New hippocampal neurons mature rapidly in response to ketamine but are not required for its acute antidepressant effects on neophagia in rats

eNeuro

Volumn 3, Issue 2, 2016, Pages 66-77

  Soumier, Amelie ^a   Carter, Rayna M ^a   Schoenfeld, Timothy J ^a   Cameron, Heather A ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE; CORTICOSTERONE; CYCLINE; KETAMINE; PENTOBARBITAL; AMINO ACID RECEPTOR BLOCKING AGENT; ANTIDEPRESSANT AGENT; GLIAL FIBRILLARY ACIDIC PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIDEPRESSANT ACTIVITY; ARTICLE; BEHAVIOR CHANGE; BRAIN NERVE CELL; BRDU ASSAY; CELL MATURATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DENTATE GYRUS; DEPRESSION; FORCED SWIM TEST; GENE EXPRESSION; HIPPOCAMPUS POTENTIAL; HISTOLOGY; MALE; MOOD DISORDER; NEOPLASM; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NOVELTY SUPPRESSED FEEDING TEST; PRIORITY JOURNAL; RAT; SEIZURE; SUCROSE PREFERENCE TEST; ANIMAL; CYTOLOGY; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; FOOD DEPRIVATION; GENE EXPRESSION REGULATION; GENETICS; HIPPOCAMPUS; LONG EVANS RAT; METABOLISM; NERVE CELL; PATHOLOGY; PSYCHOLOGY; SWIMMING; TIME FACTOR; TRANSGENIC RAT;

ANIMALS; ANTIDEPRESSIVE AGENTS; CELL PROLIFERATION; CELL SURVIVAL; CORTICOSTERONE; DEPRESSION; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY AMINO ACID ANTAGONISTS; FOOD DEPRIVATION; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; HIPPOCAMPUS; KETAMINE; MALE; NEUROGENESIS; NEURONS; RATS; RATS, LONG-EVANS; RATS, TRANSGENIC; SWIMMING; TIME FACTORS;

EID: 84993673251     PISSN: None     EISSN: 23732822     Source Type: Journal    
DOI: 10.1523/ENEURO.0116-15.2016     Document Type: Article

References (62)

1. Abdallah CG, Averill LA, Krystal JH (2015) Ketamine as a promising prototype for a new generation of rapid-acting antidepressants. Ann N Y Acad Sci 1344: 66-77. CrossRef Medline
2. Adesnik H, Li G, During MJ, Pleasure SJ, Nicoll RA (2008) NMDA receptors inhibit synapse unsilencing during brain development. Proc Natl Acad Sci U S A 105: 5597-5602. CrossRef Medline
3. Autry AE, Adachi M, Nosyreva E, Na ES, Los MF, Cheng P-F, Kavalali ET, Monteggia LM (2011) NMDA receptor blockade at rest triggers rapid behavioural antidepressant responses. Nature 475: 91-95. CrossRef Medline
4. Bodnoff SR, Suranyi-Cadotte B, Aitken DH, Quirion R, Meaney MJ (1988) The effects of chronic antidepressant treatment in an animal model of anxiety. Psychopharmacology (Berl) 95: 298-302. Medline
5. Brachman RA, McGowan JC, Perusini JN, Lim SC, Pham TH, Faye C, Gardier AM, Mendez-David I, David DJ, Hen R, Denny CA (2015) Ketamine as a prophylactic against stress-induced depressive-like behavior. Biol Psychiatry. Advance online publication. Retrieved March 23, 2016. CrossRef
6. Browne CA, Lucki I (2013) Antidepressant effects of ketamine: mechanisms underlying fast-acting novel antidepressants. Front Pharmacol 4: 161. CrossRef Medline
7. Cameron HA, McEwen BS, Gould E (1995) Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. J Neurosci 15: 4687-4692. Medline
8. Cameron HA, Tanapat P, Gould E (1998) Adrenal steroids and N-methyl-D-aspartate receptor activation regulate neurogenesis in the dentate gyrus of adult rats through a common pathway. Neuroscience 82: 349-354. Medline
9. Carrier N, Kabbaj M (2013) Sex differences in the antidepressant-like effects of ketamine. Neuropharmacology 70: 27-34. CrossRef Medline
10. Chancey JH, Adlaf EW, Sapp MC, Pugh PC, Wadiche JI, Overstreet-Wadiche LS (2013) GABA depolarization is required for experience-dependent synapse unsilencing in adult-born neurons. J Neurosci 33: 6614-6622. CrossRef Medline
11. Cryan JF, Valentino RJ, Lucki I (2005) Assessing substrates underlying the behavioral effects of antidepressants using the modified rat forced swimming test. Neurosci Biobehav Rev 29: 547-569. CrossRef Medline
12. David DJ, Samuels BA, Rainer Q, Wang J-W, Marsteller D, Mendez I, Drew M, Craig DA, Guiard BP, Guilloux J-P, Artymyshyn RP, Gardier AM, Gerald C, Antonijevic IA, Leonardo ED, Hen R (2009) Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 62: 479-493. CrossRef Medline
13. Dayer AG, Ford AA, Cleaver KM, Yassaee M, Cameron HA (2003) Short-term and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol 460: 563-572. CrossRef Medline
14. Duman RS (2004) Depression: a case of neuronal life and death? Biol Psychiatry 56: 140-145. CrossRef Medline
15. Duman RS (2014) Neurobiology of stress, depression, and rapid acting antidepressants: remodeling synaptic connections. Depress Anxiety 31: 291-296. CrossRef
16. Duman RS, Malberg J, Nakagawa S (2001) Regulation of adult neurogenesis by psychotropic drugs and stress. J Pharmacol Exp Ther 299: 401-407. Medline
17. Engin E, Treit D, Dickson C (2009) Anxiolytic- and antidepressant-like properties of ketamine in behavioral and neurophysiological animal models. Neuroscience 161: 359-369.
18. Fernando ABP, Robbins TW (2011) Animal models of neuropsychiatric disorders. Annu Rev Clin Psychol 7: 39-61. CrossRef Medline
19. Garcia LSB, Comim CM, Valvassori SS, Réus GZ, Barbosa LM, Andreazza AC, Stertz L, Fries GR, Gavioli EC, Kapczinski F, Quevedo J (2008) Acute administration of ketamine induces antidepressant-like effects in the forced swimming test and increases BDNF levels in the rat hippocampus. Prog Neuropsychopharmacol Biol Psychiatry 32: 140-144. CrossRef
20. Gideons ES, Kavalali ET, Monteggia LM (2014) Mechanisms underlying differential effectiveness of memantine and ketamine in rapid antidepressant responses. Proc Natl Acad Sci U S A 111: 8649-8654. CrossRef Medline
21. Gourley SL, Kedves AT, Olausson P, Taylor JR (2009) A history of corticosterone exposure regulates fear extinction and cortical NR2B, GluR2/3, and BDNF. Neuropsychopharmacology 34: 707-716. CrossRef Medline
22. Groc L, Gustafsson B, Hanse E (2006) AMPA signalling in nascent glutamatergic synapses: there and not there! Trends Neurosci 29: 132-139. CrossRef Medline
23. Hale CF, Dietz KC, Varela JA, Wood CB, Zirlin BC, Leverich LS, Greene RW, Cowan CW (2011) Essential role for vav guanine nucleotide exchange factors in brain-derived neurotrophic factorinduced dendritic spine growth and synapse plasticity. J Neurosci 31: 12426-12436. CrossRef Medline
24. Holtmaat A, Svoboda K (2009) Experience-dependent structural synaptic plasticity in the mammalian brain. Nat Rev Neurosci 10: 647-658. CrossRef Medline
25. Hunt MJ, Raynaud B, Garcia R (2006) Ketamine dose-dependently induces high-frequency oscillations in the nucleus accumbens in freely moving rats. Biol Psychiatry 60: 1206-1214. CrossRef Medline
26. Hyman SE (2012) Revolution stalled. Sci Transl Med 4: 155cm11. CrossRef Medline
27. Iadarola ND, Niciu MJ, Richards EM, Vande Voort JL, Ballard ED, Lundin NB, Nugent AC, Machado-Vieira R, Zarate CA (2015) Ketamine and other N-methyl-D-aspartate receptor antagonists in the treatment of depression: a perspective review. Ther Adv Chronic Dis 6: 97-114. CrossRef Medline
28. Iijima M, Fukumoto K, Chaki S (2012) Acute and sustained effects of a metabotropic glutamate 5 receptor antagonist in the noveltysuppressed feeding test. Behav Brain Res 235: 287-292. CrossRef Medline
29. Jones MW, Errington ML, French PJ, Fine A, Bliss TV, Garel S, Charnay P, Bozon B, Laroche S, Davis S (2001) A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat Neurosci 4: 289-296. CrossRef Medline
30. Jungenitz T, Radic T, Jedlicka P, Schwarzacher SW (2014) Highfrequency stimulation induces gradual immediate early gene expression in maturing adult-generated hippocampal granule cells. Cereb Cortex 24: 1845-1857.
31. Kavalali ET, Monteggia LM (2015) How does ketamine elicit a rapid antidepressant response? Curr Opin Pharmacol 20: 35-39. CrossRef Medline
32. Koike H, Iijima M, Chaki S (2011) Involvement of AMPA receptor in both the rapid and sustained antidepressant-like effects of ketamine in animal models of depression. Behav Brain Res 224: 107-111. CrossRef Medline
33. Kwon H-B, Sabatini BL (2011) Glutamate induces de novo growth of functional spines in developing cortex. Nature 474: 100-104. CrossRef Medline
34. Li N, Lee B, Liu R-J, Banasr M, Dwyer JM, Iwata M, Li X-Y, Aghajanian G, Duman RS (2010) mTOR-dependent synapse formation underlies the rapid antidepressant effects of NMDA antagonists. Science 329: 959-964. CrossRef
35. Li N, Liu R-J, Dwyer JM, Banasr M, Lee B, Son H, Li X-Y, Aghajanian G, Duman RS (2011) Glutamate N-methyl-D-aspartate receptor antagonists rapidly reverse behavioral and synaptic deficits caused by chronic stress exposure. Biol Psychiatry 69: 754-761. CrossRef Medline
36. Maeng S, Zarate CA, Du J, Schloesser RJ, McCammon J, Chen G, Manji HK (2008) Cellular mechanisms underlying the antidepressant effects of ketamine: role of alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptors. Biol Psychiatry 63: 349-352. CrossRef Medline
37. Malberg JE, Eisch AJ, Nestler EJ, Duman RS (2000) Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20: 9104-9110. Medline
38. Mathew SJ, Shah A, Lapidus K, Clark C, Jarun N, Ostermeyer B, Murrough JW (2012) Ketamine for treatment-resistant unipolar depression: current evidence. CNS Drugs 26: 189-204. CrossRef Medline
39. Nacher J, McEwen BS (2006) The role of N-methyl-D-asparate receptors in neurogenesis. Hippocampus 16: 267-270. CrossRef Medline
40. Nacher J, Rosell DR, Alonso-Llosa G, McEwen BS (2001) NMDA receptor antagonist treatment induces a long-lasting increase in the number of proliferating cells, PSA-NCAM-immunoreactive granule neurons and radial glia in the adult rat dentate gyrus. Eur J Neurosci 13: 512-520. Medline
41. Nestler EJ, Hyman SE (2010) Animal models of neuropsychiatric disorders. Nat Neurosci 13: 1161-1169. CrossRef Medline
42. Nosyreva E, Autry AE, Kavalali ET, Monteggia LM (2014) Age dependence of the rapid antidepressant and synaptic effects of acute NMDA receptor blockade. Front Mol Neurosci 7: 94. CrossRef Medline
43. Okabe S (2013) Fluorescence imaging of synapse formation and remodeling. Microscopy (Oxf) 62: 51-62. CrossRef
44. Medline Overstreet-Wadiche LS, Bromberg DA, Bensen AL, Westbrook GL (2006) Seizures accelerate functional integration of adultgenerated granule cells. J Neurosci 26: 4095-4103. CrossRef
45. Piatti VC, Espósito MS, Schinder AF (2006) The timing of neuronal development in adult hippocampal neurogenesis. Neuroscientist 12: 463-468. CrossRef Medline
46. Porsolt RD, Brossard G, Hautbois C, Roux S (2001) Rodent models of depression: forced swimming and tail suspension behavioral despair tests in rats and mice. Curr Protoc Neurosci Chapter8: Unit8.10A. CrossRef Medline
47. Sanacora G, Zarate CA, Krystal JH, Manji HK (2008) Targeting the glutamatergic system to develop novel, improved therapeutics for mood disorders. Nat Rev Drug Discov 7: 426-437. CrossRef Medline
48. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S, Weisstaub N, Lee J, Duman R, Arancio O, Belzung C, Hen R (2003) Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301: 805-809. CrossRef Medline
49. Skolnick P, Layer RT, Popik P, Nowak G, Paul IA, Trullas R (1996) Adaptation of N-methyl-D-aspartate (NMDA) receptors following antidepressant treatment: implications for the pharmacotherapy of depression. Pharmacopsychiatry 29: 23-26. CrossRef Medline
50. Skolnick P, Popik P, Trullas R (2009) Glutamate-based antidepressants: 20 years on. Trends Pharmacol Sci 30: 563-569. CrossRef Medline
51. Snyder JS, Kee N, Wojtowicz JM (2001) Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. J Neurophysiol 85: 2423-2431. Medline
52. Snyder JS, Glover LR, Sanzone KM, Kamhi JF, Cameron HA (2009a) The effects of exercise and stress on the survival and maturation of adult-generated granule cells. Hippocampus 19: 898-906. CrossRef Medline
53. Snyder JS, Choe JS, Clifford MA, Jeurling SI, Hurley P, Brown A, Kamhi JF, Cameron HA (2009b) Adult-born hippocampal neurons are more numerous, faster maturing, and more involved in behavior in rats than in mice. J Neurosci 29: 14484-14495. CrossRef Medline
54. Snyder JS, Soumier A, Brewer M, Pickel J, Cameron HA (2011) Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature 476: 458-461. CrossRef Medline
55. Soumier A, Banasr M, Lortet S, Masmejean F, Bernard N, Kerkerian-Le-Goff L, Gabriel C, Millan MJ, Mocaer E, Daszuta A (2009) Mechanisms contributing to the phase-dependent regulation of neurogenesis by the novel antidepressant, agomelatine, in the adult rat hippocampus. Neuropsychopharmacology 34: 2390-2403. CrossRef Medline
56. Sterner EY, Kalynchuk LE (2010) Behavioral and neurobiological consequences of prolonged glucocorticoid exposure in rats: relevance to depression. Prog Neuropsychopharmacol Biol Psychiatry 34: 777-790. CrossRef Medline
57. Tashiro A, Sandler VM, Toni N, Zhao C, Gage FH (2006) NMDAreceptor-mediated, cell-specific integration of new neurons in adult dentate gyrus. Nature 442: 929-933. CrossRef Medline
58. Wang J-W, David DJ, Monckton JE, Battaglia F, Hen R (2008) Chronic fluoxetine stimulates maturation and synaptic plasticity of adult-born hippocampal granule cells. J Neurosci 28: 1374-1384. CrossRef Medline
59. Warner-Schmidt JL, Duman RS (2006) Hippocampal neurogenesis: opposing effects of stress and antidepressant treatment. Hippocampus 16: 239-249. CrossRef Medline
60. Wilson C, Kercher M, Quinn B, Murphy A, Fiegel C, McLaurin A (2007) Effects of age and sex on ketamine-induced hyperactivity in rats. Physiol Behav 91: 202-207. CrossRef Medline
61. Wong EYH, Herbert J (2005) Roles of mineralocorticoid and glucocorticoid receptors in the regulation of progenitor proliferation in the adult hippocampus. Eur J Neurosci 22: 785-792. CrossRef Medline
62. Woolley CS, McEwen BS (1992) Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci 12: 2549-2554. Medline