Repeated ketamine exposure induces an enduring resilient phenotype in adolescent and adult rats

Biological Psychiatry

Volumn 74, Issue 10, 2013, Pages 750-759

  Parise, Eric M ^a   Alcantara, Lyonna F ^a   Warren, Brandon L ^a   Wright, Katherine N ^a   Hadad, Roey ^a   Sial, Omar K ^a   Kroeck, Kyle G ^a   Iñiguez, Sergio D ^a   Bolaños Guzmán, Carlos A ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

Author keywords

Adolescence; anxiety; depression; ketamine; rats; resilience; stress

Indexed keywords

KETAMINE;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIDEPRESSANT ACTIVITY; ARTICLE; AVERSIVE BEHAVIOR; CONTROLLED STUDY; DEPRESSION; DRUG EFFICACY; DRUG SEEKING BEHAVIOR; FOOD INTAKE; FORCED SWIMMING TEST; MALE; NONHUMAN; PHENOTYPE; PLACE PREFERENCE; PRIORITY JOURNAL; RAT; STRESS; TREATMENT RESPONSE; WEIGHT GAIN;

ADOLESCENCE; ANXIETY; DEPRESSION; KETAMINE; RATS; RESILIENCE; STRESS;

AGE FACTORS; ANIMALS; ANTIDEPRESSIVE AGENTS; ANXIETY; DEPRESSION; EXCITATORY AMINO ACID ANTAGONISTS; KETAMINE; MALE; PHENOTYPE; RATS; RATS, SPRAGUE-DAWLEY; STRESS, PSYCHOLOGICAL; SWIMMING;

EID: 84886722040     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2013.04.027     Document Type: Article

References (95)

1. S. Hyman, D. Chisholm, R. Kessler, V. Patel, and H. Whiteford Mental disorders D.T. Jamison, J.G. Breman, A.R. Measham, G. Alleyne, M. Claeson, D.B. Evans, Disease Control Priorities in Developing Countries, 2nd ed 2006 World Bank Publications Washington, DC
2. C.J. Murray, and A.D. Lopez Evidence-based health policy - lessons from the Global Burden of Disease Study Science 274 1996 740 743
3. P.F. Sullivan, M.J. Daly, and M. O'Donovan Genetic architectures of psychiatric disorders: The emerging picture and its implications Nat Rev Genet 13 2012 537 551
4. E.J. Nestler, M. Barrot, R.J. DiLeone, A.J. Eisch, S.J. Gold, and L.M. Monteggia Neurobiology of depression Neuron 34 2002 13 25
5. H.K. Manji, W.C. Drevets, and D.S. Charney The cellular neurobiology of depression Nat Med 7 2001 541 547
6. P.Y. Collins, V. Patel, S.S. Joestl, D. March, T.R. Insel, and A.S. Daar Grand challenges in global mental health Nature 475 2011 27 30
7. P.E. Greenberg, R.C. Kessler, H.G. Birnbaum, S.A. Leong, S.W. Lowe, and P.A. Berglund The economic burden of depression in the United States: How did it change between 1990 and 2000? J Clin Psychiatry 64 2003 1465 1475
8. T.K. Richmond, and D.S. Rosen The treatment of adolescent depression in the era of the black box warning Curr Opin Pediatr 17 2005 466 472
9. A. Slomski Chronic mental health issues in children now loom larger than physical problems JAMA 308 2012 223 225
10. K. Hawton, K.E. Saunders, and R.C. O'Connor Self-harm and suicide in adolescents Lancet 379 2012 2373 2382
11. D.J. Safer Should selective serotonin reuptake inhibitors be prescribed for children with major depressive and anxiety disorders? Pediatrics 118 2006 1248 1251
12. B. Birmaher Should we use antidepressant medications for children and adolescents with depressive disorders? Psychopharmacol Bull 34 1998 35 39
13. J.N. Jureidini, C.J. Doecke, P.R. Mansfield, M.M. Haby, D.B. Menkes, and A.L. Tonkin Efficacy and safety of antidepressants for children and adolescents BMJ 328 2004 879 883
14. C.J. Kratochvil, B. Vitiello, J. Walkup, G. Emslie, B.D. Waslick, and E.B. Weller Selective serotonin reuptake inhibitors in pediatric depression: Is the balance between benefits and risks favorable? J Child Adolesc Psychopharmacol 16 2006 11 24
15. G.J. Emslie, and T.L. Mayes Mood disorders in children and adolescents: psychopharmacological treatment Biol Psychiatry 49 2001 1082 1090
16. J.M. Zito, D.J. Safer, S. DosReis, J.F. Gardner, K. Soeken, and M. Boles Rising prevalence of antidepressants among US youths Pediatrics 109 2002 721 727
17. J.T. Coyle, D.S. Pine, D.S. Charney, L. Lewis, C.B. Nemeroff, and G.A. Carlson Depression and bipolar support alliance consensus statement on the unmet needs in diagnosis and treatment of mood disorders in children and adolescents J Am Acad Child Adolesc Psychiatry 42 2003 1494 1503
18. F.T. Maalouf, M. Atwi, and D.A. Brent Treatment-resistant depression in adolescents: Review and updates on clinical management Depress Anxiety 28 2011 946 954
19. P. Hazell Depression in children and adolescents [published online ahead of print October 21] Clin Evid (Online) 2011
20. G.J. Emslie, T. Mayes, G. Porta, B. Vitiello, G. Clarke, and K.D. Wagner Treatment of Resistant Depression in Adolescents (TORDIA): Week 24 outcomes Am J Psychiatry 167 2010 782 791
21. R.M. Berman, A. Cappiello, A. Anand, D.A. Oren, G.R. Heninger, and D.S. Charney Antidepressant effects of ketamine in depressed patients Biol Psychiatry 47 2000 351 354
22. N. Diazgranados, L. Ibrahim, N.E. Brutsche, A. Newberg, P. Kronstein, and S. Khalife A randomized add-on trial of an N-methyl-D-aspartate antagonist in treatment-resistant bipolar depression Arch Gen Psychiatry 67 2010 793 802
23. G.L. Larkin, and A.L. Beautrais A preliminary naturalistic study of low-dose ketamine for depression and suicide ideation in the emergency department Int J Neuropsychopharmacol 14 2011 1127 1131
24. S.J. Mathew, J.W. Murrough, M. aan het Rot, K.A. Collins, D.L. Reich, and D.S. Charney Riluzole for relapse prevention following intravenous ketamine in treatment-resistant depression: A pilot randomized, placebo-controlled continuation trial Int J Neuropsychopharmacol 13 2010 71 82
25. C.A. Zarate Jr, J.B. Singh, P.J. Carlson, N.E. Brutsche, R. Ameli, and D.A. Luckenbaugh A randomized trial of an N-methyl-D-aspartate antagonist in treatment-resistant major depression Arch Gen Psychiatry 63 2006 856 864
26. M. Aan Het Rot, C.A. Zarate Jr, D.S. Charney, and S.J. Mathew Ketamine for depression: Where do we go from here? Biol Psychiatry 72 2012 537 547
27. J.W. Murrough, A.M. Perez, S. Pillemer, J. Stern, M.K. Parides, and M. Aan Het Rot Rapid and longer-term antidepressant effects of repeated ketamine infusions in treatment-resistant major depression [published online ahead of print July 26] Biol Psychiatry 2012
28. A.E. Autry, M. Adachi, E. Nosyreva, E.S. Na, M.F. Los, and P.F. Cheng NMDA receptor blockade at rest triggers rapid behavioural antidepressant responses Nature 475 2011 91 95
29. E. Engin, D. Treit, and C.T. Dickson Anxiolytic- and antidepressant-like properties of ketamine in behavioral and neurophysiological animal models Neuroscience 161 2009 359 369
30. N. Li, R.J. Liu, J.M. Dwyer, M. Banasr, B. Lee, and H. Son Glutamate N-methyl-D-aspartate receptor antagonists rapidly reverse behavioral and synaptic deficits caused by chronic stress exposure Biol Psychiatry 69 2011 754 761
31. R.R. Holson, and B. Pearce Principles and pitfalls in the analysis of prenatal treatment effects in multiparous species Neurotoxicol Teratol 14 1992 221 228
32. C.W. Hughes Outcome of early experience studies as affected by between-litter variance J Nutr 109 1979 642 645
33. S.L. Andersen, and C.P. Navalta Altering the course of neurodevelopment: A framework for understanding the enduring effects of psychotropic drugs Int J Dev Neurosci 22 2004 423 440
34. L.P. Spear, and S.C. Brake Periadolescence: Age-dependent behavior and psychopharmacological responsivity in rats Dev Psychobiol 16 1983 83 109
35. L.P. Spear The adolescent brain and age-related behavioral manifestations Neurosci Biobehav Rev 24 2000 417 463
36. S.D. Iñiguez, B.L. Warren, E.M. Parise, L.F. Alcantara, B. Schuh, and M.L. Maffeo Nicotine exposure during adolescence induces a depression-like state in adulthood Neuropsychopharmacology 34 2009 1609 1624
37. B.L. Warren, V.F. Vialou, S.D. Iniguez, L.F. Alcantara, K.N. Wright, and J. Feng Neurobiological sequelae of witnessing stressful events in adult mice Biol Psychiatry 73 2013 7 14
38. C.A. Bolaños, M. Barrot, O. Berton, D. Wallace-Black, and E.J. Nestler Methylphenidate treatment during pre- and periadolescence alters behavioral responses to emotional stimuli at adulthood Biol Psychiatry 54 2003 1317 1329
39. C.A. Bolaños, M.D. Willey, M.L. Maffeo, K.D. Powers, D.W. Kinka, and K.B. Grausam Antidepressant treatment can normalize adult behavioral deficits induced by early-life exposure to methylphenidate Biol Psychiatry 63 2008 309 316
40. S.D. Iñiguez, B.L. Warren, R.L. Neve, E.J. Nestler, S.J. Russo, and C.A. Bolaños Guzmán Insulin receptor substrate-2 in the ventral tegmental area regulates behavioral responses to cocaine Behav Neurosci 122 2008 1172 1177
41. D.R. Nyholt A simple correction for multiple testing for single-nucleotide polymorphisms in linkage disequilibrium with each other Am J Hum Genet 74 2004 765 769
42. S.D. Iñiguez, B.L. Warren, and C.A. Bolaños-Guzmán Short- and long-term functional consequences of fluoxetine exposure during adolescence in male rats Biol Psychiatry 67 2010 1057 1066
43. R.D. Porsolt, M. Le Pichon, and M. Jalfre Depression: A new animal model sensitive to antidepressant treatments Nature 266 1977 730 732
44. J.F. Cryan, A. Markou, and I. Lucki Assessing antidepressant activity in rodents: Recent developments and future needs Trends Pharmacol Sci 23 2002 238 245
45. J.W. Murrough Ketamine as a novel antidepressant: From synapse to behavior Clin Pharmacol Ther 91 2012 303 309
46. M.N. Hill, K.G. Hellemans, P. Verma, B.B. Gorzalka, and J. Weinberg Neurobiology of chronic mild stress: Parallels to major depression Neurosci Biobehav Rev 36 2012 2085 2117
47. P. Willner, A. Towell, D. Sampson, S. Sophokleous, and R. Muscat Reduction of sucrose preference by chronic unpredictable mild stress, and its restoration by a tricyclic antidepressant Psychopharmacology (Berl) 93 1987 358 364
48. P. Willner Chronic mild stress (CMS) revisited: Consistency and behavioural-neurobiological concordance in the effects of CMS Neuropsychobiology 52 2005 90 110
49. M. Papp, P. Willner, and R. Muscat An animal model of anhedonia: Attenuation of sucrose consumption and place preference conditioning by chronic unpredictable mild stress Psychopharmacology (Berl) 104 1991 255 259
50. P. Willner, J.L. Moreau, C.K. Nielsen, M. Papp, and A. Sluzewska Decreased hedonic responsiveness following chronic mild stress is not secondary to loss of body weight Physiol Behav 60 1996 129 134
51. L.S. Garcia, C.M. Comim, S.S. Valvassori, G.Z. Reus, L.M. Barbosa, and A.C. Andreazza 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 2008 140 144
52. H. Koike, M. Iijima, and S. Chaki Involvement of AMPA receptor in both the rapid and sustained antidepressant-like effects of ketamine in animal models of depression Behav Brain Res 224 2011 107 111
53. L.S. Garcia, C.M. Comim, S.S. Valvassori, G.Z. Reus, L. Stertz, and F. Kapczinski Ketamine treatment reverses behavioral and physiological alterations induced by chronic mild stress in rats Prog Neuropsychopharmacol Biol Psychiatry 33 2009 450 455
54. J.M. Farah Jr, T.S. Rao, S.J. Mick, K.E. Coyne, and S. Iyengar N-methyl-D-aspartate treatment increases circulating adrenocorticotropin and luteinizing hormone in the rat Endocrinology 128 1991 1875 1880
55. H. Elvidge, J.R. Challis, J.S. Robinson, C. Roper, and G.D. Thorburn Influence of handling and sedation on plasma cortisol in rhesus monkeys (Macaca mulatta) J Endocrinol 70 1976 325 326
56. H.A. Adams, A. Thiel, A. Jung, G. Fengler, and G. Hempelmann Studies using S-(+)-ketamine on probands. Endocrine and circulatory reactions, recovery and dream experiences [article in German] Anaesthesist 41 1992 588 596
57. J.H. Broadbear, G. Winger, and J.H. Woods Self-administration of fentanyl, cocaine and ketamine: Effects on the pituitary-adrenal axis in rhesus monkeys Psychopharmacology (Berl) 176 2004 398 406
58. A.A. Sappington, G. Corssen, A.T. Becker, and M. Tavakoli Effects of ketamine on patient responsiveness during the various phases of a single induced anxiety session Ala J Med Sci 14 1977 121 124
59. S. Maeng, C.A. Zarate Jr, J. Du, R.J. Schloesser, J. McCammon, and G. Chen Cellular mechanisms underlying the antidepressant effects of ketamine: Role of alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptors Biol Psychiatry 63 2008 349 352
60. P. Cvrcek Side effects of ketamine in the long-term treatment of neuropathic pain Pain Med 9 2008 253 257
61. C. Venancio, A. Magalhaes, L. Antunes, and T. Summavielle Impaired spatial memory after ketamine administration in chronic low doses Curr Neuropharmacol 9 2011 251 255
62. F. Crews, J. He, and C. Hodge Adolescent cortical development: A critical period of vulnerability for addiction Pharmacol Biochem Behav 86 2007 189 199
63. G.L. Wenk, and C.A. Barnes Regional changes in the hippocampal density of AMPA and NMDA receptors across the lifespan of the rat Brain Res 885 2000 1 5
64. K. Hein The use of therapeutics in adolescence J Adolesc Health Care 8 1987 8 35
65. N. Li, B. Lee, R.J. Liu, M. Banasr, J.M. Dwyer, and M. Iwata mTOR-dependent synapse formation underlies the rapid antidepressant effects of NMDA antagonists Science 329 2010 959 964
66. B. Moghaddam, B. Adams, A. Verma, and D. Daly Activation of glutamatergic neurotransmission by ketamine: A novel step in the pathway from NMDA receptor blockade to dopaminergic and cognitive disruptions associated with the prefrontal cortex J Neurosci 17 1997 2921 2927
67. M. aan het Rot, K.A. Collins, J.W. Murrough, A.M. Perez, D.L. Reich, and D.S. Charney Safety and efficacy of repeated-dose intravenous ketamine for treatment-resistant depression Biol Psychiatry 67 2010 139 145
68. M. Liebrenz, R. Stohler, and A. Borgeat Repeated intravenous ketamine therapy in a patient with treatment-resistant major depression World J Biol Psychiatry 10 2009 640 643
69. L.S. Garcia, C.M. Comim, S.S. Valvassori, G.Z. Reus, A.C. Andreazza, and L. Stertz Chronic administration of ketamine elicits antidepressant-like effects in rats without affecting hippocampal brain-derived neurotrophic factor protein levels Basic Clin Pharmacol Toxicol 103 2008 502 506
70. S.L. Andersen Stimulants and the developing brain Trends Pharmacol Sci 26 2005 237 243
71. W.A. Carlezon Jr, S.D. Mague, and S.L. Andersen Enduring behavioral effects of early exposure to methylphenidate in rats Biol Psychiatry 54 2003 1330 1337
72. B.L. Warren, S.D. Iñiguez, L.F. Alcantara, K.N. Wright, E.M. Parise, and S.K. Weakley Juvenile administration of concomitant methylphenidate and fluoxetine alters behavioral reactivity to reward- and mood-related stimuli and disrupts ventral tegmental area gene expression in adulthood J Neurosci 31 2011 10347 10358
73. C.J. Morgan, and H.V. Curran Ketamine use: A review Addiction 107 2012 27 38
74. M. Coppola, and R. Mondola Methoxetamine: From drug of abuse to rapid-acting antidepressant Med Hypotheses 79 2012 504 507
75. D. Wood, A. Cottrell, S.C. Baker, J. Southgate, M. Harris, and S. Fulford Recreational ketamine: From pleasure to pain BJU Int 107 2011 1881 1884
76. K.A. Trujillo, J.J. Zamora, and K.P. Warmoth Increased response to ketamine following treatment at long intervals: Implications for intermittent use Biol Psychiatry 63 2008 178 183
77. Y. Uchihashi, H. Kuribara, T. Morita, and T. Fujita The repeated administration of ketamine induces an enhancement of its stimulant action in mice Jpn J Pharmacol 61 1993 149 151
78. P.W. Kalivas Recent understanding in the mechanisms of addiction Curr Psychiatry Rep 6 2004 347 351
79. T.E. Robinson, and K.C. Berridge Incentive-sensitization and addiction Addiction 96 2001 103 114
80. W.A. Carlezon Jr Place conditioning to study drug reward and aversion Methods Mol Med 84 2003 243 249
81. T.M. Tzschentke Measuring reward with the conditioned place preference paradigm: A comprehensive review of drug effects, recent progress and new issues Prog Neurobiol 56 1998 613 672
82. M.T. Bardo, and R.A. Bevins Conditioned place preference: What does it add to our preclinical understanding of drug reward? Psychopharmacology (Berl) 153 2000 31 43
83. C.A. Bolaños, and E.J. Nestler Neurotrophic mechanisms in drug addiction Neuromolecular Med 5 2004 69 83
84. T. Suzuki, T. Aoki, H. Kato, M. Yamazaki, and M. Misawa Effects of the 5-HT(3) receptor antagonist ondansetron on the ketamine- and dizocilpine-induced place preferences in mice Eur J Pharmacol 385 1999 99 102
85. E.L. van der Kam, J. De Vry, and T.M. Tzschentke 2-Methyl-6- (phenylethynyl)-pyridine (MPEP) potentiates ketamine and heroin reward as assessed by acquisition, extinction, and reinstatement of conditioned place preference in the rat Eur J Pharmacol 606 2009 94 101
86. F. Li, Q. Fang, Y. Liu, M. Zhao, D. Li, and J. Wang Cannabinoid CB(1) receptor antagonist rimonabant attenuates reinstatement of ketamine conditioned place preference in rats Eur J Pharmacol 589 2008 122 126
87. S.D. Iñiguez, B.L. Warren, E.M. Parise, L.F. Alcantara, B. Schuh, and M.L. Maffeo Nicotine exposure during adolescence induces a depression-like state in adulthood Neuropsychopharmacology 34 2009 1609 1624
88. S.D. Iñiguez, B.L. Warren, R.L. Neve, S.J. Russo, E.J. Nestler, and C.A. Bolaños Guzmán Viral-mediated expression of extracellular signal-regulated kinase-2 in the ventral tegmental area modulates behavioral responses to cocaine Behav Brain Res 214 2010 460 464
89. H.S. Cho, D.C. D'Souza, R. Gueorguieva, E.B. Perry, S. Madonick, and L.P. Karper Absence of behavioral sensitization in healthy human subjects following repeated exposure to ketamine Psychopharmacology (Berl) 179 2005 136 143
90. R. Machado-Vieira, G. Salvadore, N. Diazgranados, and C.A. Zarate Jr. Ketamine and the next generation of antidepressants with a rapid onset of action Pharmacol Ther 123 2009 143 150
91. R.C. Kessler, K.A. McGonagle, M. Swartz, D.G. Blazer, and C.B. Nelson Sex and depression in the National Comorbidity Survey. I: Lifetime prevalence, chronicity and recurrence J Affect Disord 29 1993 85 96
92. C.W. Cotman, D.T. Monaghan, and A.H. Ganong Excitatory amino acid neurotransmission: NMDA receptors and Hebb-type synaptic plasticity Annu Rev Neurosci 11 1988 61 80
93. A.H. Rezvani Involvement of the NMDA system in learning and memory E.D. Levin, J.J. Buccafusco, Animal Models of Cognitive Impairment 2006 CRC Press Boca Raton, FL
94. M. Moosavi, G. Yadollahi Khales, K. Rastegar, and A. Zarifkar The effect of sub-anesthetic and anesthetic ketamine on water maze memory acquisition, consolidation and retrieval Eur J Pharmacol 677 2012 107 110
95. C.J. Morgan, L. Muetzelfeldt, and H.V. Curran Ketamine use, cognition and psychological wellbeing: a comparison of frequent, infrequent and ex-users with polydrug and non-using controls Addiction 104 2009 77 87