Differential effects produced by ketamine on oscillatory activity recorded in the rat hippocampus, dorsal striatum and nucleus accumbens

Journal of Psychopharmacology

Volumn 25, Issue 6, 2011, Pages 808-821

  Hunt, Mark J ^a   Falinska, Monika ^a   Łȩski, Szymon ^a   Wójcik, Daniel K ^a   Kasicki, Stefan ^a  

^a NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

Author keywords

Hippocampus; ketamine; nucleus accumbens; schizophrenia; synchronization

Indexed keywords

KETAMINE;

ANIMAL EXPERIMENT; ARTICLE; BRAIN REGION; CONTROLLED STUDY; CORPUS STRIATUM; DELTA RHYTHM; DRUG EFFECT; ELECTROENCEPHALOGRAM; GAMMA RHYTHM; HIPPOCAMPUS; MALE; MOTOR ACTIVITY; NONHUMAN; NUCLEUS ACCUMBENS; OSCILLATORY POTENTIAL; PRIORITY JOURNAL; RAT;

ANIMALS; BRAIN WAVES; CORPUS STRIATUM; EXCITATORY AMINO ACID ANTAGONISTS; HIPPOCAMPUS; KETAMINE; MALE; NUCLEUS ACCUMBENS; RATS; RATS, WISTAR;

EID: 79960528357     PISSN: 02698811     EISSN: 14617285     Source Type: Journal    
DOI: 10.1177/0269881110362126     Document Type: Article

References (76)

1. Berke JD The Basal Ganglia VIII. Bolam JP Ingham CA Magill PJ, ed. New York: Springer ; 2006: 25-35.
2. Berke JD, Okatan M, Skurski J, Eichenbaum HB. Oscillatory entrainment of striatal neurons in freely moving rats. Neuron. 2004 ; 43: 883-896 (Pubitemid 39215018)
3. Boyer P, Phillips JL, Rousseau FL, Ilivitsky S. Hippocampal abnormalities and memory deficits: new evidence of a strong pathophysiological link in schizophrenia. Brain Res Rev. 2007 ; 54: 92-112 (Pubitemid 46509660)
4. Brovelli A, Ding M, Ledberg A, Chen Y, Nakamura R, Bressler SL. Beta oscillations in a large-scale sensorimotor cortical network: directional influences revealed by Granger causality. Proc Natl Acad Sci USA. 2004 ; 101: 9849-9854 (Pubitemid 38869325)
5. Brown P, Oliviero A, Mazzone P, Insola A, Tonali P, Di Lazzaro V. Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson's disease. J Neurosci. 2001 ; 21: 1033-1038 (Pubitemid 32163143)
6. Buzsaki G. Hippocampal sharp waves: their origin and significance. Brain Res. 1986 ; 398: 242-252 (Pubitemid 17210167)
7. Buzsaki G, Chen LS, Gage FH. Spatial organization of physiological activity in the hippocampal region: relevance to memory formation. Prog Brain Res. 1990 ; 83: 257-268 (Pubitemid 20205285)
8. Buzsaki G, Leung LW, Vanderwolf CH. Cellular bases of hippocampal EEG in the behaving rat. Brain Res. 1983 ; 287: 139-171 (Pubitemid 14230350)
9. Canolty RT, Edwards E, Dalal SS, et al. High gamma power is phase-locked to theta oscillations in human neocortex. Science. 2006 ; 313: 1626-1628 (Pubitemid 44414034)
10. Chrobak JJ, Buzsaki G. High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat. J Neurosci. 1996 ; 16: 3056-3066
11. Chrobak JJ, Lorincz A, Buzsaki G. Physiological patterns in the hippocampo-entorhinal cortex system. Hippocampus. 2000 ; 10: 457-465
12. Cohen MX, Axmacher N, Lenartz D, Elger CE, Sturm V, Schlaepfer TE. Good vibrations: cross-frequency coupling in the human nucleus accumbens during reward processing. J Cogn Neurosci. 2009 ; 21: 875-889
13. Crone NE, Sinai A, Korzeniewska A. High-frequency gamma oscillations and human brain mapping with electrocorticography. Prog Brain Res. 2006 ; 159: 275-295 (Pubitemid 44634651)
14. Csicsvari J, Hirase H, Czurko A, Buzsaki G. Reliability and state dependence of pyramidal cell-interneuron synapses in the hippocampus: an ensemble approach in the behaving rat. Neuron. 1998 ; 21: 179-189 (Pubitemid 28355702)
15. Cunningham MO, Hunt J, Middleton S, et al. Region-specific reduction in entorhinal gamma oscillations and parvalbumin-immunoreactive neurons in animal models of psychiatric illness. J Neurosci. 2006 ; 26: 2767-2776 (Pubitemid 43357860)
16. Darbin O, Newton L, Wichmann T. A new probe to monitor the effects of drugs on local field potentials. J Neurosci Methods. 2006 ; 155: 291-295
17. DeCoteau WE, Thorn C, Gibson DJ, et al. Oscillations of local field potentials in the rat dorsal striatum during spontaneous and instructed behaviors. J Neurophysiol. 2007 ; 97: 3800-3805 (Pubitemid 47084789)
18. Draguhn A, Traub RD, Bibbig A, Schmitz D. Ripple (approximately 200-Hz) oscillations in temporal structures. J Clin Neurophysiol. 2000 ; 17: 361-376
19. Enomoto T, Floresco SB. Disruptions in spatial working memory, but not short-term memory, induced by repeated ketamine exposure. Prog Neuropsychopharmacol Biol Psychiatry. 2009 ; 33: 668-675
20. Finnerty GT, Jefferys JG. 9-16 Hz oscillation precedes secondary generalization of seizures in the rat tetanus toxin model of epilepsy. J Neurophysiol. 2000 ; 83: 2217-2226 (Pubitemid 30198675)
21. Fogelson N, Williams D, Tijssen M, van BG, Speelman H, Brown P. Different functional loops between cerebral cortex and the subthalmic area in Parkinson's disease. Cereb Cortex. 2006 ; 16: 64-75 (Pubitemid 41746731)
22. Freedman R, Goldowitz D. Studies on the hippocampal formation: from basic development to clinical applications: studies on schizophrenia. Prog Neurobiol. 2009 ;:
23. Girardeau G, Benchenane K, Wiener SI, Buzsaki G, Zugaro MB. Selective suppression of hippocampal ripples impairs spatial memory. Nat Neurosci. 2009 ; 12: 1222-1223
24. Glasgow SD, Chapman CA. Local generation of theta-frequency EEG activity in the parasubiculum. J Neurophysiol. 2007 ; 97: 3868-3879 (Pubitemid 47080623)
25. Grace AA. Gating of information flow within the limbic system and the pathophysiology of schizophrenia. Brain Res Brain Res Rev. 2000 ; 31: 330-341 (Pubitemid 30136188)
26. Gruber AJ, O'Donnell P. Bursting activation of prefrontal cortex drives sustained up states in nucleus accumbens spiny neurons in vivo. Synapse. 2009 ; 63: 173-180
27. Hakami T, Jones NC, Tolmacheva EA, et al. NMDA receptor hypofunction leads to generalized and persistent aberrant gamma oscillations independent of hyperlocomotion and the state of consciousness. PLoS One. 2009 ; 4: e6755 - e6755
28. Herrmann CS, Demiralp T. Human EEG gamma oscillations in neuropsychiatric disorders. Clin Neurophysiol. 2005 ; 116: 2719-2733 (Pubitemid 41714021)
29. Homayoun H, Moghaddam B. Fine-tuning of awake prefrontal cortex neurons by clozapine: comparison with haloperidol and N-desmethylclozapine. Biol Psychiatry. 2007 ; 61: 679-687 (Pubitemid 46328858)
30. Hong LE, Summerfelt A, Buchanan RW, et al. Gamma and delta neural oscillations and association with clinical symptoms under subanesthetic ketamine. Neuropsychopharmacology. 2010 ; 35 (3). 632-640
31. Hunt MJ, Falinska M, Kasicki S. Local injection of MK801 modifies oscillatory activity in the nucleus accumbens in awake rats. J Psychopharmacol. 2010 ; 24: 931-941
32. Hunt MJ, Garcia R, Large CH, Kasicki S. Modulation of high-frequency oscillations associated with NMDA receptor hypofunction in the rodent nucleus accumbens by lamotrigine. Prog Neuropsychopharmacol Biol Psychiatry. 2008 ; 32: 1312-1319
33. Hunt MJ, Kessal K, Garcia R. Ketamine induces dopamine-dependent depression of evoked hippocampal activity in the nucleus accumbens in freely moving rats. J Neurosci. 2005 ; 25: 524-531 (Pubitemid 40105625)
34. Hunt MJ, Matulewicz P, Gottesmann C, Kasicki S. State-dependent changes in high-frequency oscillations recorded in the rat nucleus accumbens. Neuroscience. 2009b ; 164: 380-386
35. Hunt MJ, Raynaud B, Garcia R. Ketamine dose-dependently induces high-frequency oscillations in the nucleus accumbens in freely moving rats. Biol Psychiatry. 2006 ; 60: 1206-1214 (Pubitemid 44693529)
36. Jackson ME, Homayoun H, Moghaddam B. NMDA receptor hypofunction produces concomitant firing rate potentiation and burst activity reduction in the prefrontal cortex. Proc Natl Acad Sci USA. 2004 ; 101: 8467-8472 (Pubitemid 38736598)
37. Jones MS, Barth DS. Spatiotemporal organization of fast (>200 Hz) electrical oscillations in rat Vibrissa/Barrel cortex. J Neurophysiol. 1999 ; 82: 1599-1609 (Pubitemid 29439721)
38. Kelley AE, Domesick VB. The distribution of the projection from the hippocampal formation to the nucleus accumbens in the rat: an anterograde- and retrograde-horseradish peroxidase study. Neuroscience. 1982 ; 7: 2321-2335 (Pubitemid 12004419)
39. Krystal JH, Karper LP, Seibyl JP, et al. Subanesthetic effects of the noncompetitive NMDA antagonist, ketamine, in humans. Psychotomimetic, perceptual, cognitive, and neuroendocrine responses. Arch Gen Psychiatry. 1994 ; 51: 199-214 (Pubitemid 24081509)
40. Lahti AC, Koffel B, LaPorte D, Tamminga CA. Subanesthetic doses of ketamine stimulate psychosis in schizophrenia. Neuropsychopharmacology. 1995 ; 13: 9-19
41. Large CH, Webster EL, Goff DC. The potential role of lamotrigine in schizophrenia. Psychopharmacology (Berl). 2005 ; 181: 415-436 (Pubitemid 41480891)
42. Leski S, Wojcik DK, Tereszczuk J, Swiejkowski DA, Kublik E, Wrobel A. Inverse current-source density method in 3D: reconstruction fidelity, boundary effects, and influence of distant sources. Neuroinformatics. 2007 ; 5: 207-222 (Pubitemid 351496191)
43. Light GA, Hsu JL, Hsieh MH, et al. Gamma band oscillations reveal neural network cortical coherence dysfunction in schizophrenia patients. Biol Psychiatry. 2006 ; 60: 1231-1240 (Pubitemid 44693537)
44. Lodge DJ, Behrens MM, Grace AA. A loss of parvalbumin-containing interneurons is associated with diminished oscillatory activity in an animal model of schizophrenia. J Neurosci. 2009 ; 29: 2344-2354
45. Ma J, Leung LS. Relation between hippocampal gamma waves and behavioral disturbances induced by phencyclidine and methamphetamine. Behav Brain Res. 2000 ; 111: 1-11 (Pubitemid 30326697)
46. Ma J, Leung LS. The supramammillo-septal-hippocampal pathway mediates sensorimotor gating impairment and hyperlocomotion induced by MK-801 and ketamine in rats. Psychopharmacology (Berl). 2007 ; 191: 961-974 (Pubitemid 46399137)
47. Magill PJ, Sharott A, Harnack D, Kupsch A, Meissner W, Brown P. Coherent spike-wave oscillations in the cortex and subthalamic nucleus of the freely moving rat. Neuroscience. 2005 ; 132: 659-664
48. Masimore B, Kakalios J, Redish AD. Measuring fundamental frequencies in local field potentials. J Neurosci Methods. 2004 ; 138: 97-105 (Pubitemid 39485982)
49. Moghaddam B, Adams B, Verma A, Daly D. 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. 1997 ; 17: 2921-2927 (Pubitemid 27155025)
50. Nunez PL, Srinivasan, R (2005) Electric Fields of the Brain: The Neurophysics of EEG. Oxford: Oxford University Press.
51. O'Donnell P, Grace AA. Synaptic interactions among excitatory afferents to nucleus accumbens neurons: hippocampal gating of prefrontal cortical input. J Neurosci. 1995 ; 15: 3622-3639
52. O'Donnell P, Grace AA. Phencyclidine interferes with the hippocampal gating of nucleus accumbens neuronal activity in vivo. Neuroscience. 1998 ; 87: 823-830 (Pubitemid 28400353)
53. Paxinos W, Watson C The Rat Brain in Stereotaxic Coordinates. London: Academic Press ; 1986 :
54. Pennartz CM, Lee E, Verheul J, Lipa P, Barnes CA, McNaughton BL. The ventral striatum in off-line processing: ensemble reactivation during sleep and modulation by hippocampal ripples. J Neurosci. 2004 ; 24: 6446-6456 (Pubitemid 38971691)
55. Pettersen KH, Devor A, Ulbert I, Dale AM, Einevoll GT. Current-source density estimation based on inversion of electrostatic forward solution: effects of finite extent of neuronal activity and conductivity discontinuities. J Neurosci Methods. 2006 ; 154: 116-133 (Pubitemid 43816718)
56. Pinault D. N-methyl d-aspartate receptor antagonists ketamine and MK-801 induce wake-related aberrant gamma oscillations in the rat neocortex. Biol Psychiatry. 2008 ; 63: 730-735 (Pubitemid 351400766)
57. Ponomarenko AA, Korotkova TM, Haas HL. High-frequency (200 Hz) oscillations and firing patterns in the basolateral amygdala and dorsal endopiriform nucleus of the behaving rat. Behav Brain Res. 2003 ; 141: 123-129 (Pubitemid 36542959)
58. Rajagovindan R, Ding M. Decomposing neural synchrony: toward an explanation for near-zero phase-lag in cortical oscillatory networks. PLoS One. 2008 ; 3: e3649 - e3649
59. Roopun AK, Cunningham MO, Racca C, Alter K, Traub RD, Whittington MA. Region-specific changes in gamma and beta2 rhythms in NMDA receptor dysfunction models of schizophrenia. Schizophr Bull. 2008 ; 34: 962-973
60. Sams-Dodd F. Phencyclidine in the social interaction test: an animal model of schizophrenia with face and predictive validity. Rev Neurosci. 1999 ; 10: 59-90 (Pubitemid 29396547)
61. Sauleau P, Eusebio A, Thevathasan W, et al. Involvement of the subthalamic nucleus in engagement with behaviourally relevant stimuli. Eur J Neurosci. 2009 ; 29: 931-942
62. Singer W. Neuronal synchrony: a versatile code for the definition of relations?. Neuron. 1999 ; 24: 49-25
63. Spencer KM. The functional consequences of cortical circuit abnormalities on gamma oscillations in schizophrenia: insights from computational modeling. Front Hum Neurosci. 2009 ; 3: 33-33
64. Spencer KM, Nestor PG, Perlmutter R, et al. Neural synchrony indexes disordered perception and cognition in schizophrenia. Proc Natl Acad Sci USA. 2004 ; 101: 17288-17293 (Pubitemid 39627812)
65. Verma A, Moghaddam B. NMDA receptor antagonists impair prefrontal cortex function as assessed via spatial delayed alternation performance in rats: modulation by dopamine. J Neurosci. 1996 ; 16: 373-379 (Pubitemid 26010723)
66. Wilson CJ. The generation of natural firing patterns in neostriatal neurons. Prog Brain Res. 1993 ; 99: 277-297 (Pubitemid 24015900)
67. Wilson CJ, Kawaguchi Y. The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons. J Neurosci. 1996 ; 16: 2397-2410 (Pubitemid 26154349)
68. Wojcik DK, Leski S. Current source density reconstruction from incomplete data. Neural Comput. 2010 ; 22: 48-60
69. Ylinen A, Bragin A, Nadasdy Z, et al. Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J Neurosci. 1995 ; 15: 30-46
70. Ashton H. The diagnosis and management of benzodiazepine dependence. Curr Opin Psychiatry. 2005 ; 18: 19-28
71. Chouinard G. Issues in the clinical use of benzodiazepines: potency, withdrawal, and rebound. J Clin Psychiatry. 2004 ; 65: 7-12
72. Gerra G, Zaimovich A, Giusti F, Moi G, Brewer C. Intravenous flumazenil versus oxazepam tapering in the treatment of benzodiazepine withdrawal: a randomized, placebo-controlled study. Addict Biol. 2002 ; 7: 385-395 (Pubitemid 35402511)
73. Hood S, O'Neil G, Hulse G. The role of flumazenil in the treatment of benzodiazepine dependence: physiological and psychological profiles. J Psychopharmacol. 2009 ; 23: 401-409
74. Marriott S, Tyrer P. Benzodiazepine dependence. Avoidance and withdrawal. Drug Saf. 1993 ; 9: 93-103 (Pubitemid 23243521)
75. O'brien C. Benzodiazepine use, abuse, and dependence. J Clin Psychiatry. 2005 ; 66: 28-33 (Pubitemid 40343678)
76. Quaglio G, Lugoboni F, Fornasiero A, Lechi A, Gerra G, Mezzelani P. Dependence on zolpidem: two case reports of detoxification with flumazenil infusion. Int Clin Psychopharmacol. 2005 ; 20: 285-287 (Pubitemid 41192149)