990701)46:1 · Cited by 62 · see citing works
Reynolds, L. M., Makowski, C., Yogendran, S., Kießling, S., Cermakian, N., & Flores, C. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.287 · Cited by 60 · see citing works
Self-citationSoto, P. L., Wilcox, K. M., Zhou, Y., Ator, N. A., Riddle, M. A., Wong, D. F., & Weed, M. R. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.119 · Cited by 57 · see citing works
Watt, M. J., Roberts, C. L., Scholl, J. L., Meyer, D. L., Miiller, L. C., Barr, J. L., Novick, A. M., Renner, K. J., & Forster, G. L. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3353-9 · Cited by 56 · see citing works
What’s bugging your teen?—The microbiota and adolescent mental health
McVey Neufeld, K.-A., Luczynski, P., Seira Oriach, C., Dinan, T. G., & Cryan, J. F. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.06.005 · Cited by 56 · see citing works
Culture of Postnatal Mesencephalic Dopamine Neurons on an Astrocyte Monolayer
Fasano, C., Thibault, D., & Trudeau, L. (2008) · Current Protocols in Neuroscience · doi:10.1002/0471142301.ns0321s44 · Cited by 53 · see citing works
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Vassilev, P., Pantoja-Urbán, A. H., Giroux, M., Nouel, D., Hernández, G., Orsini, T., & Flores, C. (2021) · eNeuro · doi:10.1523/eneuro.0045-21.2021 · Cited by 48 · see citing works
Self-citationAdolescent social defeat alters markers of adult dopaminergic function
Novick, A. M., Forster, G. L., Tejani‐Butt, S. M., & Watt, M. J. (2011) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2011.06.009 · Cited by 47 · see citing works
Yan, R., Wang, T., & Zhou, Q. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1901902116 · Cited by 43 · see citing works
Cuesta, S., Restrepo-Lozano, J. M., Popescu, C., He, S., Reynolds, L. M., Israel, S. A., Hernández, G., Rais, R., Slusher, B. S., & Flores, C. (2019) · Addiction Biology · doi:10.1111/adb.12791 · Cited by 38 · see citing works
Self-citationDopamine Axon Targeting in the Nucleus Accumbens in Adolescence Requires Netrin-1
Cuesta, S., Nouel, D., Reynolds, L. M., Morgunova, A., Torres‐Berrío, A., White, A., Hernández, G., Cooper, H. M., & Flores, C. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00487 · Cited by 38 · see citing works
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Synaptic Protein Degradation Controls Sexually Dimorphic Circuits through Regulation of DCC/UNC-40
Salzberg, Y., Pechuk, V., Gat, A., Setty, H., Sela, S., & Oren‐Suissa, M. (2020) · Current Biology · doi:10.1016/j.cub.2020.08.002 · Cited by 33 · see citing works
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Cuesta, S., Restrepo-Lozano, J. M., Silvestrin, S., Nouel, D., Torres‐Berrío, A., Reynolds, L. M., Arvanitogiannis, A., & Flores, C. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.284 · Cited by 31 · see citing works
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Self-citationExposure to Bullying and General Psychopathology: A Prospective, Longitudinal Study
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Adolescence: a time of transition for the phenotype of dcc heterozygous mice
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Adolescent dopamine development
Reynolds, L. M., & Flores, C. (2021) · Diagnosis, Management and Modeling of Neurodevelopmental Disorders · doi:10.1016/b978-0-12-817988-8.00026-9 · Cited by 10 · see citing works
Self-citationQuantifying Dopaminergic Innervation in Rodents Using Unbiased Stereology
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Self-citation
Flagged first, then by citations
Research works printed but not linked: 1
- [110]Paxinos, G. & Franklin, K. B. J. The mouse brain in stereotaxic coordinates (Academic Press, 2008).
Cited by
Sorted by citations
Reynolds, L. M., Faure, P., & Barik, J. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-03110-0 · Cited by 26 · see citing works
Self-citationReynolds, L. M., Gulmez, A., Fayad, S. L., Campos, R. C., Rigoni, D., Nguyen, C., Le Borgne, T., Topilko, T., Rajot, D., Franco, C., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-53327-w · Cited by 10 · see citing works
Self-citationThe scheduling of adolescence with Netrin-1 and UNC5C
Hoops, D., Kyne, R., Salameh, S., MacGowan, D., Avramescu, R. G., Ewing, E., He, A. T., Orsini, T., Durand, A., Popescu, C., et al. (2024) · eLife · doi:10.7554/elife.88261 · Cited by 8 · see citing works
Self-citation
- Authors
- Reynolds, L. M., Hernandez, G., MacGowan, D., Popescu, C., Nouel, D., Cuesta, S., Burke, S., Savell, K. E., Zhao, J., Restrepo-Lozano, J. M., Giroux, M., Israel, S., Orsini, T., He, S., Wodzinski, M., Avramescu, R. G., Pokinko, M., Epelbaum, J. G., Niu, Z., Pantoja-Urbán, A. H., Trudeau, L.-É., Kolb, B., Day, J. J., & Flores, C.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Douglas Mental Health University Institute (CA)
- Rutgers, The State University of New Jersey (US)
- Université de Montréal (CA)
- University of Alabama at Birmingham (US)
- University of Lethbridge (CA)
- Corresponding author
- Flores, Cecilia
- ORCID
- Venue
- Nature Communications
- Published
- 2023-07-07
- Volume
- 14
- Issue
- 1
- Pages
- 4035-4035
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC10329029
- OpenAlex
- W4383499952
- Cited by
- 30
- References
- 121
- Citations by year
- 2026: 2 · 2025: 10 · 2024: 13 · 2023: 5
- FWCI
- 3.63
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Nature Communications (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- U.S. Department of Health & Human Services | NIH | National Institute on Drug Abuse (R01DA037911, F31DA041188)
- Gouvernement du Canada | Natural Sciences and Engineering Research Council of Canada (RGPIN-2020-04703)
- Gouvernement du Canada | Canadian Institutes of Health Research (156272)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- amphetamine, adolescence, sex differences, netrin-1, DCC receptor, axon guidance, mesolimbic dopamine system, prefrontal cortex, cognitive impairment, drug vulnerability, adolescent age
- MeSH terms
- Netrin-1, DCC Receptor, Amphetamine, Animals, Axons, Dopamine, Female, Male, Mice
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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