Delayed emergence of behavioral and electrophysiological effects following juvenile ketamine exposure in mice

Translational Psychiatry

Volumn 5, Issue 9, 2015, Pages

  Nagy, L R ^a   Featherstone, R E ^a   Hahn, C G ^a   Siegel, S J ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KETAMINE; AMINO ACID RECEPTOR BLOCKING AGENT;

ACTION POTENTIAL AMPLITUDE; ADOLESCENT; ADOLESCENT BEHAVIOR; ADULT; ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUDITORY STIMULATION; BRAIN ELECTROPHYSIOLOGY; COGNITIVE DEVELOPMENT; CONTROLLED STUDY; DRUG ABUSE; ELECTROENCEPHALOGRAPHY; EVENT RELATED POTENTIAL; MALE; MOUSE; NONHUMAN; RADIAL ARM MAZE TEST; SOCIAL BEHAVIOR; SOCIAL INTERACTION; SPATIAL MEMORY; THETA RHYTHM; WORKING MEMORY; ANIMAL; ANIMAL BEHAVIOR; AUDITORY EVOKED POTENTIAL; BRAIN; C57BL MOUSE; CHEMICALLY INDUCED; COGNITION; COGNITIVE DEFECT; DISEASE MODEL; DRUG EFFECTS; PATHOPHYSIOLOGY; REACTION TIME; SHORT TERM MEMORY; STATISTICS AND NUMERICAL DATA; TIME FACTOR;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; COGNITION; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; ELECTROENCEPHALOGRAPHY; EVOKED POTENTIALS, AUDITORY; EXCITATORY AMINO ACID ANTAGONISTS; KETAMINE; MALE; MEMORY, SHORT-TERM; MICE; MICE, INBRED C57BL; REACTION TIME; TIME FACTORS;

EID: 84990876405     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2015.111     Document Type: Article

References (77)

1. US Department of Justice, Drug Enforcement Administration. Drugs of Abuse: A DEA Resource Guide. Drug Enforcement Administration: Springfield, VA, 2011 edn. 2011.
2. Archer JR, Dargan PI, Hudson S, Wood DM. Analysis of anonymous pooled urine from portable urinals in central London confirms the significant use of novel psychoactive substances. QJM 2013; 106: 147-152.
3. Lua AC, Lin HR, Tseng YT, Hu AR, Yeh PC. Profiles of urine samples from participants at rave party in Taiwan: Prevalence of ketamine and MDMA abuse. Forensic Sci Int 2003; 136: 47-51.
4. World Health Organization (WHO). Ketamine: Expert Peer Review on Critical Review Report. WHO: Hammamet, Tunisia, June 4-8, 2012. 35th ECDD Agenda Item 422012.
5. Tang WK, Liang HJ, Lau CG, Tang A, Ungvari GS. Relationship between cognitive impairment and depressive symptoms in current ketamine users. J Stud Alcohol Drugs 2012; 73: 460-468.
6. Torjesen I. Ketamine helps a third of patients with treatment resistant depression, finds small UK study. BMJ 2014; 348: G2576.
7. Price RB, Iosifescu DV, Murrough JW, Chang LC, Al Jurdi RK, Iqbal SZ et al. Effects of ketamine on explicit and implicit suicidal cognition: A randomized controlled trial in treatment-resistant depression. Depress Anxiety 2014; 31: 335-343.
8. Jeevakumar V, Driskill C, Paine A, Sobhanian M, Vakil H, Morris B et al. Ketamine administration during the second postnatal week induces enduring schizophrenia-like behavioral symptoms and reduces parvalbumin expression in the medial prefrontal cortex of adult mice. Behav Brain Res 2015; 282: 165-175.
9. Xu K, Krystal JH, Ning Y, Chen da C, He H, Wang D et al. Preliminary analysis of positive and negative syndrome scale in ketamine-associated psychosis in comparison with schizophrenia. J Psychiatr Res 2015; 61: 64-72.
10. Zugno AI, Juliao RF, Budni J, Volpato AM, Fraga DB, Pacheco FD et al. Rivastigmine reverses cognitive deficit and acetylcholinesterase activity induced by ketamine in an animal model of schizophrenia. Metab Brain Dis 2013; 28: 501-508.
11. Frohlich J, Van Horn JD. Reviewing the ketamine model for schizophrenia. J Psychopharmacol 2014; 28: 287-302.
12. Featherstone RE, Nagy LR, Hahn CG, Siegel SJ. Juvenile exposure to ketamine causes delayed emergence of EEG abnormalities during adulthood in mice. Drug Alcohol Depend 2014; 134: 123-127.
13. Featherstone RE, Liang Y, Saunders JA, Tatard-Leitman VM, Ehrlichman RS, Siegel SJ. Subchronic ketamine treatment leads to permanent changes in EEG, cognition and the astrocytic glutamate transporter EAAT2 in mice. Neurobiol Dis 2012; 47: 338-346.
14. Jeevakumar V, Kroener S. Ketamine administration during the second postnatal week alters synaptic properties of fast-spiking interneurons in the medial prefrontal cortex of adult mice. Cereb Cortex 2014; 282: 165-175.
15. Morgan CJ, Muetzelfeldt L, Curran HV. Ketamine use, cognition and psychological wellbeing: A comparison of frequent, infrequent and ex-users with polydrug and non-using controls. Addiction 2009; 104: 77-87.
16. Morgan CJ, Muetzelfeldt L, Curran HV. Consequences of chronic ketamine self-administration upon neurocognitive function and psychological wellbeing: A 1-year longitudinal study. Addiction 2010; 105: 121-133.
17. Venancio C, Magalhaes A, Antunes L, Summavielle T. Impaired spatial memory after ketamine administration in chronic low doses. Curr Neuropharmacol 2011; 9: 251-255.
18. Hiyoshi T, Hikichi H, Karasawa J, Chaki S. Metabotropic glutamate receptors regulate cortical gamma hyperactivities elicited by ketamine in rats. Neurosci Lett 2014; 567: 30-34.
19. Morgan CJ, Duffin S, Hunt S, Monaghan L, Mason O, Curran HV. Neurocognitive function and schizophrenia-proneness in individuals dependent on ketamine, on high potency cannabis ('skunk') or on cocaine. Pharmacopsychiatry 2012; 45: 269-274.
20. van Nimwegen L, de Haan L, van Beveren N, van den Brink W, Linszen D. [Adolescence, schizophrenia and drug abuse: Interactive vulnerability. A hypothesis]. Tijdschr Psychiatr 2007; 49: 169-178.
21. Squeglia LM, Jacobus J, Tapert SF. The influence of substance use on adolescent brain development. Clin EEG Neurosci 2009; 40: 31-38.
22. Fredriksson A, Ponten E, Gordh T, Eriksson P. Neonatal exposure to a combination of N-methyl-D-aspartate and gamma-aminobutyric acid type A receptor anesthetic agents potentiates apoptotic neurodegeneration and persistent behavioral deficits. Anesthesiology 2007; 107: 427-436.
23. Huang L, Liu Y, Jin W, Ji X, Dong Z. Ketamine potentiates hippocampal neurodegeneration and persistent learning and memory impairment through the PKCgamma-ERK signaling pathway in the developing brain. Brain Res 2012; 1476: 164-171.
24. Paule MG, Li M, Allen RR, Liu F, Zou X, Hotchkiss C et al. Ketamine anesthesia during the first week of life can cause long-lasting cognitive deficits in rhesus monkeys. Neurotoxicol Teratol 2011; 33: 220-230.
25. Young C, Jevtovic-Todorovic V, Qin YQ, Tenkova T, Wang H, Labruyere J et al. Potential of ketamine and midazolam, individually or in combination, to induce apoptotic neurodegeneration in the infant mouse brain. Br J Pharmacol 2005; 146: 189-197.
26. Scallet AC, Schmued LC, Slikker W Jr, Grunberg N, Faustino PJ, Davis H et al. Developmental neurotoxicity of ketamine: Morphometric confirmation, exposure parameters, and multiple fluorescent labeling of apoptotic neurons. Toxicol Sci 2004; 81: 364-370.
27. Zou X, Patterson TA, Sadovova N, Twaddle NC, Doerge DR, Zhang X et al. Potential neurotoxicity of ketamine in the developing rat brain. Toxicol Sci 2009; 108: 149-158.
28. Jin J, Gong K, Zou X, Wang R, Lin Q, Chen J. The blockade of NMDA receptor ion channels by ketamine is enhanced in developing rat cortical neurons. Neurosci Lett 2013; 539: 11-15.
29. Green SM, Rothrock SG, Harris T, Hopkins GA, Garrett W, Sherwin T. Intravenous ketamine for pediatric sedation in the emergency department: Safety profile with 156 cases. Acad Emerg Med 1998; 5: 971-976.
30. Green SM, Rothrock SG, Lynch EL, Ho M, Harris T, Hestdalen R et al. Intramuscular ketamine for pediatric sedation in the emergency department: Safety profile in 1,022 cases. Ann Emerg Med 1998; 31: 688-697.
31. Green SM, Krauss B. Clinical practice guideline for emergency department ketamine dissociative sedation in children. Ann Emerg Med 2004; 44: 460-471.
32. Craven R. Ketamine. Anaesthesia 2007; 62: 48-53.
33. Petrack EM, Marx CM, Wright MS. Intramuscular ketamine is superior to meperidine, promethazine, and chlorpromazine for pediatric emergency department sedation. Arch Pediatr Adolesc Med 1996; 150: 676-681.
34. Chen GH, Wang YJ, Wang XM, Zhou JN. Accelerated senescence prone mouse-8 shows early onset of deficits in spatial learning and memory in the radial six-arm water maze. Physiol Behav 2004; 82: 883-890.
35. Shukitt-Hale B, McEwen JJ, Szprengiel A, Joseph JA. Effect of age on the radial arm water maze-A test of spatial learning and memory. Neurobiol Aging 2004; 25: 223-229.
36. Kim S, Pickup S, Fairless AH, Ittyerah R, Dow HC, Abel T et al. Association between sociability and diffusion tensor imaging in BALB/cJ mice. NMR Biomed 2012; 25: 104-112.
37. Sankoorikal GM, Kaercher KA, Boon CJ, Lee JK, Brodkin ES. A mouse model system for genetic analysis of sociability: C57BL/6J versus BALB/cJ inbred mouse strains. Biol Psychiatry 2006; 59: 415-423.
38. Fairless AH, Shah RY, Guthrie AJ, Li H, Brodkin ES. Deconstructing sociability, an autism-relevant phenotype, in mouse models. Anat Rec (Hoboken) 2011; 294: 1713-1725.
39. Uhlhaas PJ, Singer W. The development of neural synchrony and large-scale cortical networks during adolescence: Relevance for the pathophysiology of schizophrenia and neurodevelopmental hypothesis. Schizophr Bull 2011; 37: 514-523.
40. Uhlhaas PJ, Roux F, Rodriguez E, Rotarska-Jagiela A, Singer W. Neural synchrony and the development of cortical networks. Trends Cogn Sci 2010; 14: 72-80.
41. Uhlhaas PJ, Singer W. Neural synchrony in brain disorders: Relevance for cognitive dysfunctions and pathophysiology. Neuron 2006; 52: 155-168.
42. Lazarewicz MT, Ehrlichman RS, Maxwell CR, Gandal MJ, Finkel LH, Siegel SJ. Ketamine modulates theta and gamma oscillations. J Cogn Neurosci 2010; 22: 1452-1464.
43. Ehrlichman RS, Gandal MJ, Maxwell CR, Lazarewicz MT, Finkel LH, Contreras D et al. N-methyl-d-aspartic acid receptor antagonist-induced frequency oscillations in mice recreate pattern of electrophysiological deficits in schizophrenia. Neuroscience 2009; 158: 705-712.
44. Featherstone RE, MT-L V, Suh JD, Lin R, Lucki I, Siegel SJ. Electrophysiological and behavioral responses to ketamine in mice with reduced Akt1 expression. Psychopharmacology (Berl) 2013; 227: 639-649.
45. Saunders JA, Gandal MJ, Roberts TP, Siegel SJ. NMDA antagonist MK801 recreates auditory electrophysiology disruption present in autism and other neurodevelopmental disorders. Behav Brain Res 2012; 234: 233-237.
46. Saunders JA, Gandal MJ, Siegel SJ. NMDA antagonists recreate signal-to-noise ratio and timing perturbations present in schizophrenia. Neurobiol Dis 2012; 46: 93-100.
47. Tesche CD, Karhu J. Theta oscillations index human hippocampal activation during a working memory task. Proc Natl Acad Sci USA 2000; 97: 919-924.
48. Poch C, Fuentemilla L, Barnes GR, Duzel E. Hippocampal theta-phase modulation of replay correlates with configural-relational short-term memory performance. J Neurosci 2011; 31: 7038-7042.
49. Fuentemilla L, Penny WD, Cashdollar N, Bunzeck N, Duzel E. Theta-coupled periodic replay in working memory. Curr Biol 2010; 20: 606-612.
50. Duzel E, Penny WD, Burgess N. Brain oscillations and memory. Curr Opin Neurobiol 2010; 20: 143-149.
51. Guderian S, Duzel E. Induced theta oscillations mediate large-scale synchrony with mediotemporal areas during recollection in humans. Hippocampus 2005; 15: 901-912.
52. Monte AS, de Souza GC, McIntyre RS, Soczynska JK, dos Santos JV, Cordeiro RC et al. Prevention and reversal of ketamine-induced schizophrenia related behavior by minocycline in mice: Possible involvement of antioxidant and nitrergic pathways. J Psychopharmacol 2013; 27: 1032-1043.
53. Bian SZ, Liu WL, Zhang ZX, Gu ZL, Jiang XG, Guo CY. [The correlation between ketamine-induced schizophrenia-like signs in mice and the expressions of NRG1, ErbB4 mRNA]. Fa Yi Xue Za Zhi. Fa Yi Xue Za Zhi 2009; 25: 348-351, 358.
54. Gandal MJ, Edgar JC, Klook K, Siegel SJ. Gamma synchrony: Towards a translational biomarker for the treatment-resistant symptoms of schizophrenia. Neuropharmacology 2012; 62: 1504-1518.
55. Jeffrey M, Lang M, Gane J, Wu C, Burnham WM, Zhang L. A reliable method for intracranial electrode implantation and chronic electrical stimulation in the mouse brain. BMC Neurosci 2013; 14: 82.
56. Wu C, Wais M, Sheppy E, del Campo M, Zhang L. A glue-based, screw-free method for implantation of intra-cranial electrodes in young mice. J Neurosci Methods 2008; 171: 126-131.
57. Roach BJ, Mathalon DH. Event-related EEG time-frequency analysis: An overview of measures and an analysis of early gamma band phase locking in schizophrenia. Schizophr Bull 2008; 34: 907-926.
58. Brodkin ES, Hagemann A, Nemetski SM, Silver LM. So cial approach-avoidance behavior of inbred mouse strains towards DBA/2 mice. Brain Res 2004; 1002: 151-157.
59. Semple BD, Blomgren K, Gimlin K, Ferriero DM, Noble-Haeusslein LJ. Brain development in rodents and humans: Identifying benchmarks of maturation and vulnerability to injury across species. Prog Neurobiol 2013; 106-107: 1-16.
60. Ebert A, Haussleiter IS, Juckel G, Brune M, Roser P. Impaired facial emotion recognition in a ketamine model of psychosis. Psychiatry Res 2012; 200: 724-727.
61. Moy SS, Nonneman RJ, Shafer GO, Nikolova VD, Riddick NV, Agster KL et al. Disruption of social approach by MK-801, amphetamine, and fluoxetine in adolescent C57BL/6J mice. Neurotoxicol Teratol 2013; 36: 36-46.
62. Kohler CG, Bilker W, Hagendoorn M, Gur RE, Gur RC. Emotion recognition deficit in schizophrenia: Association with symptomatology and cognition. Biol Psychiatry 2000; 48: 127-136.
63. Sachs G, Steger-Wuchse D, Kryspin-Exner I, Gur RC, Katschnig H. Facial recognition deficits and cognition in schizophrenia. Schizophr Res 2004; 68: 27-35.
64. Gresack JE, Frick KM. Male mice exhibit better spatial working and reference memory than females in a water-escape radial arm maze task. Brain Res 2003; 982: 98-107.
65. Fine JM, Baillargeon AM, Renner DB, Hoerster NS, Tokarev J, Colton S et al. Intranasal deferoxamine improves performance in radial arm water maze, stabilizes HIF-1alpha, and phosphorylates GSK3beta in P301L tau transgenic mice. Exp Brain Res 2012; 219: 381-390.
66. Kiang M, Braff DL, Sprock J, Light GA. The relationship between preattentive sensory processing deficits and age in schizophrenia patients. Clin Neurophysiol 2009; 120: 1949-1957.
67. Turetsky BI, Dress EM, Braff DL, Calkins ME, Green MF, Greenwood TA et al. The utility of P300 as a schizophrenia endophenotype and predictive biomarker: Clinical and socio-demographic modulators in COGS-2. Schizophr Res 2015; 163: 53-62.
68. Light GA, Swerdlow NR. Future clinical uses of neurophysiological biomarkers to predict and monitor treatment response for schizophrenia. Ann NY Acad Sci 2015; 1344: 105-119.
69. Light GA, Swerdlow NR, Thomas ML, Calkins ME, Green MF, Greenwood TA et al. Validation of mismatch negativity and P3a for use in multi-site studies of schizophrenia: Characterization of demographic, clinical, cognitive, and functional correlates in COGS-2. Schizophr Res 2015; 163: 63-72.
70. Basar E, Basar-Eroglu C, Karakas S, Schurmann M. Gamma, alpha, delta, and theta oscillations govern cognitive processes. Int J Psychophysiol 2001; 39: 241-248.
71. Kemp IR, Kaada BR. The relation of hippocampal theta activity to arousal, attentive behaviour and somato-motor movements in unrestrained cats. Brain Res 1975; 95: 323-342.
72. Neill JC, Barnes S, Cook S, Grayson B, Idris NF, McLean SL et al. Animal models of cognitive dysfunction and negative symptoms of schizophrenia: Focus on NMDA receptor antagonism. Pharmacol Ther 2010; 128: 419-432.
73. Anderer P, Semlitsch HV, Saletu B. Multichannel auditory event-related brain potentials: Effects of normal aging on the scalp distribution of N1, P2, N2 and P300 latencies and amplitudes. Electroencephalogr Clin Neurophysiol 1996; 99: 458-472.
74. Crowley KE, Colrain IM. A review of the evidence for P2 being an independent component process: Age, sleep and modality. Clin Neurophysiol 2004; 115: 732-744.
75. Garcia-Larrea L, Lukaszewicz AC, Mauguiere F. Revisiting the oddball paradigm. Non-target vs neutral stimuli and the evaluation of ERP attentional effects. Neuropsychologia 1992; 30: 723-741.
76. Bodatsch M, Klosterkotter J, Daumann J. Contributions of experimental psychiatry to research on the psychosis prodrome. Front Psychiatry 2013; 4: 170.
77. Banerjee A, Wang HY, Borgmann-Winter KE, MacDonald ML, Kaprielian H, Stucky A et al. Src kinase as a mediator of convergent molecular abnormalities leading to NMDAR hypoactivity in schizophrenia. Mol Psychiatry 2014; 20: 1091-1100.