Electrophysiological and behavioral responses to ketamine in mice with reduced Akt1 expression

Psychopharmacology

Volumn 227, Issue 4, 2013, Pages 639-649

  Featherstone, Robert E ^a   M tatard Leitman, Valerie ^a   Suh, Jimmy D ^a   Lin, Robert ^a   Lucki, Irwin ^a   Siegel, Steven J ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Drug abuse; ERSP; Evoked potential; Gamma; ITC; Ketamine; N100; P50; Schizophrenia; Theta

Indexed keywords

KETAMINE; PROTEIN KINASE B; UNCLASSIFIED DRUG; V AKT MURINE THYMOMA VIRAL ONCOGENE HOMOLOG 1 PROTEIN;

ACTION POTENTIAL; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; AUDITORY STIMULATION; BEHAVIOR CHANGE; CONTROLLED STUDY; DISEASE PREDISPOSITION; DRUG EXPOSURE; ELECTROENCEPHALOGRAPHY; EVENT RELATED POTENTIAL; GAMMA RHYTHM; GENE EXPRESSION REGULATION; GENOTYPE; INTERTRIAL COHERENCE; MALE; MOUSE; MOUSE MUTANT; N40 (S1-S2) DIFFERENCE; N40 AMPLITUDE; NERVOUS SYSTEM PARAMETERS; NONHUMAN; OSCILLATORY POTENTIAL; P20 (S1-S2) DIFFERENCE; P20 AMPLITUDE; PREPULSE INHIBITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCHIZOPHRENIA; STARTLE REFLEX; THETA RHYTHM; V AKT MURINE THYMOMA VIRAL ONCOGENE HOMOLOG 1 GENE; VIRUS ONCOGENE; WHITE NOISE; WILD TYPE;

ANIMALS; BEHAVIOR, ANIMAL; ELECTROENCEPHALOGRAPHY; EVOKED POTENTIALS; EXCITATORY AMINO ACID ANTAGONISTS; GENE EXPRESSION REGULATION; KETAMINE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROTO-ONCOGENE PROTEINS C-AKT; SCHIZOPHRENIA; STARTLE REACTION; THETA RHYTHM;

EID: 84878685909     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-013-2997-9     Document Type: Article

References (63)

1. Adler LE, Olincy A, Waldo M, Harris JG, Griffith J, Stevens K, Flach K, Nagamoto H, Bickford P, Leonard S, Freedman R (1998) Schizophrenia, sensory gating, and nicotinic receptors. Schizophr Bull 24:189-202
2. Balu DT, Carlson GC, Talbot K, Kazi H, Hill-Smith TE, Easton RM, Birnbaum MJ, Lucki I (2012) Akt1 deficiency in schizophrenia and impairment of hippocampal plasticity and function. Hippocampus 22:30-40
3. Behrens MM, Ali SS, Dao DN, Lucero J, Shekhtman G, Quick KL, Dugan LL (2007) Ketamine-induced loss of phenotype of fast-spiking interneurons is mediated by NADPH-oxidase. Science 318:1645-1647
4. Blasi G, Napolitano F, Ursini G, Taurisano P, Romano R, Caforio G, Fazio L, Gelao B, Di Giorgio A, Iacovelli L, Sinibaldi L, Popolizio T, Usiello A, Bertolino A (2012) DRD2/AKT1 interaction on D2 c-AMP independent signaling, attentional processing, and response to olanzapine treatment in schizophrenia. Proc Natl Acad Sci U S A 108:1158-1163
5. Boutros NN, Brockhaus-Dumke A, Gjini K, Vedeniapin A, Elfakhani M, Burroughs S, Keshavan M (2009) Sensory-gating deficit of the N100 mid-latency auditory evoked potential in medicated schizophrenia patients. Schizophr Res 113:339-346
6. Boutros NN, Korzyuko O, Oliwa G, Feingold A, Campbell D, McClain-Furmanski D, Struve F, Jansen BH (2004a) Morphological and latency abnormalities of the mid-latency auditory evoked responses in schizophrenia: a preliminary report. Schizophr Res 70:303-313
7. Boutros NN, Korzyukov O, Jansen B, Feingold A, Bell M (2004b) Sensory gating deficits during the mid-latency phase of information processing in medicated schizophrenia patients. Psychiatry Res 126:203-215
8. Braff DL, Grillon C, Geyer MA (1992) Gating and habituation of the startle reflex in schizophrenic patients. Arch Gen Psychiatry 49:206-215
9. Brenner CA, Kieffaber PD, Clementz BA, Johannesen JK, Shekhar A, O'Donnell BF, Hetrick WP (2009) Event-related potential abnormalities in schizophrenia: a failure to "gate in" salient information? Schizophr Res 113:332-338
10. Cao YA, Featherstone RE, Gandal MJ, Liang Y, Jutzeler C, Saunders J, Tatard-Leitman V, Chen J, Weinberger DR, Lerman C, Siegel SJ (2012) Nicotine normalizes event related potentials in COMT-Val-tg mice and increases gamma and theta spectral density. Behav Neurosci 126:332-343
11. Carlen M, Meletis K, Siegle JH, Cardin JA, Futai K, Vierling-Claassen D, Ruhlmann C, Jones SR, Deisseroth K, Sheng M, Moore CI, Tsai LH (2011) A critical role for NMDA receptors in parvalbumin interneurons for gamma rhythm induction and behavior. Mol Psychiatry 17:537-548
12. Chen YC, Chen YW, Hsu YF, Chang WT, Hsiao CK, Min MY, Lai WS (2012) Akt1 deficiency modulates reward learning and reward prediction error in mice. Genes Brain Behav 11:157-169
13. Cho H, Thorvaldsen JL, Chu Q, Feng F, Birnbaum MJ (2001) Akt1/PKB alpha is required for normal growth but dispensable for maintenance of glucose homeostasis in mice. J Biol Chem 276:38349-38352
14. Connolly PM, Maxwell C, Liang Y, Kahn JB, Kanes SJ, Abel T, Gur RE, Turetsky BI, Siegel SJ (2004) The effects of ketamine vary among inbred mouse strains and mimic schizophrenia for the P80, but not P20 or N40 auditory ERP components. Neurochem Res 29:1179-1188
15. de Bruin NM, Ellenbroek BA, Cools AR, Coenen AM, van Luijtelaar EL (1999) Differential effects of ketamine on gating of auditory evoked potentials and prepulse inhibition in rats. Psychopharmacology (Berl) 142:9-17
16. Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9-21
17. Di Forti M, Iyegbe C, Sallis H, Kolliakou A, Falcone MA, Paparelli A, Sirianni M, La Cascia C, Stilo SA, Marques TR, Handley R, Mondelli V, Dazzan P, Pariante C, David AS, Morgan C, Powell J, Murray RM (2012) Confirmation that the AKT1 (rs2494732) genotype influences the risk of psychosis in cannabis users. Biol Psychiatry 72:811-816
18. Doege K, Bates AT, White TP, Das D, Boks MP, Liddle PF (2009) Reduced event-related low frequency EEG activity in schizophrenia during an auditory oddball task. Psychophysiology 46:566-577
19. Ehrlichman RS, Gandal MJ, Maxwell CR, Lazarewicz MT, Finkel LH, Contreras D, Turetsky BI, Siegel SJ (2009) N-methyl-d-aspartic acid receptor antagonist-induced frequency oscillations in mice recreate pattern of electrophysiological deficits in schizophrenia. Neuroscience 158:705-712
20. Ehrlichman RS, Maxwell CR, Majumdar S, Siegel SJ (2008) Deviance-elicited changes in event-related potentials are attenuated by ketamine in mice. J Cogn Neurosci 20:1403-1414
21. Emamian ES, Hall D, Birnbaum MJ, Karayiorgou M, Gogos JA (2004) Convergent evidence for impaired AKT1-GSK3beta signaling in schizophrenia. Nat Genet 36:131-137
22. Erwin RJ, Turetsky BI, Moberg P, Gur RC, Gur RE (1998) P50 abnormalities in schizophrenia: relationship to clinical and neuropsychological indices of attention. Schizophr Res 33:157-167
23. Featherstone RE, Liang Y, Saunders JA, Tatard-Leitman VM, Ehrlichman RS, Siegel SJ (2012) Subchronic ketamine treatment leads to permanent changes in EEG, cognition and the astrocytic glutamate transporter EAAT2 in mice. Neurobiol Dis 47:338-346
24. Ford JM, Roach BJ, Hoffman RS, Mathalon DH (2008) The dependence of P300 amplitude on gamma synchrony breaks down in schizophrenia. Brain Res 1235:133-142
25. Freedman R, Adler LE, Waldo MC, Pachtman E, Franks RD (1983) Neurophysiological evidence for a defect in inhibitory pathways in schizophrenia: comparison of medicated and drug-free patients. Biol Psychiatry 18:537-551
26. Johannesen JK, Bodkins M, O'Donnell BF, Shekhar A, Hetrick WP (2008) Perceptual anomalies in schizophrenia co-occur with selective impairments in the gamma frequency component of midlatency auditory ERPs. J Abnorm Psychol 117:106-118
27. Kirihara K, Rissling AJ, Swerdlow NR, Braff DL, Light GA (2012) Hierarchical organization of gamma and theta oscillatory dynamics in schizophrenia. Biol Psychiatry 71:873-880
28. Klimesch W (1999) EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Res Brain Res Rev 29:169-195
29. Krystal JH, Karper LP, Seibyl JP, Freeman GK, Delaney R, Bremner JD, Heninger GR, Bowers MB Jr, Charney DS (1994) Subanesthetic effects of the noncompetitive NMDA antagonist, ketamine, in humans. Psychotomimetic, perceptual, cognitive, and neuroendocrine responses. Arch Gen Psychiatry 51:199-214
30. Kwon JS, O'Donnell BF, Wallenstein GV, Greene RW, Hirayasu Y, Nestor PG, Hasselmo ME, Potts GF, Shenton ME, McCarley RW (1999) Gamma frequency-range abnormalities to auditory stimulation in schizophrenia. Arch Gen Psychiatry 56:1001-1005
31. Lahti AC, Koffel B, LaPorte D, Tamminga CA (1995) Subanesthetic doses of ketamine stimulate psychosis in schizophrenia. Neuropsychopharmacology 13:9-19
32. Lahti AC, Weiler MA, Tamara Michaelidis BA, Parwani A, Tamminga CA (2001) Effects of ketamine in normal and schizophrenic volunteers. Neuropsychopharmacology 25:455-467
33. Lai WS, Xu B, Westphal KG, Paterlini M, Olivier B, Pavlidis P, Karayiorgou M, Gogos JA (2006) Akt1 deficiency affects neuronal morphology and predisposes to abnormalities in prefrontal cortex functioning. Proc Natl Acad Sci U S A 103:16906-16911
34. Lazarewicz MT, Ehrlichman RS, Maxwell CR, Gandal MJ, Finkel LH, Siegel SJ (2010) Ketamine modulates theta and gamma oscillations. J Cogn Neurosci 22:1452-1464
35. Light GA, Malaspina D, Geyer MA, Luber BM, Coleman EA, Sackeim HA, Braff DL (1999) Amphetamine disrupts P50 suppression in normal subjects. Biol Psychiatry 46:990-996
36. Lijffijt M, Lane SD, Meier SL, Boutros NN, Burroughs S, Steinberg JL, Moeller FG, Swann AC (2009) P50, N100, and P200 sensory gating: relationships with behavioral inhibition, attention, and working memory. Psychophysiology 46:1059-1068
37. Makeig S (1993) Auditory event-related dynamics of the EEG spectrum and effects of exposure to tones. Electroencephalogr Clin Neurophysiol 86:283-293
38. Malhotra AK, Pinals DA, Adler CM, Elman I, Clifton A, Pickar D, Breier A (1997) Ketamine-induced exacerbation of psychotic symptoms and cognitive impairment in neuroleptic-free schizophrenics. Neuropsychopharmacology 17:141-150
39. Malhotra AK, Pinals DA, Weingartner H, Sirocco K, Missar CD, Pickar D, Breier A (1996) NMDA receptor function and human cognition: the effects of ketamine in healthy volunteers. Neuropsychopharmacology 14:301-307
40. Maxwell CR, Ehrlichman RS, Liang Y, Trief D, Kanes SJ, Karp J, Siegel SJ (2006) Ketamine produces lasting disruptions in encoding of sensory stimuli. J Pharmacol Exp Ther 316:315-324
41. Maxwell CR, Kanes SJ, Abel T, Siegel SJ (2004a) Phosphodiesterase inhibitors: a novel mechanism for receptor-independent antipsychotic medications. Neuroscience 129:101-107
42. Maxwell CR, Liang Y, Weightman BD, Kanes SJ, Abel T, Gur RE, Turetsky BI, Bilker WB, Lenox RH, Siegel SJ (2004b) Effects of chronic olanzapine and haloperidol differ on the mouse N1 auditory evoked potential. Neuropsychopharmacology 29:739-746
43. Moghaddam B, Adams B, Verma A, Daly D (1997) 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 17:2921-2927
44. Neill JC, Barnes S, Cook S, Grayson B, Idris NF, McLean SL, Snigdha S, Rajagopal L, Harte MK (2010) Animal models of cognitive dysfunction and negative symptoms of schizophrenia: focus on NMDA receptor antagonism. Pharmacol Ther 128:419-432
45. Newcomer JW, Farber NB, Jevtovic-Todorovic V, Selke G, Melson AK, Hershey T, Craft S, Olney JW (1999) Ketamine-induced NMDA receptor hypofunction as a model of memory impairment and psychosis. Neuropsychopharmacology 20:106-118
46. Ohi K, Hashimoto R, Yasuda Y, Fukumoto M, Nemoto K, Ohnishi T, Yamamori H, Takahashi H, Iike N, Kamino K, Yoshida T, Azechi M, Ikezawa K, Tanimukai H, Tagami S, Morihara T, Okochi M, Tanaka T, Kudo T, Iwase M, Kazui H, Takeda M (2011) The AKT1 gene is associated with attention and brain morphology in schizophrenia. World J Biol Psychiatry. doi: 10.3109/15622975.2011.591826
47. Olney JW, Newcomer JW, Farber NB (1999) NMDA receptor hypofunction model of schizophrenia. J Psychiatr Res 33:523-533
48. Oranje B, Gispen-de Wied CC, Verbaten MN, Kahn RS (2002) Modulating sensory gating in healthy volunteers: the effects of ketamine and haloperidol. Biol Psychiatry 52:887-895
49. Phillips JM, Ehrlichman RS, Siegel SJ (2007) Mecamylamine blocks nicotine-induced enhancement of the P20 auditory event-related potential and evoked gamma. Neuroscience 144:1314-1323
50. Potter D, Summerfelt A, Gold J, Buchanan RW (2006) Review of clinical correlates of P50 sensory gating abnormalities in patients with schizophrenia. Schizophr Bull 32:692-700
51. Roach BJ, Mathalon DH (2008) Event-related EEG time-frequency analysis: an overview of measures and an analysis of early gamma band phase locking in schizophrenia. Schizophr Bull 34:907-926
52. Rudnick ND, Koehler C, Picciotto MR, Siegel SJ (2009) Role of beta2-containing nicotinic acetylcholine receptors in auditory event-related potentials. Psychopharmacology (Berl) 202:745-751
53. Siegel SJ, Connolly P, Liang Y, Lenox RH, Gur RE, Bilker WB, Kanes SJ, Turetsky BI (2003) Effects of strain, novelty, and NMDA blockade on auditory-evoked potentials in mice. Neuropsychopharmacology 28:675-682
54. Siegel SJ, Maxwell CR, Majumdar S, Trief DF, Lerman C, Gur RE, Kanes SJ, Liang Y (2005) Monoamine reuptake inhibition and nicotine receptor antagonism reduce amplitude and gating of auditory evoked potentials. Neuroscience 133:729-738
55. Smith AK, Edgar JC, Huang M, Lu BY, Thoma RJ, Hanlon FM, McHaffie G, Jones AP, Paz RD, Miller GA, Canive JM (2010) Cognitive abilities and 50- and 100-msec paired-click processes in schizophrenia. Am J Psychiatry 167:1264-1275
56. Stevens KE, Meltzer J, Rose GM (1995) Nicotinic cholinergic normalization of amphetamine-induced loss of auditory gating in freely moving rats. Psychopharmacology (Berl) 119:163-170
57. Szamosi A, Kelemen O, Keri S (2012) Hippocampal volume and the AKT signaling system in first-episode schizophrenia. J Psychiatr Res 46:279-284
58. Tan HY, Chen AG, Chen Q, Browne LB, Verchinski B, Kolachana B, Zhang F, Apud J, Callicott JH, Mattay VS, Weinberger DR (2011) Epistatic interactions of AKT1 on human medial temporal lobe biology and pharmacogenetic implications. Mol Psychiatry 17:1007-1016
59. Tan HY, Nicodemus KK, Chen Q, Li Z, Brooke JK, Honea R, Kolachana BS, Straub RE, Meyer-Lindenberg A, Sei Y, Mattay VS, Callicott JH, Weinberger DR (2008) Genetic variation in AKT1 is linked to dopamine-associated prefrontal cortical structure and function in humans. J Clin Invest 118:2200-2208
60. Turetsky BI, Bilker WB, Siegel SJ, Kohler CG, Gur RE (2009) Profile of auditory information-processing deficits in schizophrenia. Psychiatry Res 165:27-37
61. van Berckel BN, Oranje B, van Ree JM, Verbaten MN, Kahn RS (1998) The effects of low dose ketamine on sensory gating, neuroendocrine secretion and behavior in healthy human subjects. Psychopharmacology (Berl) 137:271-281
62. van Winkel R, van Beveren NJ, Simons C (2011) AKT1 moderation of cannabis-induced cognitive alterations in psychotic disorder. Neuropsychopharmacology 36:2529-2537
63. Wan M, Easton RM, Gleason CE, Monks BR, Ueki K, Kahn CR, Birnbaum MJ (2012) Loss of Akt1 in mice increases energy expenditure and protects against diet-induced obesity. Mol Cell Biol 32:96-106