The neurogenesis hypothesis of affective and anxiety disorders: Are we mistaking the scaffolding for the building?
Open accessAbstract
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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A few studies provide evidence that absence of neurogenesis elicits depressive-like symptoms in rodents, but most studies find that absent neurogenesis is not sufficient to induce a depressive phenotype, although it is required in mice for the behavioral effects of antidepressants.
“A few studies provide evidence that the absence of neurogenesis elicits depressive like symptoms in rodents123, 124, but most studies find that absent neurogenesis is not sufficient to induce a depressive phenotype125 although it is required in mice for the behavioral effects of antidepressants118, 126.”
From Dysregulation of adult hippocampal neuroplasticity in major depression: Pathogenesis and therapeutic implications (2022) · cites this paper as [124]
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The Role of Neural Plasticity in Depression: From Hippocampus to Prefrontal Cortex
Liu, W., Ge, T., Leng, Y., Pan, Z., Fan, J., Yang, W., & Cui, R. (2017) · Neural Plasticity · doi:10.1155/2017/6871089 · Cited by 640 · see citing works
“The neurogenic hypothesis of depression emphasizes the theory that impaired adult hippocampal neurogenesis results in depression, and newborn neurons in the adult brain are critical to mood regulation and antidepressant efficacy [27, 28].”
BackgroundRegulation 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
The neurobiology of depression and antidepressant action
Willner, P., Scheel-Krüger, J., & Belzung, C. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.12.007 · Cited by 519 · see citing works
“Hippocampal neurogenesis is powerfully suppressed by stress r by prolonged corticosterone exposure (Wong and Herbert, 2004; ineur et al., 2007; Samuels and Hen, 2011; Hanson et al., 2011; etrik et al., 2012).”
BackgroundDepression and Hippocampal Neurogenesis: A Road to Remission?
Eisch, A. J., & Petrik, D. (2012) · Science · doi:10.1126/science.1222941 · Cited by 516 · see citing works
Self-citationNeural Mechanisms of Stress Resilience and Vulnerability
Franklin, T. B., Saab, B. J., & Mansuy, I. M. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.016 · Cited by 500 · see citing works
“However, it can also sometimes increase anxiety after stress but have no effect on depression or even have no effect at all (Petrik et al., 2012; Revest et al., 2009; Saxe et al., 2006; Shors et al., 2002).”
Tartt, A. N., Mariani, M. B., Hen, R., Mann, J. J., & Boldrini, M. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01520-y · Cited by 408 · see citing works
“A few studies provide evidence that the absence of neurogenesis elicits depressive like symptoms in rodents [122, 123], but most studies find that absent neurogenesis is not sufficient to induce a depressive phenotype [124] although it is required in mice for the behavioral effects of antidepressants [117, 125].”
BackgroundThe current state of the neurogenic theory of depression and anxiety
Miller, B. R., & Hen, R. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.08.012 · Cited by 386 · see citing works
Epigenetic mechanisms in neurogenesis
Yao, B., Christian, K. M., He, C., Jin, P., Ming, G., & Song, H. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.70 · Cited by 391 · see citing works
Neuroplastic changes in depression: A role for the immune system
Eyre, H., & Baune, B. T. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.03.019 · Cited by 319 · see citing works
“…and hypometabolism of the frontal cortical regions; and decreased growth and development of neurons (reduce spine density, hence dendritic retraction) (Piser, 2010; Fournier and Duman, 2011; Hanson et al., 2011; Petrik et al., 2011; Drevets, 2003, 2007; Mayberg, 2003; Drevets et al., 2008).”
InfluentialChronic peripheral inflammation, hippocampal neurogenesis, and behavior
Chesnokova, V., Pechnick, R. N., & Wawrowsky, K. (2016) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2016.01.017 · Cited by 299 · see citing works
“Some studies found that altered or decreased neurogenesis is associated with depression-like behavior (Wang et al., 2015), but others have not found this relationship (Petrik et al., 2012).”
BackgroundDu Preez, A., Onorato, D., Eiben, I., Musaelyan, K., Egeland, M., Zunszain, P. A., Fernandes, C., Thuret, S., & Pariante, C. M. (2021) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2020.07.015 · Cited by 285 · see citing works
Savitz, J., Drevets, W. C., Smith, C. M., Victor, T. A., Wurfel, B. E., Bellgowan, P. S., Bodurka, J., Teague, T. K., & Dantzer, R. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2014.194 · Cited by 272 · see citing works
Orchestrating transcriptional control of adult neurogenesisPreprint
Hsieh, J. (2012) · Genes & Development · doi:10.1101/gad.187336.112 · Cited by 208 · see citing works
“Adult hippocampal neurogenesis contributes to learning and memory and may also be involved in neuropsychiatric disorders (Noonan et al. 2010; Aimone et al. 2011; Sahay et al. 2011; Snyder et al. 2011; Petrik et al. 2012).”
BackgroundTanti, A., & Belzung, C. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.08.017 · Cited by 220 · see citing works
Hippocampal structural and functional changes associated with electroconvulsive therapy response
Abbott, C., Jones, T. R., Lemke, N. T., Gallegos, P., McClintock, S. M., Mayer, A. R., Bustillo, J., & Calhoun, V. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.124 · Cited by 207 · see citing works
Molecular mechanisms in the regulation of adult neurogenesis during stress
Egeland, M., Zunszain, P. A., & Pariante, C. M. (2015) · Nature Reviews Neuroscience · doi:10.1038/nrn3855 · Cited by 203 · see citing works
From the stressed adolescent to the anxious and depressed adult: Investigations in rodent models
McCormick, C. M., & Green, M. R. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.08.063 · Cited by 180 · see citing works
“The role of neurogenesis in anxiety and depressive disorders is a promising avenue of research, but far from understood (see reviews by Samuels and Hen (2011) and Petrik et al. (2012)).”
<scp>BDNF</scp> isoforms: a round trip ticket between neurogenesis and serotonin?
Foltran, R. B., & Diaz, S. L. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13658 · Cited by 187 · see citing works
“A recent and exhaustive revision covering diverse behavioral tests classically used to evaluate a depressive-like phenotype in rodents, clearly demonstrates that solely decreasing neurogenesis is not enough to induce a depressive-like state (Petrik et al. 2012).”
Birey, F., Kloc, M. L., Chavali, M., Hussein, I., Wilson, M., Christoffel, D. J., Chen, T., Frohman, M. A., Robinson, J. K., Russo, S. J., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.10.046 · Cited by 204 · see citing works
Mah, L., Szabuniewicz, C., & Fiocco, A. J. (2015) · Current Opinion in Psychiatry · doi:10.1097/yco.0000000000000223 · Cited by 206 · see citing works
Depression: from psychopathology to pathophysiology.
Belzung, C., Willner, P., & Philippot, P. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.08.013 · Cited by 171 · see citing works
Lipopolysaccharide-induced sepsis induces long-lasting affective changes in the mouse
Anderson, S. T., Commins, S., Moynagh, P. N., & Coogan, A. N. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2014.07.007 · Cited by 169 · see citing works
“Neurogenesis is strongly implicated in the pathology of affective disorders, although the experimental interruption of neurogenesis in the rodent hippocampus is not by itself always sufficient to produce increased anxiety-like and depressive-like symptoms, with stress appearing to play an important role (Petrik et al.…”
Tendolkar, I., van Beek, M., van Oostrom, I., Mulder, M., Janzing, J., Voshaar, R. O., & van Eijndhoven, P. V. (2013) · Psychiatry Research · doi:10.1016/j.pscychresns.2013.09.004 · Cited by 163 · see citing works
Walker, A. K., Rivera, P. D., Wang, Q., Chuang, J.-C., Tran, S., Osborne-Lawrence, S., Estill, S. J., Starwalt, R., Huntington, P., Morlock, L., et al. (2015) · Molecular Psychiatry · doi:10.1038/mp.2014.34 · Cited by 161 · see citing works
Self-citationFunctional Dissociation of Adult-Born Neurons Along the Dorsoventral Axis of the Dentate Gyrus
Wu, M. V., & Hen, R. (2014) · Hippocampus · doi:10.1002/hipo.22265 · Cited by 156 · see citing works
“Taken together, these results support a model where adult-born hippocampal neurons function not so much as behavioral master regulators, but instead as modulators of the local underlying network under conditions of high demand (Piatti et al., 2013).”
ResultMoylan, S., Eyre, H. A., Maes, M., Baune, B. T., Jacka, F. N., & Berk, M. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.02.003 · Cited by 155 · see citing works
Dias, G. P., Cavegn, N., Nix, A., do Nascimento Bevilaqua, M. C., Stangl, D., Zainuddin, M. S. A., Nardi, A. E., Gardino, P. F., & Thuret, S. (2012) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2012/541971 · Cited by 153 · see citing works
“Several of these pathways also act to upregulate neurogenesis both directly and indirectly, which is a further way in which curcumin may exert its antidepressant-like effects as some antidepressant drugs have been shown to exert neurogenesis-dependent behavioural effects [30, 109, 110].”
BackgroundGABAergic Control of Depression-Related Brain States
Luscher, B., & Fuchs, T. (2015) · Advances in Pharmacology · doi:10.1016/bs.apha.2014.11.003 · Cited by 149 · see citing works
GABAA receptor-acting neurosteroids: a role in the development and regulation of the stress response
Gunn, B. G., Cunningham, L., Mitchell, S. G., Swinny, J. D., Lambert, J. J., & Belelli, D. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.06.001 · Cited by 149 · see citing works
“Moreover, there is a general consensus that ablation of hippocampal neurogenesis is not sufficient to induce a depressive or anxiety-like behaviour in rodents (reviewed in Petrik et al., 2012).”
Major Depression: One Brain, One Disease, One Set of Intertwined Processes
Filatova, E. V., Shadrina, M. I., & Slominsky, P. A. (2021) · Cells · doi:10.3390/cells10061283 · Cited by 167 · 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
The Dynamic Brain: Neuroplasticity and Mental Health
Kays, J. L., Hurley, R. A., & Taber, K. H. (2012) · The Journal of Neuropsychiatry and Clinical Neurosciences · doi:10.1176/appi.neuropsych.12050109 · Cited by 128 · 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
Self-citationSaaltink, D.-J., & Vreugdenhil, E. (2014) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1568-5 · Cited by 127 · 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
“…yet the precise mechanism and function of hippocampal neurogenesis in antidepressant‐mediated mood regulation remain to be elucidated with many controversies arising from different species and methods used by different laboratories (for reviews, see Petrik et al., 2012; Zhao et al., 2008; Table 1).”
BackgroundMethodMediators of allostasis and systemic toxicity in bipolar disorder.
Grande, I., Magalhães, P., Kunz, M., Vieta, E., & Kapczinski, F. (2012) · Physiology and Behavior · doi:10.1016/j.physbeh.2011.10.029 · Cited by 121 · see citing works
“Although this whole vicious cycle is yet to be demonstrated in people with mood disorders and other factors are probably at play [44,45], the dynamic inter-regulation of stress levels, neurogenesis and systemic changes”
Stimulation of entorhinal cortex-dentate gyrus circuitry is antidepressive
Yun, S., Reynolds, R. P., Petrof, I., White, A., Rivera, P. D., Segev, A., Gibson, A. D., Suarez, M., DeSalle, M. J., Ito, N., et al. (2018) · Nature Medicine · doi:10.1038/s41591-018-0002-1 · Cited by 120 · see citing works
“Multiple lines of evidence implicate DG adult neurogenesis in antidepressant efficacy, particularly under stressful conditions 22–25 .”
Self-citationSavitz, J. B., Dantzer, R., Wurfel, B. E., Victor, T. A., Ford, B. N., Bodurka, J., Bellgowan, P. S. F., Teague, T. K., & Drevets, W. C. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.11.015 · Cited by 131 · see citing works
Mechanisms of antidepressant resistance
El-Hage, W., Leman, S., Camus, V., & Belzung, C. (2013) · Frontiers in Pharmacology · doi:10.3389/fphar.2013.00146 · Cited by 111 · see citing works
“…(adult neurogenesis) has been shown to be compromised in rodent models of MDD; this effect is prevented by administration of monoaminergic AD drugs (see Hanson et al., 2011; Eisch and Petrik, 2012; Petrik et al., 2012; Bambico and Belzung, 2013; Tanti and Belzung, 2013a,b for recent reviews).”
BackgroundTanti, A., Westphal, W.-P., Girault, V., Brizard, B., Devers, S., Leguisquet, A.-M., Surget, A., & Belzung, C. (2013) · Hippocampus · doi:10.1002/hipo.22134 · Cited by 106 · see citing works
“While there is still much debate regarding the implication of neurogenesis in stress- related and mood disorders (Petrik et al., 2012), suppression of neurogenesis has been shown to impair hippocampal functions underlain by both septal and temporal divisions of the hippocampus, such as spatial…”
BackgroundInfluentialmiR-17-92 cluster regulates adult hippocampal neurogenesis, anxiety and depression
Jin, J., Kim, S.-N., Liu, X., Zhang, H., Zhang, C., Seo, J.-S., Kim, Y., & Sun, T. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.06.101 · Cited by 103 · see citing works
GABA suppresses neurogenesis in the adult hippocampus through GABAB receptors
Giachino, C., Barz, M., Tchorz, J. S., Tomé, M., Gassmann, M., Bischofberger, J., Bettler, B., & Taylor, V. (2013) · Development · doi:10.1242/dev.102608 · Cited by 114 · see citing works
“Given that antidepressant drugs can promote adult neurogenesis and new hippocampal neurons have been implicated in mediating some effects of antidepressants (Petrik et al., 2012), our findings are relevant for human disease.”
ResultA possible negative influence of depression on the ability to overcome memory interference
Shelton, D. J., & Kirwan, C. B. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.08.016 · Cited by 101 · see citing works
Adult hippocampal neurogenesis in the pathogenesis of addiction and dual diagnosis disorders
Chambers, R. A. (2012) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2012.12.005 · Cited by 107 · see citing works
“Although low levels of neurogenesis do not guarantee the presence of, or by any means represent the sole cause of a given mental illness, neurogenesis seems helpful to behavioral adaptation (Petrik et al., 2012).”
BackgroundLong-lasting effects of chronic rTMS to treat chronic rodent model of depression.
Feng, S.-F., Shi, T.-R., Fan-Yang, Wang, W.-N., Chen, Y.-C., & Tan, Q.-R. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.04.019 · Cited by 100 · see citing works
Egeland, M., Guinaudie, C., Du Preez, A., Musaelyan, K., Zunszain, P. A., Fernandes, C., Pariante, C. M., & Thuret, S. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.68 · Cited by 98 · see citing works
Kohl, Z., Abdallah, N. B. B., Vogelgsang, J., Tischer, L., Deusser, J., Amato, D., Anderson, S., Müller, C., Riess, O., Masliah, E., et al. (2015) · Neurobiology of Disease · doi:10.1016/j.nbd.2015.10.021 · Cited by 89 · see citing works
Sun, M.-Y., Yetman, M. J., Lee, T.-C., Chen, Y., & Jankowsky, J. L. (2014) · The Journal of comparative neurology · doi:10.1002/cne.23497 · Cited by 88 · see citing works
“…the unique restriction sites Mlu1, Fse1, and AsiS1 for later linearization of the targeting vector. pROSA26PA containing the CAG-loxP-stop-loxPGluCla-GluClb-eYFP-WPRE insert was linearized with MluI, purified, and electroporated into agouti C57BL/ 6N JM8 embryonic stem cells (Pettitt et al., 2009).”
MethodLussier, A. L., Lebedeva, K., Fenton, E. Y., Guskjolen, A., Caruncho, H., & Kalynchuk, L. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.04.012 · Cited by 88 · see citing works
“, 2004), decreased cell proliferation and survival in animal models of stress and depression (Petrik et al., 2012), and increased cell proliferation and survival after antidepressant treatment (Santarelli et al.”
Influence of Physical Exercise on Traumatic Brain Injury Deficits: Scaffolding Effect
Archer, T. (2011) · Neurotoxicity Research · doi:10.1007/s12640-011-9297-0 · Cited by 90 · see citing works
“It is important to distinguish between what constitutes scaffolding and what constitutes the building itself (Petrik et al. 2012), whereas exercise regimes have been shown to induce neurogenesis, neurorepair, and damage control that buttress the brain against neurodegenerative processes it is the molecular, cellular,…”
BackgroundNeurogenesis in neurological and psychiatric diseases and brain injury: From bench to bedside
Ruan, L., Lau, B. W.-M., Wang, J., Huang, L., Zhuge, Q., Wang, B. Z., Jin, K., & So, K. (2014) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2013.12.006 · Cited by 85 · see citing works
“the two behavioral phenotypes in animal studies (Petrik et al., 2012).”
BackgroundGender Differences in the Neurobiology of Anxiety: Focus on Adult Hippocampal Neurogenesis
Marques, A. A., Bevilaqua, M. C. D. N., da Fonseca, A. M. P., Nardi, A. E., Thuret, S., & Dias, G. P. (2016) · Neural Plasticity · doi:10.1155/2016/5026713 · Cited by 78 · see citing works
“In addition, recent studies have attributed to AHN a regulatory role in various cognitive processes such as memory [42, 62], learning [61, 63, 64], besides a significant influence on affective disorders [65], anxiety [12], and emotional behavior [66].”
BackgroundLajud, N., & Torner, L. (2015) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2015.00003 · Cited by 76 · see citing works
“However, the correlation of long term behavioral changes with hippocampal neurogenesis changes is still controversial due to several observations that neurogenesis and emotionality are independently regulated (Petrik et al., 2012).”
Wu, J., Chen, H., Li, H., Tang, Y., Yang, L., Cao, S.-S., & Qin, D.-L. (2016) · Molecules · doi:10.3390/molecules21030260 · Cited by 76 · see citing works
“Whereas CGA (1 nM) prevents Cort-induced cell damage of raphe neurons by stimulating new axon and dendrite growth (Figure 1F), suggesting the pharmacological effect of CGA on protection of Cort-induced neuron damage is likely to be associated with neurogenesis, which has been proved to be an important factor for antid…”
BackgroundOdaira, T., Nakagawasai, O., Takahashi, K., Nemoto, W., Sakuma, W., Lin, J.-R., & Tan–No, K. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.03.026 · Cited by 80 · see citing works
“Newly generated neurons are incorporated into the hippocampal circuitry and contribute to hippocampal functions, including mood and memory (Petrik et al., 2012).”
Saraulli, D., Costanzi, M., Mastrorilli, V., & Vecchioli, S. F. (2017) · Current Neuropharmacology · doi:10.2174/1570159x14666160412150223 · Cited by 96 · see citing works
Tanti, A., & Belzung, C. (2013) · Cell and Tissue Research · doi:10.1007/s00441-013-1612-z · Cited by 71 · see citing works
“…on this subject extensively, as such reviews have recently been published (Bambico and Belzung 2012; David et al. 2010; Hanson et al. 2011b; Petrik et al. 2012; Tanti and Belzung 2010a) but rather to try to provide a frame enabling us to understand the way that these new hippocampal…”
BackgroundThe role of inflammatory cytokines on the aetiopathogenesis of depression
Makhija, K., & Karunakaran, S. (2013) · Australian & New Zealand Journal of Psychiatry · doi:10.1177/0004867413488220 · Cited by 76 · see citing works
“The hippocampus is involved in learning/memory context-dependent emotional responses (Fanselow, 2000), and mood control (Petrik et al., 2012).”
BackgroundTGF-β/Smad Signalling in Neurogenesis: Implications for Neuropsychiatric Diseases
Hiew, L.-F., Poon, C.-H., You, H.-Z., & Lim, L.-W. (2021) · Cells · doi:10.3390/cells10061382 · Cited by 71 · see citing works
Varela-Nallar, L., Rojas-Ábalos, M., Abbott, A. C., Moya, E., Iturriaga, R., & Inestrosa, N. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00017 · Cited by 71 · see citing works
“The possibility to activate endogenous NSCs and stimulate the generation of new neurons in the adult brain could have therapeutic potential in pathological conditions in which neurogenesis is altered, such as mood disorders, schizophrenia and neurodegenerative diseases (Kaneko and Sawamoto, 2009; Winner et al., 2011;…”
Wang, H.-N., Wang, L., Zhang, R.-G., Chen, Y.-C., Liu, L., Gao, F., Nie, H., Hou, W.-G., Peng, Z., & Tan, Q.-R. (2014) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2014.01.004 · Cited by 70 · see citing works
“The hippocampus is one of the several limbic structures that have been extensively studied in individuals with depression (Petrik et al., 2012), it has been shown undergoing morphological changes in response to stress, including atrophy and loss of CA3 pyramidal neurons (Kim et al., 2007; Yang et…”
Felice, D. F., O'Leary, O., Pizzo, R., & Cryan, J. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.06.066 · Cited by 70 · see citing works
Additive gene-environment effects on hippocampal structure in healthy humans
Rabl, U., Meyer, B. M., Diers, K., Bartova, L., Berger, A., Mandorfer, D., Popovic, A., Scharinger, C., Huemer, J., Kalcher, K., et al. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.3113-13.2014 · Cited by 68 · see citing works
“In line with their effects on the stress system and brain function, these variants have repeatedly been shown to directly affect hippocampal volume (Pezawas et al., 2004; Frodl et al., 2008; Honea et al., 2009), although others failed to show these effects (Dutt et al., 2009; Cole et al., 2011;…”
BackgroundLiang, G., Kow, A. S. F., Yusof, R., Tham, C. L., Ho, Y.-C., & Lee, M. T. (2024) · Biomedicines · doi:10.3390/biomedicines12010184 · Cited by 68 · see citing works
“These results illustrated that neurogenesis plays a vital role in depression and can impact behavioral output and the efficacy of antidepressant therapy, which was also the simplest form of the neurogenesis hypothesis [119].”
BackgroundFunctional and mechanistic exploration of an adult neurogenesis‐promoting small molecule
Petřík, D., Jiang, Y., Birnbaum, S. G., Powell, C. M., Kim, M., Hsieh, J., & Eisch, A. J. (2012) · The FASEB Journal · doi:10.1096/fj.11-201426 · Cited by 68 · see citing works
“Adult-generated hippocampal granule cell (GC) neurons incorporate into hippocampal circuitry (3, 4) and are implicated in many hippocampal functions, including learning and memory (5) and mood control (6).”
BackgroundSelf-citationRief, W., Barsky, A. J., Bingel, U., Doering, B. K., Schwarting, R., Wöhr, M., & Schweiger, U. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.11.008 · Cited by 67 · see citing works
Vulnerability of the Hippocampus to Insults: Links to Blood–Brain Barrier Dysfunction
Davidson, T. L., & Stevenson, R. J. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25041991 · Cited by 77 · see citing works
“The second contention is better supported and fits especially neatly with the therapeutic delay observed for anti-depressant medications [307,308], for behavioral interventions [306], and for the beneficial effects of electroconvulsive therapy [309].”
BackgroundSah, A., Schmuckermair, C., Sartori, S. B., Gaburro, S., Kandasamy, M., Irschick, R., Klimaschewski, L. P., Landgraf, R., Aigner, L., & Singewald, N. (2012) · Translational Psychiatry · doi:10.1038/tp.2012.94 · Cited by 67 · see citing works
“increasing or decreasing neurogenesis using knockouts or X-ray or pharmacological treatment is not sufficient to lead to the development of a depression-like phenotype in animals (for review, see Petrik et al.(46) and Sahay”
BackgroundInfluentialLeschik, J., Lutz, B., & Gentile, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22147339 · Cited by 70 · see citing works
Opendak, M., Offit, L., Monari, P., Schoenfeld, T. J., Sonti, A. N., Cameron, H. A., & Gould, E. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.4435-15.2016 · Cited by 61 · see citing works
“Studies have shown that stress-induced changes in behavior may be adaptive in many circumstances (Lagace et al., 2010; Petrik et al., 2012; Blanchard et al., 2013).”
BackgroundHarris, B. N. (2019) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2019.113355 · Cited by 76 · see citing works
Stress modulation of hippocampal activity – Spotlight on the dentate gyrus
Fa, M., Li, X., Anunu, R., Kehat, O., Kriebel, M., Volkmer, H., & Richter‐Levin, G. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.04.008 · Cited by 58 · see citing works
Perceived Stress Is Differentially Related to Hippocampal Subfield Volumes among Older Adults
Zimmerman, M. E., Ezzati, A., Katz, M. J., Lipton, M. L., Brickman, A. M., Sliwinski, M. J., & Lipton, R. B. (2016) · PLoS ONE · doi:10.1371/journal.pone.0154530 · Cited by 60 · see citing works
Yun, S., Donovan, M. H., Ross, M. N., Richardson, D. R., Reister, R., Farnbauch, L. A., Fischer, S. J., Riethmacher, D., Gershenfeld, H. K., Lagace, D. C., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0147256 · Cited by 50 · see citing works
Self-citationThe Kynurenine Pathway in Traumatic Brain Injury: Implications for Psychiatric Outcomes
Meier, T. B., & Savitz, J. B. (2021) · Biological Psychiatry · doi:10.1016/j.biopsych.2021.05.021 · Cited by 77 · see citing works
Zhao, L., Ren, H.-C., Gu, S.-N., Li, X., Jiang, C., Li, J., Zhang, M.-M., Mu, J.-L., Li, W., Wang, W., et al. (2018) · Psychiatry Research · doi:10.1016/j.psychres.2018.08.017 · Cited by 58 · see citing works
“The hippocampus is one of several limbic structures implicated in depression (Petrik et al., 2012).”
Functional differentiation of adult-born neurons along the septotemporal axis of the dentate gyrus.Preprint
Wu, M. V., Sahay, A., Duman, R., & Hen, R. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a018978 · Cited by 56 · see citing works
“In contrast, temporal, but not septal, hippocampal lesions result in deficits in predator-induced freezing (Phillips and LeDoux 1992), cued fear conditioning (Maren and Holt 2004), and novelty-induced hyponeophagia (Bannerman et al. 2002).”
BackgroundSex differences in response to chronic mild stress and congenital serotonin deficiency
Sachs, B. D., Ni, J. R., & Caron, M. G. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.11.008 · Cited by 51 · see citing works
“Chronic stress has been reported to inhibit adult hippocampal neurogenesis (Gould et al., 1997, 1998; Malberg and Duman, 2003), but the importance of hippocampal neurogenesis for depression- and anxiety-like behavior remains controversial (Petrik et al., 2012).”
BackgroundDiet-dependent gut microbiota impacts on adult neurogenesis through mitochondrial stress modulation
Ribeiro, M. F., Santos, A. A., Afonso, M. B., Rodrigues, P., Santos, S. S., Castro, R., Rodrigues, C., & Solá, S. (2020) · Brain Communications · doi:10.1093/braincomms/fcaa165 · Cited by 53 · see citing works
“, 2006; Hamilton and Holscher, 2012) and psychiatric disorders, particularly depression and anxiety (Petrik et al., 2012; Fang et al., 2018), whereas an increased rate of SGZ neurogenesis induced by treatment with antidepressants improves psychiatric disorders (Perera et al.”
BackgroundHu, P., Wang, Y., Liu, J., Meng, F., Qi, X., Chen, L., van Dam, A., Joëls, M., Lucassen, P. J., & Zhou, J. (2016) · Hippocampus · doi:10.1002/hipo.22574 · Cited by 39 · see citing works
“However, ablation of neurogenesis per se often does not induce a depressive phenotype (Santarelli et al., 2003; Henn and Vollmayr, 2004; Petrik et al., 2012).”
BackgroundSchnell, A., Sandrelli, F., Ranc, V., Ripperger, J. A., Brai, E., Alberi, L. A., Rainer, G., & Albrecht, U. (2015) · Chronobiology International · doi:10.3109/07420528.2015.1062024 · Cited by 53 · see citing works
“A growing body of evidence suggests that mooddisorders are associated with disturbed adult neurogenesis (Benes et al., 1998; Rajkowska, 2000), which appears to be crucial for proper mood control and efficient antidepressant therapy (Petrik et al., 2012; Samuels & Hen, 2011).”
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“, 2000), it is not clear if defects in neurogenesis play a role in depression (Petrik et al., 2012).”
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Dietary Polyphenols and Their Effects on Cell Biochemistry and Pathophysiology
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“This could be due to their capacities to scavenge NO or to decrease the NO synthase activity [110, 164, 185].”
BackgroundHuntingtin Mediates Anxiety/Depression-Related Behaviors and Hippocampal Neurogenesis
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Stressing new neurons into depression?
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Modulation of GABAA Receptor Signaling Increases Neurogenesis and Suppresses Anxiety through NFATc4
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The effects of congenital brain serotonin deficiency on responses to chronic fluoxetine
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“, 2011), whereas other studies did either not observe any change or an decrease in anxiety (recently reviewed by (Petrik et al., 2012).”
Microbiota-Gut-Brain Axis Regulation of Adult Hippocampal Neurogenesis
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Dietary Polyphenols and Their Effects on Cell Biochemistry and Pathophysiology 2013
Maraldi, T., Vauzour, D., & Angeloni, C. (2014) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2014/576363 · Cited by 53 · see citing works
“This could be due to their capacities to scavenge NO or to decrease the NO synthase activity [110, 164, 185].”
BackgroundInfluentialPI3K/AKT/GSK3β/CRMP-2-mediated neuroplasticity in depression induced by stress
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Reelin-Related Disturbances in Depression: Implications for Translational Studies
Caruncho, H. J., Brymer, K. J., Romay-Tallón, R., Mitchell, M. A., Baltanás, T. R., Botterill, J. J., Olivares, J. M., & Kalynchuk, L. E. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00048 · Cited by 42 · see citing works
“…from data showing that patients with depression have reduced hippocampal volume (MacQueen et al., 2003; Campbell et al., 2004) and that chronic stress and antidepressant drugs can decrease and increase cell proliferation and survival respectively (Santarelli et al., 2003; Petrik et al., 2012).”
BackgroundSakalem, M., Seidenbecher, T., Zhang, M.-Y., Saffari, R., Kravchenko, M., Wördemann, S., Diederich, K., Schwamborn, J., Zhang, W.-Q., & Ambrée, O. (2017) · Hippocampus · doi:10.1002/hipo.22669 · Cited by 42 · see citing works
“Indeed, as recently reviewed, almost every study which could show depressive-like or anxiety-related phenotypes due to neurogenesis impairments used different stressors prior to testing (Petrik et al., 2012).”
Background
- 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.
- Venue
- Neuropharmacology
- Publisher
- Elsevier BV
- Published
- 2012-01
- Volume
- 62
- Issue
- 1
- Pages
- 21-34
- ISSN
- 0028-3908 (ISSN-L)
- 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
- 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 › 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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