Changes in ensemble activity of hippocampus CA1 neurons induced by chronic morphine administration in freely behaving mice

Neuroscience

Volumn 171, Issue 3, 2010, Pages 747-759

  Liu, F ^a   Jiang, H ^a   Zhong, W ^a   Wu, X ^a   Luo, J ^a  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Chronic morphine administration; Ensemble activity; Freely behaving mice; Hippocampus; Multi channel recordings

Indexed keywords

DOPAMINE 1 RECEPTOR BLOCKING AGENT; DOPAMINE RECEPTOR; MORPHINE; NALOXONE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTRIC POTENTIAL; GAMMA RHYTHM; HIPPOCAMPUS; INTERNEURON; LONG TERM EXPOSURE; MALE; MORPHINE ADDICTION; MOUSE; MULTICHANNEL RECORDER; NERVE CELL NETWORK; NEUROMODULATION; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SPIKE WAVE; THETA RHYTHM;

ACTION POTENTIALS; ANIMALS; BEHAVIOR, ANIMAL; CA1 REGION, HIPPOCAMPAL; DISEASE MODELS, ANIMAL; DRUG ADMINISTRATION SCHEDULE; MALE; MICE; MICE, INBRED C57BL; MORPHINE; NERVE NET; NEURONS; RECEPTORS, DOPAMINE; THETA RHYTHM;

EID: 78349309502     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.09.052     Document Type: Article

References (90)

1. Axmacher N., Henseler M.M., Jensen O., Weinreich I., Elger C.E., Fell J. Cross-frequency coupling supports multi-item working memory in the human hippocampus. Proc Natl Acad Sci U S A 2010, 107:3228-3233.
2. Bals-Kubik R., Ableitner A., Herz A., Shippenberg T.S. Neuroanatomical sites mediating the motivational effects of opioids as mapped by the conditioned place preference paradigm in rats. J Pharmacol Exp Ther 1993, 264:489-495.
3. Bauer M., Oostenveld R., Peeters M., Fries P. Tactile spatial attention enhances gamma-band activity in somatosensory cortex and reduces low-frequency activity in parieto-occipital areas. J Neurosci 2006, 26:490-501.
4. Beninger R.J., Miller R. Dopamine D1-like receptors and reward-related incentive learning. Neurosci Biobehav Rev 1998, 22:335-345.
5. Berke J.D., Hyman S.E. Addiction, dopamine, and the molecular mechanisms of memory. Neuron 2000, 25:515-532.
6. Black Y.D., Green-Jordan K., Eichenbaum H.B., Kantak K.M. Hippocampal memory system function and the regulation of cocaine self-administration behavior in rats. Behav Brain Res 2004, 151:225-238.
7. Bragin A., Jando G., Nadasdy Z., Hetke J., Wise K., Buzsaki G. Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. J Neurosci 1995, 15:47-60.
8. Buzsaki G. Theta oscillations in the hippocampus. Neuron 2002, 33:325-340.
9. Buzsaki G., Buhl D.L., Harris K.D., Csicsvari J., Czeh B., Morozov A. Hippocampal network patterns of activity in the mouse. Neuroscience 2003, 116:201-211.
10. Buzsaki G., Eidelberg E. Phase relations of hippocampal projection cells and interneurons to theta activity in the anesthetized rat. Brain Res 1983, 266:334-339.
11. Buzsaki G., Laszlovszky I., Lajtha A., Vadasz C. Spike-and-wave neocortical patterns in rats: genetic and aminergic control. Neuroscience 1990, 38:323-333.
12. Chrobak J.J., Buzsaki G. Gamma oscillations in the entorhinal cortex of the freely behaving rat. J Neurosci 1998, 18:388-398.
13. Colgin L.L., Denninger T., Fyhn M., Hafting T., Bonnevie T., Jensen O., Moser M.B., Moser E.I. Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 2009, 462:353-357.
14. Csicsvari J., Jamieson B., Wise K.D., Buzsaki G. Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 2003, 37:311-322.
15. del Olmo N., Miguens M., Higuera-Matas A., Torres I., Garcia-Lecumberri C., Solis J.M., Ambrosio E. Enhancement of hippocampal long-term potentiation induced by cocaine self-administration is maintained during the extinction of this behavior. Brain Res 2006, 1116:120-126.
16. Devine D.P., Leone P., Pocock D., Wise R.A. Differential involvement of ventral tegmental mu, delta and kappa opioid receptors in modulation of basal mesolimbic dopamine release: in vivo microdialysis studies. J Pharmacol Exp Ther 1993, 266:1236-1246.
17. DiLeone R.J., Georgescu D., Nestler E.J. Lateral hypothalamic neuropeptides in reward and drug addiction. Life Sci 2003, 73:759-768.
18. Dong Z., Han H., Wang M., Xu L., Hao W., Cao J. Morphine conditioned place preference depends on glucocorticoid receptors in both hippocampus and nucleus accumbens. Hippocampus 2006, 16:809-813.
19. Dong Z., Zhong W., Tian M., Han H., Cao J., Xu T., Luo J., Xu L. Stress evoked by opiate withdrawal facilitates hippocampal LTP in vivo. Hippocampus 2006, 16:1017-1025.
20. Dragoi G., Buzsaki G. Temporal encoding of place sequences by hippocampal cell assemblies. Neuron 2006, 50:145-157.
21. Everitt B.J., Robbins T.W. Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 2005, 8:1481-1489.
22. Fell J., Fernandez G., Klaver P., Elger C.E., Fries P. Is synchronized neuronal gamma activity relevant for selective attention?. Brain Res Brain Res Rev 2003, 42:265-272.
23. Fell J., Klaver P., Lehnertz K., Grunwald T., Schaller C., Elger C.E., Fernandez G. Human memory formation is accompanied by rhinal-hippocampal coupling and decoupling. Nat Neurosci 2001, 4:1259-1264.
24. Ferbinteanu J., McDonald R.J. Dorsal/ventral hippocampus, fornix, and conditioned place preference. Hippocampus 2001, 11:187-200.
25. Fisher N.I. Statistical analysis of circular data 1993, Cambridge University Press.
26. Fries P., Neuenschwander S., Engel A.K., Goebel R., Singer W. Rapid feature selective neuronal synchronization through correlated latency shifting. Nat Neurosci 2001, 4:194-200.
27. Gasbarri A., Packard M.G., Campana E., Pacitti C. Anterograde and retrograde tracing of projections from the ventral tegmental area to the hippocampal formation in the rat. Brain Res Bull 1994, 33:445-452.
28. Gasbarri A., Sulli A., Packard M.G. The dopaminergic mesencephalic projections to the hippocampal formation in the rat. Prog Neuropsychopharmacol Biol Psychiatry 1997, 21:1-22.
29. Hasselmo M.E., Eichenbaum H. Hippocampal mechanisms for the context-dependent retrieval of episodes. Neural Netw 2005, 18:1172-1190.
30. Hasselmo M.E., Hay J., Ilyn M., Gorchetchnikov A. Neuromodulation, theta rhythm and rat spatial navigation. Neural Netw 2002, 15:689-707.
31. Howard M.W., Rizzuto D.S., Caplan J.B., Madsen J.R., Lisman J., Aschenbrenner-Scheibe R., Schulze-Bonhage A., Kahana M.J. Gamma oscillations correlate with working memory load in humans. Cereb Cortex 2003, 13:1369-1374.
32. Huang Y.Y., Kandel E.R. D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of the hippocampus. Proc Natl Acad Sci U S A 1995, 92:2446-2450.
33. Hyman S.E. Addiction: a disease of learning and memory. Am J Psychiatry 2005, 162:1414-1422.
34. Hyman S.E., Malenka R.C. Addiction and the brain: the neurobiology of compulsion and its persistence. Nat Rev Neurosci 2001, 2:695-703.
35. Hyman S.E., Malenka R.C., Nestler E.J. Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 2006, 29:565-598.
36. Ito R., Robbins T.W., Pennartz C.M., Everitt B.J. Functional interaction between the hippocampus and nucleus accumbens shell is necessary for the acquisition of appetitive spatial context conditioning. J Neurosci 2008, 28:6950-6959.
37. Jaber M., Robinson S.W., Missale C., Caron M.G. Dopamine receptors and brain function. Neuropharmacology 1996, 35:1503-1519.
38. Jacobs J., Kahana M.J., Ekstrom A.D., Fried I. Brain oscillations control timing of single-neuron activity in humans. J Neurosci 2007, 27:3839-3844.
39. Jeewajee A., Barry C., O'Keefe J., Burgess N. Grid cells and theta as oscillatory interference: electrophysiological data from freely moving rats. Hippocampus 2008, 18:1175-1185.
40. Jeewajee A., Lever C., Burton S., O'Keefe J., Burgess N. Environmental novelty is signaled by reduction of the hippocampal theta frequency. Hippocampus 2008, 18:340-348.
41. Johnson S.W., North R.A. Opioids excite dopamine neurons by hyperpolarization of local interneurons. J Neurosci 1992, 12:483-488.
42. Kanji G.K. 100 statistical tests. Statistical Papers 2006.
43. Karami M., Zarrindast M.R., Sepehri H., Sahraei H. Role of nitric oxide in the rat hippocampal CA1 area on morphine-induced conditioned place preference. Eur J Pharmacol 2002, 449:113-119.
44. Kelley A.E. Memory and addiction: shared neural circuitry and molecular mechanisms. Neuron 2004, 44:161-179.
45. Koob G.F. Brain stress systems in the amygdala and addiction. Brain Res 2009, 1293:61-75.
46. Kramis R., Vanderwolf C.H., Bland B.H. Two types of hippocampal rhythmical slow activity in both the rabbit and the rat: relations to behavior and effects of atropine, diethyl ether, urethane, and pentobarbital. Exp Neurol 1975, 49:58-85.
47. Lee H., Simpson G.V., Logothetis N.K., Rainer G. Phase locking of single neuron activity to theta oscillations during working memory in monkey extrastriate visual cortex. Neuron 2005, 45:147-156.
48. Leung L.S. Fast (beta) rhythms in the hippocampus: a review. Hippocampus 1992, 2:93-98.
49. Liang D., Shi X., Qiao Y., Angst M.S., Yeomans D.C., Clark J.D. Chronic morphine administration enhances nociceptive sensitivity and local cytokine production after incision. Mol Pain 2008, 4:7.
50. Lin L., Chen G., Xie K., Zaia K.A., Zhang S., Tsien J.Z. Large-scale neural ensemble recording in the brains of freely behaving mice. J Neurosci Methods 2006, 155:28-38.
51. Linderman M.D., Gilja V., Santhanam G., Afshar A., Ryu S., Meng T.H., Shenoy K.V. Neural recording stability of chronic electrode arrays in freely behaving primates. Conf Proc IEEE Eng Med Biol Soc 2006, 1:4387-4391.
52. Lisman J.E., Idiart M.A. Storage of 7 +/-2 short-term memories in oscillatory subcycles. Science 1995, 267:1512-1515.
53. Lu L., Zeng S., Liu D., Ceng X. Inhibition of the amygdala and hippocampal calcium/calmodulin-dependent protein kinase II attenuates the dependence and relapse to morphine differently in rats. Neurosci Lett 2000, 291:191-195.
54. Lubenov E.V., Siapas A.G. Hippocampal theta oscillations are travelling waves. Nature 2009, 459:534-539.
55. Maldonado R., Blendy J.A., Tzavara E., Gass P., Roques B.P., Hanoune J., Schutz G. Reduction of morphine abstinence in mice with a mutation in the gene encoding CREB. Science 1996, 273:657-659.
56. Masuoka T., Fujii Y., Kamei C. Participation of the hippocampal theta rhythm in memory formation for an eight-arm radial maze task in rats. Brain Res 2006, 1103:159-163.
57. Montgomery S.M., Sirota A., Buzsaki G. Theta and gamma coordination of hippocampal networks during waking and rapid eye movement sleep. J Neurosci 2008, 28:6731-6741.
58. Morris R.G., Moser E.I., Riedel G., Martin S.J., Sandin J., Day M., O'Carroll C. Elements of a neurobiological theory of the hippocampus: the role of activity-dependent synaptic plasticity in memory. Philos Trans R Soc Lond B Biol Sci 2003, 358:773-786.
59. Nestler E.J. Neurobiology. Total recall-the memory of addiction. Science 2001, 292:2266-2267.
60. Noble F., Cox B.M. The role of dopaminergic systems in opioid receptor desensitization in nucleus accumbens and caudate putamen of rat after chronic morphine treatment. J Pharmacol Exp Ther 1997, 283:557-565.
61. O'Keefe J., Recce M.L. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 1993, 3:317-330.
62. Osipova D., Takashima A., Oostenveld R., Fernandez G., Maris E., Jensen O. Theta and gamma oscillations predict encoding and retrieval of declarative memory. J Neurosci 2006, 26:7523-7531.
63. Otmakhova N.A., Lisman J.E. D1/D5 dopamine receptor activation increases the magnitude of early long-term potentiation at CA1 hippocampal synapses. J Neurosci 1996, 16:7478-7486.
64. Pastalkova E., Itskov V., Amarasingham A., Buzsaki G. Internally generated cell assembly sequences in the rat hippocampus. Science 2008, 321:1322-1327.
65. Penttonen M., Kamondi A., Acsady L., Buzsaki G. Gamma frequency oscillation in the hippocampus of the rat: intracellular analysis in vivo. Eur J Neurosci 1998, 10:718-728.
66. Pesaran B., Pezaris J.S., Sahani M., Mitra P.P., Andersen R.A. Temporal structure in neuronal activity during working memory in macaque parietal cortex. Nat Neurosci 2002, 5:805-811.
67. Raghavachari S., Kahana M.J., Rizzuto D.S., Caplan J.B., Kirschen M.P., Bourgeois B., Madsen J.R., Lisman J.E. Gating of human theta oscillations by a working memory task. J Neurosci 2001, 21:3175-3183.
68. Rezayof A., Zarrindast M.R., Sahraei H., Haeri-Rohani A. Involvement of dopamine receptors of the dorsal hippocampus on the acquisition and expression of morphine-induced place preference in rats. J Psychopharmacol 2003, 17:415-423.
69. Rivas J., Gaztelu J.M., Garcia-Austt E. Changes in hippocampal cell discharge patterns and theta rhythm spectral properties as a function of walking velocity in the guinea pig. Exp Brain Res 1996, 108:113-118.
70. Robbins T.W., Everitt B.J. Limbic-striatal memory systems and drug addiction. Neurobiol Learn Mem 2002, 78:625-636.
71. Salinas E., Sejnowski T.J. Correlated neuronal activity and the flow of neural information. Nat Rev Neurosci 2001, 2:539-550.
72. Sato N., Yamaguchi Y. Theta synchronization networks emerge during human object-place memory encoding. Neuroreport 2007, 18:419-424.
73. Shippenberg T.S., Herz A. Place preference conditioning reveals the involvement of D1-dopamine receptors in the motivational properties of mu- and kappa-opioid agonists. Brain Res 1987, 436:169-172.
74. Shippenberg T.S., Herz A. Motivational effects of opioids: influence of D-1 versus D-2 receptor antagonists. Eur J Pharmacol 1988, 151:233-242.
75. Siapas A.G., Lubenov E.V., Wilson M.A. Prefrontal phase locking to hippocampal theta oscillations. Neuron 2005, 46:141-151.
76. Skaggs W.E., McNaughton B.L. Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 1996, 271:1870-1873.
77. Skaggs W.E., McNaughton B.L., Wilson M.A., Barnes C.A. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 1996, 6:149-172.
78. Slawinska U., Kasicki S. The frequency of rat's hippocampal theta rhythm is related to the speed of locomotion. Brain Res 1998, 796:327-331.
79. Spielewoy C., Gonon F., Roubert C., Fauchey V., Jaber M., Caron M.G., Roques B.P., Hamon M., Betancur C., Maldonado R., Giros B. Increased rewarding properties of morphine in dopamine-transporter knockout mice. Eur J Neurosci 2000, 12:1827-1837.
80. Tallon-Baudry C., Bertrand O., Henaff M.A., Isnard J., Fischer C. Attention modulates gamma-band oscillations differently in the human lateral occipital cortex and fusiform gyrus. Cereb Cortex 2005, 15:654-662.
81. Thompson A.M., Gosnell B.A., Wagner J.J. Enhancement of long-term potentiation in the rat hippocampus following cocaine exposure. Neuropharmacology 2002, 42:1039-1042.
82. Tort A.B., Komorowski R.W., Manns J.R., Kopell N.J., Eichenbaum H. Theta-gamma coupling increases during the learning of item-context associations. Proc Natl Acad Sci U S A 2009, 106:20942-20947.
83. Volkow N.D., Fowler J.S., Wang G.J., Goldstein R.Z. Role of dopamine, the frontal cortex and memory circuits in drug addiction: insight from imaging studies. Neurobiol Learn Mem 2002, 78:610-624.
84. Vorel S.R., Liu X., Hayes R.J., Spector J.A., Gardner E.L. Relapse to cocaine-seeking after hippocampal theta burst stimulation. Science 2001, 292:1175-1178.
85. Way E.L., Loh H.H., Shen F.H. Simultaneous quantitative assessment of morphine tolerance and physical dependence. J Pharmacol Exp Ther 1969, 167:1-8.
86. White N.M. Addictive drugs as reinforcers: multiple partial actions on memory systems. Addiction 1996, 91:921-949. discussion 951-965.
87. Wulff P., Ponomarenko A.A., Bartos M., Korotkova T.M., Fuchs E.C., Bahner F., Both M., Tort A.B., Kopell N.J., Wisden W., Monyer H. Hippocampal theta rhythm and its coupling with gamma oscillations require fast inhibition onto parvalbumin-positive interneurons. Proc Natl Acad Sci U S A 2009, 106:3561-3566.
88. Young C.K., McNaughton N. Coupling of theta oscillations between anterior and posterior midline cortex and with the hippocampus in freely behaving rats. Cereb Cortex 2009, 19:24-40.
89. Zhong W.X., Dong Z.F., Tian M., Cao J., Xu L., Luo J.H. N-methyl-d-aspartate receptor-dependent long-term potentiation in CA1 region affects synaptic expression of glutamate receptor subunits and associated proteins in the whole hippocampus. Neuroscience 2006, 141:1399-1413.
90. Zornoza T., Cano-Cebrian M.J., Martinez-Garcia F., Polache A., Granero L. Hippocampal dopamine receptors modulate cFos expression in the rat nucleus accumbens evoked by chemical stimulation of the ventral hippocampus. Neuropharmacology 2005, 49:1067-1076.