Cited by 241Neurogenesis and neuroplasticity mechanismsTreatment of Major DepressionStress Responses and Cortisol

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The neurogenesis hypothesis of affective and anxiety disorders: Are we mistaking the scaffolding for the building?

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Petrik, David, Lagace, Diane C., Eisch, Amelia J.·2012·Neuropharmacology

DOI 10.1016/j.neuropharm.2011.09.003PMC PMC3698048

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Abstract

Hypotheses are scaffoldings erected in front of a building and then dismantled when the building is finished. They are indispensable for the workman; but you mustn't mistake the scaffolding for the building. Johann Wolfgang von Goethe. The neurogenesis hypothesis of affective disorders - in its simplest form - postulates that the generation of neurons in the postnatal hippocampal dentate gyrus is involved in the etiology and treatment efficacy of major depressive disorder (MDD). The hypothesis was established in the 1990s but was built on a broad foundation of earlier research on the hippocampus, serotonin and MDD. It has gone through several growth phases fueled by discoveries both correlative and causative in nature. Recently, the hypothesis has also been broadened to also include potential relevance for anxiety disorders, like post-traumatic stress disorder (PTSD). As any hypothesis should be, it has been tested and challenged, sometimes vigorously. Here we review the current standing of the neurogenesis hypothesis of affective and anxiety disorders, noting in particular how a central postulate - that decreased neurogenesis results in depression or anxiety - has, in general, been rejected. We also review the controversies on whether treatments for these disorders, like antidepressants, rely on intact neurogenesis for their efficacy, and the existence of neurogenesis-dependent and -independent effects of antidepressants. In addition, we review the implications that the hypothesis has for the response to stress, PTSD, and the neurobiology of resilience, and highlight our own work showing that adult-generated neurons are functionally important for the behavioral response to social stress. We conclude by emphasizing how advancements in transgenic mouse technology, rodent behavioral analyses, and our understanding of the neurogenesis process will allow us to refine our conclusions and perform ever more specific experiments. Such scrutiny is critical, since if we "mistake the scaffolding for the building" we could overlook opportunities for translational impact in the clinic. This article is part of a special Issue entitled 'Anxiety and Depression'.

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Hippocampal SPARC regulates depression‐related behavior
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Self-citation
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Steine, I. M., Zayats, T., Stansberg, C. T., Pallesen, S., Mrdalj, J., Håvik, B., Soule, J. D., Haavik, J., Milde, A. M., Skrede, S., et al. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.248 · Cited by 20
Conditional Inhibition of Adult Neurogenesis by Inducible and Targeted Deletion of ERK5 MAP Kinase Is Not Associated with Anxiety/Depression-Like Behaviors
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“The specific role of dentate gyrus neurogenesis in regulating anxiety and negative affect remains unclear [285].”
Background
Doublecortin-Like Is Implicated in Adult Hippocampal Neurogenesis and in Motivational Aspects to Escape from an Aversive Environment in Male Mice
Saaltink, D., van Zwet, E. W., & Vreugdenhil, E. (2020) · eNeuro · doi:10.1523/eneuro.0324-19.2020 · Cited by 14
“associated impaired learning and memory formation (Clelland et al., 2009; Sahay et al., 2011; Fitzsimons et al., 2013; for review, see Samuels and Hen, 2011; Petrik et al., 2012).”
BackgroundInfluential
Depressive behavior induced by unpredictable chronic mild stress increases dentin hypersensitivity in rats
Barbosa, F. M., Cabral, D., Kabadayan, F., Bondan, E. F., Martins, M. D. F. M., Kirsten, T. B., Bonamin, L. V., Queiroz‐Hazarbassanov, N., Bernardi, M. M., & Saraceni, C. H. C. (2017) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2017.04.005 · Cited by 14
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Cerebro-cerebellar functional neuroplasticity mediates the effect of electric field on electroconvulsive therapy outcomes
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“Moreover, the initial hypothesis postulating that the generation of neurons in the postnatal hippocampal dentate gyrus is involved in the etiology and treatment efficacy of major depressive disorders has been also extended for anxiety disorders [34].”
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Podoplanin Gene Disruption in Mice Promotes in vivo Neural Progenitor Cells Proliferation, Selectively Impairs Dentate Gyrus Synaptic Depression and Induces Anxiety-Like Behaviors
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Decreased [3H]naloxone Binding in the Dentate Gyrus of Cloninger Type 1 Anxiety-Prone Alcoholics: A Postmortem Whole-Hemisphere Autoradiography Study.
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Long-term betamethasone 21-phosphate disodium treatment has distinct effects in CD1 and DBA/2 mice on animal behavior accompanied by opposite effects on neurogenesis
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Neurogenic hypothesis and psychiatric disorders
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Predictive signature of static and dynamic functional connectivity for ECT clinical outcomes
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“As one of the most popular ECT mechanisms, the neurogenic hypothesis believes that generating new neurons is beneficial for the depressive brain because of its impairment of producing neurons for mood control (Scott et al., 2000; Petrik et al., 2012).”
Background
Loss of the mu opioid receptor induces strain-specific alterations in hippocampal neurogenesis and spatial learning.
Cominski, T. P., Ansonoff, M., Turchin, C., & Pintar, J. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.07.039 · Cited by 6
“To this end, neurogenesis is unaffected following treatment with tapentadol, a novel analgesic, and methadone (Sankararaman et al., 2012; Meneghini et al., 2014); opiates like these may be better suited for patients displaying opiate-induced cognitive deficits.”
Vangl2, a Core Component of the WNT/PCP Pathway, Regulates Adult Hippocampal Neurogenesis and Age-Related Decline in Cognitive Flexibility
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Zebrafish as a translational model for stress neurobiology: Mechanisms, tools, and advances
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Brief pup separation during lactation confers resilience in behavioural deficits induced by chronic restraint stress in postpartum C57BL/6J dams
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Plasma Metabolomic Signature of Early Abuse in Middle-Aged Women
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“Adult hippocampal neurogenesis has been proposed to be indispensable for the anxiolytic effect of EE [54].”
Depressive Disorders: Prevalence, Costs, and Theories
Grosso, C., Valentão, P., & Andrade, P. B. (2016) · Springer eBooks · doi:10.1007/978-3-319-14021-6_1 · Cited by 3
Therapeutic ultrasound for the treatment of demyelinating diseases
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Diabetes-induced depression: unravelling the role of gut dysbiosis
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The effect of magnesium sulfate on memory and anxiety-like behavior in a rat model: an investigation of its neuronal molecular mechanisms
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Can Adult Neurogenesis Be Considered as Neuroplasticity?
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“The suppression of neurogenesis, in turn, may cause various psychiatric comorbidities such as depression and anxiety disorders (55, 56).”
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Morphological Changes in Hippocampus and Prefrontal Cortex of Confined Sows with Prolonged Pupillary Light Reflex
Fang-lu, L., Xiang, L., Li, J., Shi-quan, C., Liu, H., & Bao, J. (2016) · Journal of Northeast Agricultural University (English edition) · doi:10.1016/s1006-8104(16)30057-5 · Cited by 2
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“It is worth noting that the hippocampus is an important part of the limbic lobe, studies have shown that the signi cant reduction of hippocampal volume is related to depression [24, 25], and the abnormalities of hippocampus are related to depression causality [26].”
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Bumetanide and use in depressive states
Tessier, M., Rezzag, A., Pellegrino, C., & Rivera, C. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-817933-8.00053-0 · Cited by 1
Acute Stress and Anxiety
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Authors: Petrik, D., Lagace, D. C., & Eisch, A. J.
Affiliations: University of Ottawa (CA)
The University of Texas Southwestern Medical Center (US)
Corresponding author: Eisch, Amelia J.
ORCID: Lagace, Diane C.
Eisch, Amelia J.
Venue: Neuropharmacology
Publisher: Elsevier BV
Published: 2012-01
Volume: 62
Issue: 1
Pages: 21-34
ISSN: 0028-3908 (ISSN-L)
DOI: 10.1016/j.neuropharm.2011.09.003
PMC: PMC3698048
OpenAlex: W1988200425
Cited by: 241
References: 204
Citations by year: 2026: 5 · 2025: 4 · 2024: 7 · 2023: 6 · 2022: 8 · 2021: 19 · 2020: 11 · 2019: 13 · 2018: 14 · 2017: 12 · 2016: 29 · 2015: 22 · 2014: 35 · 2013: 29 · 2012: 25
FWCI: 2.52
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuropharmacology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
ORCA Online Research @Cardiff (Cardiff University) (submittedVersion)
Funders: National Institutes of Health (R01 DA016765, K02 DA023555)
NASA (NNX07AP84G)
NSERC (371716)
Topics: Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Health Sciences › Medicine › Pharmacology (medical) › Treatment of Major Depression
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Keywords: adult neurogenesis, dentate gyrus, major depressive disorder, anxiety disorders, post-traumatic stress disorder, antidepressant mechanism, stress response, resilience, social stress, serotonin, transgenic mouse model
MeSH terms: Animals, Anxiety, Hippocampus, Humans, Models, Biological, Anti-Anxiety Agents, Mood Disorders, Neurogenesis

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The neurogenesis hypothesis of affective and anxiety disorders: Are we mistaking the scaffolding for the building?

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