The current state of the neurogenic theory of depression and anxiety

Current Opinion in Neurobiology

Volumn 30, Issue , 2015, Pages 51-58

  Miller, Bradley R ^a,b   Hen, René ^a,b  

^a Howard Hughes Medical Institute   (United States)

^b NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANXIETY; BRAIN FUNCTION; BRAIN SIZE; COGNITION; COGNITIVE DEFECT; DEPRESSION; DISEASE ASSOCIATION; DISEASE MODEL; EXPERIMENTAL ANIMAL; HIPPOCAMPUS; HUMAN; MENTAL STRESS; NERVE CELL PLASTICITY; NERVE STIMULATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROIMAGING; NEUROPATHOLOGY; NONHUMAN; PATHOLOGICAL ANATOMY; PRIMATE; REVIEW; RODENT MODEL; ANIMAL; DRUG EFFECTS; NERVE CELL; PATHOLOGY; PHYSIOLOGY;

ANTIDEPRESSANT AGENT;

ANIMALS; ANTIDEPRESSIVE AGENTS; ANXIETY; DEPRESSION; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; HUMANS; NEUROGENESIS; NEURONS;

EID: 84907483716     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2014.08.012     Document Type: Review

References (73)

1. Spalding K.L., Bergmann O., Alkass K., Bernard S., Salehpour M., Huttner H.B., Boström E., Westerlund I., Vial C., Buchholz B.A., et al. Dynamics of hippocampal neurogenesis in adult humans. Cell 2013, 153:1219-1227.
2. Jacobs B.L., van Praag H., Gage F.H. Adult brain neurogenesis and psychiatry: a novel theory of depression. Mol Psychiatry 2000, 5:262-269.
3. Kempton M.J., Salvador Z., Munafò M.R., Geddes J.R., Simmons A., Frangou S., Williams S.C.R. Structural neuroimaging studies in major depressive disorder, meta-analysis and comparison with bipolar disorder. Arch Gen Psychiatry 2011, 68:675-690.
4. Cameron H.A., Gould E. Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 1994, 61:203-209.
5. Malberg J.E., Eisch A.J., Nestler E.J., Duman R.S. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci Off J Soc Neurosci 2000, 20:9104-9110.
6. Kessler R.C., Berglund P., Demler O., Jin R., Koretz D., Merikangas K.R., Rush A.J., Walters E.E., Wang P.S. National Comorbidity Survey Replication: the epidemiology of major depressive disorder: results from the National Comorbidity Survey Replication (NCS-R). J Am Med Assoc 2003, 289:3095-3105.
7. Kheirbek M.A., Klemenhagen K.C., Sahay A., Hen R. Neurogenesis and generalization: a new approach to stratify and treat anxiety disorders. Nat Neurosci 2012, 15:1613-1620.
8. Sahay A., Hen R. Adult hippocampal neurogenesis in depression. Nat Neurosci 2007, 10:1110-1115.
9. Leal S.L., Tighe S.K., Yassa M.A. Asymmetric effects of emotion on mnemonic interference. Neurobiol Learn Mem 2014, 111:41-48.
10. Santarelli L., Saxe M., Gross C., Surget A., Battaglia F., Dulawa S., Weisstaub N., Lee J., Duman R., Arancio O., et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 2003, 301:805-809.
11. Ferrari A.J., Charlson F.J., Norman R.E., Patten S.B., Freedman G., Murray C.J.L., Vos T., Whiteford H.A. Burden of depressive disorders by country, sex, age, and year: findings from the global burden of disease study 2010. PLoS Med 2013, 10:e1001547.
12. Gaynes B.N., Rush A.J., Trivedi M.H., Wisniewski S.R., Spencer D., Fava M. The STAR*D study: treating depression in the real world. Cleve Clin J Med 2008, 75:57-66.
13. Pham K., Nacher J., Hof P.R., McEwen B.S. Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur J Neurosci 2003, 17:879-886.
14. Lee K.-J., Kim S.-J., Kim S.-W., Choi S.-H., Shin Y.-C., Park S.-H., Moon B.-H., Cho E., Lee M.-S., Choi S.-H., et al. Chronic mild stress decreases survival, but not proliferation, of new-born cells in adult rat hippocampus. Exp Mol Med 2006, 38:44-54.
15. Van Bokhoven P., Oomen C.A., Hoogendijk W.J.G., Smit A.B., Lucassen P.J., Spijker S. Reduction in hippocampal neurogenesis after social defeat is long-lasting and responsive to late antidepressant treatment. Eur J Neurosci 2011, 33:1833-1840.
16. Dranovsky A., Picchini A.M., Moadel T., Sisti A.C., Yamada A., Kimura S., Leonardo E.D., Hen R. Experience dictates stem cell fate in the adult hippocampus. Neuron 2011, 70:908-923.
17. Hanson N.D., Owens M.J., Boss-Williams K.A., Weiss J.M., Nemeroff C.B. Several stressors fail to reduce adult hippocampal neurogenesis. Psychoneuroendocrinology 2011, 36:1520-1529.
18. Montero-Pedrazuela A., Venero C., Lavado-Autric R., Fernández-Lamo I., García-Verdugo J.M., Bernal J., Guadaño-Ferraz A. Modulation of adult hippocampal neurogenesis by thyroid hormones: implications in depressive-like behavior. Mol Psychiatry 2006, 11:361-371.
19. Wigger A., Neumann I.D. Periodic maternal deprivation induces gender-dependent alterations in behavioral and neuroendocrine responses to emotional stress in adult rats. Physiol Behav 1999, 66:293-302.
20. Mirescu C., Peters J.D., Gould E. Early life experience alters response of adult neurogenesis to stress. Nat Neurosci 2004, 7:841-846.
21. Perera T.D., Dwork A.J., Keegan K.A., Thirumangalakudi L., Lipira C.M., Joyce N., Lange C., Higley J.D., Rosoklija G., Hen R., et al. Necessity of hippocampal neurogenesis for the therapeutic action of antidepressants in adult nonhuman primates. PLoS ONE 2011, 6:e17600.
22. Gould E., Tanapat P., McEwen B.S., Flügge G., Fuchs E. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc Natl Acad Sci U S A 1998, 95:3168-3171.
23. Wu M.V., Shamy J.L., Bedi G., Choi C-W.J., Wall M.M., Arango V., Boldrini M., Foltin R.W., Hen R. Impact of social status and antidepressant treatment on neurogenesis in the baboon hippocampus. Neuropsychopharmacol Off Publ Am Coll Neuropsychopharmacol 2014, 10.1038/npp.2014.33.
24. Spalding K.L., Bhardwaj R.D., Buchholz B.A., Druid H., Frisén J. Retrospective birth dating of cells in humans. Cell 2005, 122:133-143.
25. Reif A., Fritzen S., Finger M., Strobel A., Lauer M., Schmitt A., Lesch K-P. Neural stem cell proliferation is decreased in schizophrenia, but not in depression. Mol Psychiatry 2006, 11:514-522.
26. Boldrini M., Underwood M.D., Hen R., Rosoklija G.B., Dwork A.J., John Mann J., Arango V. Antidepressants increase neural progenitor cells in the human hippocampus. Neuropsychopharmacol Off Publ Am Coll Neuropsychopharmacol 2009, 34:2376-2389.
27. Lucassen P.J., Stumpel M.W., Wang Q., Aronica E. Decreased numbers of progenitor cells but no response to antidepressant drugs in the hippocampus of elderly depressed patients. Neuropharmacology 2010, 58:940-949.
28. Boldrini M., Santiago A.N., Hen R., Dwork A.J., Rosoklija G.B., Tamir H., Arango V., John Mann J. Hippocampal granule neuron number and dentate gyrus volume in antidepressant-treated and untreated major depression. Neuropsychopharmacol Off Publ Am Coll Neuropsychopharmacol 2013, 38:1068-1077.
29. Huang Y., Coupland N.J., Lebel R.M., Carter R., Seres P., Wilman A.H., Malykhin N.V. Structural changes in hippocampal subfields in major depressive disorder: a high-field magnetic resonance imaging study. Biol Psychiatry 2013, 74:62-68.
30. Wang Z., Neylan T.C., Mueller S.G., Lenoci M., Truran D., Marmar C.R., Weiner M.W., Schuff N. Magnetic resonance imaging of hippocampal subfields in posttraumatic stress disorder. Arch Gen Psychiatry 2010, 67:296-303.
31. Arnone D., McKie S., Elliott R., Juhasz G., Thomas E.J., Downey D., Williams S., Deakin J.F.W., Anderson I.M. State-dependent changes in hippocampal grey matter in depression. Mol Psychiatry 2013, 18:1265-1272.
32. Nakashiba T., Cushman J.D., Pelkey K.A., Renaudineau S., Buhl D.L., McHugh T.J., Rodriguez Barrera V., Chittajallu R., Iwamoto K.S., McBain C.J., et al. Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell 2012, 149:188-201.
33. Déry N., Pilgrim M., Gibala M., Gillen J., Wojtowicz J.M., Macqueen G., Becker S. Adult hippocampal neurogenesis reduces memory interference in humans: opposing effects of aerobic exercise and depression. Front Neurosci 2013, 7:66.
34. Shelton D.J., Kirwan C.B. A possible negative influence of depression on the ability to overcome memory interference. Behav Brain Res 2013, 256:20-26.
35. Leal S.L., Tighe S.K., Jones C.K., Yassa M.A. Pattern separation of emotional information in hippocampal dentate and CA3. Hippocampus 2014, 10.1002/hipo.22298.
36. Ho N.F., Hooker J.M., Sahay A., Holt D.J., Roffman J.L. In vivo imaging of adult human hippocampal neurogenesis: progress, pitfalls and promise. Mol Psychiatry 2013, 18:404-416.
37. Manganas L.N., Zhang X., Li Y., Hazel R.D., Smith S.D., Wagshul M.E., Henn F., Benveniste H., Djuric P.M., Enikolopov G., et al. Magnetic resonance spectroscopy identifies neural progenitor cells in the live human brain. Science 2007, 318:980-985.
38. Pereira A.C., Huddleston D.E., Brickman A.M., Sosunov A.A., Hen R., McKhann G.M., Sloan R., Gage F.H., Brown T.R., Small S.A. An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus. Proc Natl Acad Sci U S A 2007, 104:5638-5643.
39. Petrik D., Lagace D.C., Eisch A.J. The neurogenesis hypothesis of affective and anxiety disorders: are we mistaking the scaffolding for the building?. Neuropharmacology 2012, 62:21-34.
40. Revest J.-M., Dupret D., Koehl M., Funk-Reiter C., Grosjean N., Piazza P.-V., Abrous D.N. Adult hippocampal neurogenesis is involved in anxiety-related behaviors. Mol Psychiatry 2009, 14:959-967.
41. Snyder J.S., Soumier A., Brewer M., Pickel J., Cameron H.A. Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature 2011, 476:458-461.
42. Schloesser R.J., Manji H.K., Martinowich K. Suppression of adult neurogenesis leads to an increased hypothalamo-pituitary-adrenal axis response. Neuroreport 2009, 20:553-557.
43. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders 2013, American Psychiatric Association, [Internet]. edn 5.
44. Burghardt N.S., Park E.H., Hen R., Fenton A.A. Adult-born hippocampal neurons promote cognitive flexibility in mice. Hippocampus 2012, 22:1795-1808.
45. Pereira Dias G., Hollywood R., Bevilaqua M.C., do N., da Luz A.C.D., da S., Hindges R., Nardi A.E., Thuret S. Consequences of cancer treatments on adult hippocampal neurogenesis: implications for cognitive function and depressive symptoms. Neuro-Oncology 2014, 16:476-492.
46. Lydiatt W.M., Bessette D., Schmid K.K., Sayles H., Burke W.J. Prevention of depression with escitalopram in patients undergoing treatment for head and neck cancer: randomized, double-blind, placebo-controlled clinical trial. JAMA Otolaryngol Head Neck Surg 2013, 139:678-686.
47. Madsen T.M., Treschow A., Bengzon J., Bolwig T.G., Lindvall O., Tingström A. Increased neurogenesis in a model of electroconvulsive therapy. Biol Psychiatry 2000, 47:1043-1049.
48. Scott B.W., Wojtowicz J.M., Burnham W.M. Neurogenesis in the dentate gyrus of the rat following electroconvulsive shock seizures. Exp Neurol 2000, 165:231-236.
49. Chen G., Rajkowska G., Du F., Seraji-Bozorgzad N., Manji H.K. Enhancement of hippocampal neurogenesis by lithium. J Neurochem 2000, 75:1729-1734.
50. Benninghoff J., Grunze H., Schindler C., Genius J., Schloesser R.J., van der Ven A., Dehning S., Wiltfang J., Möller H.J., Rujescu D. Ziprasidone-not haloperidol-induces more de-novo neurogenesis of adult neural stem cells derived from murine hippocampus. Pharmacopsychiatry 2013, 46:10-15.
51. Remaud S., Gothié J.-D., Morvan-Dubois G., Demeneix B.A. Thyroid hormone signaling and adult neurogenesis in mammals. Front Endocrinol 2014, 5:62.
52. Keilhoff G., Bernstein H.-G., Becker A., Grecksch G., Wolf G. Increased neurogenesis in a rat ketamine model of schizophrenia. Biol Psychiatry 2004, 56:317-322.
53. Holick K.A., Lee D.C., Hen R., Dulawa S.C. Behavioral effects of chronic fluoxetine in BALB/cJ mice do not require adult hippocampal neurogenesis or the serotonin 1A receptor. Neuropsychopharmacol Off Publ Am Coll Neuropsychopharmacol 2008, 33:406-417.
54. Huang G.-J., Bannerman D., Flint J. Chronic fluoxetine treatment alters behavior, but not adult hippocampal neurogenesis, in BALB/cJ mice. Mol Psychiatry 2008, 13:119-121.
55. Cowen D.S., Takase L.F., Fornal C.A., Jacobs B.L. Age-dependent decline in hippocampal neurogenesis is not altered by chronic treatment with fluoxetine. Brain Res 2008, 1228:14-19.
56. Huang G.-J., Herbert J. Stimulation of neurogenesis in the hippocampus of the adult rat by fluoxetine requires rhythmic change in corticosterone. Biol Psychiatry 2006, 59:619-624.
57. Miller B.H., Schultz L.E., Gulati A., Cameron M.D., Pletcher M.T. Genetic regulation of behavioral and neuronal responses to fluoxetine. Neuropsychopharmacol Off Publ Am Coll Neuropsychopharmacol 2008, 33:1312-1322.
58. Alahmed S., Herbert J. Strain differences in proliferation of progenitor cells in the dentate gyrus of the adult rat and the response to fluoxetine are dependent on corticosterone. Neuroscience 2008, 157:677-682.
59. David D.J., Samuels B.A., Rainer Q., Wang J.-W., Marsteller D., Mendez I., Drew M., Craig D.A., Guiard B.P., Guilloux J.-P., et al. Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 2009, 62:479-493.
60. Anacker C., Zunszain P.A., Cattaneo A., Carvalho L.A., Garabedian M.J., Thuret S., Price J., Pariante C.M. Antidepressants increase human hippocampal neurogenesis by activating the glucocorticoid receptor. Mol Psychiatry 2011, 16:738-750.
61. Perera T.D., Coplan J.D., Lisanby S.H., Lipira C.M., Arif M., Carpio C., Spitzer G., Santarelli L., Scharf B., Hen R., et al. Antidepressant-induced neurogenesis in the hippocampus of adult nonhuman primates. J Neurosci Off J Soc Neurosci 2007, 27:4894-4901.
62. Boldrini M., Butt T.H., Santiago A.N., Tamir H., Dwork A.J., Rosoklija G.B., Arango V., Hen R., Mann J.J. Benzodiazepines and the potential trophic effect of antidepressants on dentate gyrus cells in mood disorders. Int J Neuropsychopharmacol Off Sci J Coll Int Neuropsychopharmacol CINP 2014, 10.1017/S1461145714000844.
63. Tendolkar I., van Beek M., van Oostrom I., Mulder M., Janzing J., Voshaar R.O., van Eijndhoven P. Electroconvulsive therapy increases hippocampal and amygdala volume in therapy refractory depression: a longitudinal pilot study. Psychiatry Res 2013, 214:197-203.
64. Vermetten E., Vythilingam M., Southwick S.M., Charney D.S., Bremner J.D. Long-term treatment with paroxetine increases verbal declarative memory and hippocampal volume in posttraumatic stress disorder. Biol Psychiatry 2003, 54:693-702.
65. Hallahan B., Newell J., Soares J.C., Brambilla P., Strakowski S.M., Fleck D.E., Kieseppä T., Altshuler L.L., Fornito A., Malhi G.S., et al. Structural magnetic resonance imaging in bipolar disorder: an international collaborative mega-analysis of individual adult patient data. Biol Psychiatry 2011, 69:326-335.
66. Duman R.S. Neural plasticity: consequences of stress and actions of antidepressant treatment. Dialogues Clin Neurosci 2004, 6:157-169.
67. Singer B.H., Jutkiewicz E.M., Fuller C.L., Lichtenwalner R.J., Zhang H., Velander A.J., Li X., Gnegy M.E., Burant C.F., Parent J.M. Conditional ablation and recovery of forebrain neurogenesis in the mouse. J Comp Neurol 2009, 514:567-582.
68. Surget A., Tanti A., Leonardo E.D., Laugeray A., Rainer Q., Touma C., Palme R., Griebel G., Ibarguen-Vargas Y., Hen R., et al. Antidepressants recruit new neurons to improve stress response regulation. Mol Psychiatry 2011, 16:1177-1188.
69. Deisseroth K. Circuit dynamics of adaptive and maladaptive behaviour. Nature 2014, 505:309-317.
70. Lim B.K., Huang K.W., Grueter B.A., Rothwell P.E., Malenka R.C. Anhedonia requires MC4R-mediated synaptic adaptations in nucleus accumbens. Nature 2012, 487:183-189.
71. 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. Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 2011, 472:466-470.
72. Pieper A.A., Xie S., Capota E., Estill S.J., Zhong J., Long J.M., Becker G.L., Huntington P., Goldman S.E., Shen C-H., et al. Discovery of a proneurogenic, neuroprotective chemical. Cell 2010, 142:39-51.
73. 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. The P7C3 class of neuroprotective compounds exerts antidepressant efficacy in mice by increasing hippocampal neurogenesis. Mol Psychiatry 2014, 10.1038/mp.2014.34.