Hippocampal serotonin depletion facilitates place learning concurrent with an increase in CA1 high frequency theta activity expression in the rat

European Journal of Pharmacology

Volumn 652, Issue 1-3, 2011, Pages 73-81

  Gutiérrez Guzmán, Blanca Erika ^a   Hernández Pérez, J Jesús ^a   González Burgos, Ignacio ^a   Feria Velásco, Alfredo ^b,c   Medina, Rafael ^a   Guevara, Miguel Ángel ^b,c   López Vázquez, Miguel Ángel ^a   Olvera Cortés, María Esther ^a  

^a INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

^b UNIVERSITY OF GUADALAJARA   (Mexico)

^c Francisco de Quevedo 180 ^*  (Mexico)

Author keywords

5,7 Dihydroxytriptamine; Hippocampus; Serotonin; Spatial learning; Theta activity

Indexed keywords

5,7 DIHYDROXYTRYPTAMINE; SEROTONIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DAMAGE; BRAIN FORNIX; CINGULATE GYRUS; CONTROLLED STUDY; ELECTRIC ACTIVITY; FACILITATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL FIMBRIA; HIPPOCAMPUS THETA RHYTHM; LEARNING; LEARNING TEST; MALE; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; RAT; SEROTONIN BRAIN LEVEL; SEROTONIN RELEASE; SEROTONINERGIC SYSTEM;

5,7-DIHYDROXYTRYPTAMINE; ANIMALS; CA1 REGION, HIPPOCAMPAL; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; LEARNING; MALE; RATS; RATS, SPRAGUE-DAWLEY; SEROTONIN; SPACE PERCEPTION; THETA RHYTHM;

EID: 78650915981     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2010.11.014     Document Type: Article

References (70)

1. W. Adams, S. Kusljic, and M. van den Buuse Serotonin depletion in the dorsal and ventral hippocampus: effects on locomotor hyperactivity, prepulse inhibition and learning and memory Neuropharmacology 55 2008 1048 1055
2. H.J. Altman, D.A. Nordy, and S.O. Ogren Role of serotonin in memory: facilitation by alaproclate and zimeldine Psychopharmacology (Berl) 84 1984 496 502
3. H.J. Altman, S.O. Ogren, R.F. Berman, and H.J. Normile The effects of p-chloroamphetamine, a depletor of brain serotonin, on the performance of rats in two types of positively reinforced complex spatial discrimination tasks Behav. Neural Biol. 52 1989 131 144
4. H.J. Altman, H.J. Normile, M.P. Galloway, A. Ramirez, and E.C. Azmitia Enhanced spatial discrimination learning in rats following 5,7-DHT-induced serotonergic deafferentation of the hippocampus Brain Res. 518 1990 61 66
5. P.B. Anguiano-Rodriguez, L. Gaytan-Tocaven, and M.E. Olvera-Cortes Striatal serotonin depletion facilitates rat egocentric learning via dopamine modulation Eur. J. Pharmacol. 556 2007 91 98
6. S.Y. Assaf, and J.J. Miller The role of a raphe serotonin system in the control of septal unit activity and hippocampal desynchronization Neuroscience 3 1978 539 550
7. E.C. Azmitia The serotonin-producing neurons of the midbrain median and dorsal raphe nuclei L.L. Iversen, S.D. Iversen, S.H. Snyder, Handbook of Psychopharmacology Vol. 8 1978 Raven New York 233 262
8. S. Aznar, Z.X. Qian, and G.M. Knudsen Non-serotonergic dorsal and median raphe projection onto parvalbumin- and calbindin-containing neurons in hippocampus and septum Neuroscience 124 2004 573 581
9. I. Belcheva, R. Tashev, and S. Belcheva Hippocampal asymmetry in serotonergic modulation of learning and memory in rats Laterality 12 2007 475 486
10. B.H. Bland, S.D. Oddie, and L.V. Colom Mechanisms of neural synchrony in the septohippocampal pathways underlying hippocampal theta generation J. Neurosci. 19 1999 3223 3237
11. R.A. Brown, S.G. Walling, J.S. Milway, and C.W. Harley Locus ceruleus activation suppresses feedforward interneurons and reduces beta-gamma electroencephalogram frequencies while it enhances theta frequencies in rat dentate gyrus J. Neurosci. 25 2005 1985 1991
12. M.C. Buhot, S.K. Patra, and S. Naili Spatial memory deficits following stimulation of hippocampal 5-HT1B receptors in the rat Eur. J. Pharmacol. 285 1995 221 228
13. M.C. Buhot, S. Martin, and L. Segu Role of serotonin in memory impairment Ann. Med. 32 2000 210 221
14. M. Carli, R. Luschi, P. Garofalo, and R. Samanin 8-OH-DPAT impairs spatial but not visual learning in a water maze by stimulating 5-HT1A receptors in the hippocampus Behav. Brain Res. 67 1995 67 74
15. C. Destrade Two types of diencephalically driven RSA (theta) as a means of studying memory formation in mice Brain Res. 234 1982 486 493
16. H. Eichenbaum, T. Otto, and N.J. Cohen The hippocampus-what does it do? Behav Neural Biol. 57 1992 2 36
17. P.J. Fletcher, K.M. Korth, and J.W. Chambers Selective destruction of brain serotonin neurons by 5,7-dihydroxytryptamine increases responding for a conditioned reward Psychopharmacology (Berl) 147 1999 291 299
18. V.V. Gavrilov, S.I. Wiener, and A. Berthoz Enhanced hippocampal theta EEG during whole body rotations in awake restrained rats Neurosci. Lett. 197 1995 239 241
19. T. Goto, F. Kuzuya, H. Endo, T. Tajima, and H. Ikari Some effects of CNS cholinergic neurons on memory J. Neural Transm. Suppl. 30 1990 1 11
20. M.E. Hasselmo, C. Bodelon, and B.P. Wyble A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning Neural Comput. 14 2002 793 817
21. R.M. Hayman, S. Chakraborty, M.I. Anderson, and K.J. Jeffery Context-specific acquisition of location discrimination by hippocampal place cells Eur. J. Neurosci. 18 2003 2825 2834
22. K. Kasamo, T. Suzuki, K. Tada, N. Ueda, E. Matsuda, K. Ishikawa, and T. Kojima Endogenous 5-HT tonically inhibits spontaneous firing activity of dorsal hippocampus CA1 pyramidal neurons through stimulation of 5-HT(1A) receptors in quiet awake rats: in vivo electrophysiological evidence Neuropsychopharmacology 24 2001 141 151
23. V.F. Kitchigina, T.A. Kudina, E.V. Kutyreva, and O.S. Vinogradova Neuronal activity of the septal pacemaker of theta rhythm under the influence of stimulation and blockade of the median raphe nucleus in the awake rabbit Neuroscience 94 1999 453 463
24. W. Klimesch EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis Brain Res. Brain Res. Rev. 29 1999 169 195
25. R. Kramis, C.H. Vanderwolf, and B.H. Bland 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. 49 1975 58 85
26. M.G. Lee, J.J. Chrobak, A. Sik, R.G. Wiley, and G. Buzsaki Hippocampal theta activity following selective lesion of the septal cholinergic system Neuroscience 62 1994 1033 1047
27. O. Lehmann, F. Bertrand, H. Jeltsch, M. Morer, C. Lazarus, B. Will, and J.C. Cassel 5,7-DHT-induced hippocampal 5-HT depletion attenuates behavioural deficits produced by 192 IgG-saporin lesions of septal cholinergic neurons in the rat Eur. J. Neurosci. 15 2002 1991 2006
28. C. Leranth, and R.P. Vertes Neuronal networks that control the septal pacemaker system: synaptic interconnections between the septal complex, hippocampus, supramamillary area, and median raphe R.N. The behavioral neuroscience of the septal region 2000 Springer-Verlag New York 15 47
29. F.H. Lopes da Silva The rhythmic slow activity (theta) of the limbic cortex: an oscillation in search of a function E. Basar, T.H.B. Induced rhythms in the brain 1992 Birkhäuser Boston 1063 1086
30. C. Maho, G. Dutrieux, and M. Ammassari-Teule Parallel modifications of spatial memory performances, exploration patterns, and hippocampal theta rhythms in fornix-damaged rats: reversal by oxotremorine Behav. Neurosci. 102 1988 601 604
31. N. Majlessi, M. Kadkhodaee, M. Parviz, and N. Naghdi Serotonin depletion in rat hippocampus attenuates L-NAME-induced spatial learning deficits Brain Res. 963 2003 244 251
32. E. Maru, L.K. Takahashi, and S. Iwahara Effects of median raphe nucleus lesions on hippocampal EEG in the freely moving rat Brain Res. 163 1979 223 234
33. R.K. McNamara, and R.W. Skelton The neuropharmacological and neurochemical basis of place learning in the Morris water maze Brain Res. Brain Res. Rev. 18 1993 33 49
34. N. McNaughton, M. Ruan, and M.A. Woodnorth Restoring theta-like rhythmicity in rats restores initial learning in the Morris water maze Hippocampus 16 2006 1102 1110
35. S.J. Murtha, and B.A. Pappas Neurochemical, histopathological and mnemonic effects of combined lesions of the medial septal and serotonin afferents to the hippocampus Brain Res. 651 1994 16 26
36. O.G. Nilsson, R.E. Strecker, A. Daszuta, and A. Bjorklund Combined cholinergic and serotonergic denervation of the forebrain produces severe deficits in a spatial learning task in the rat Brain Res. 453 1988 235 246
37. H.J. Normile, D.J. Jenden, D.M. Kuhn, W.A. Wolf, and H.J. Altman Effects of combined serotonin depletion and lesions of the nucleus basalis magnocellularis on acquisition of a complex spatial discrimination task in the rat Brain Res. 536 1990 245 250
38. S.D. Oddie, and B.H. Bland Hippocampal formation theta activity and movement selection Neurosci. Biobehav. Rev. 22 1998 221 231
39. E. Olvera-Cortes, M. Cervantes, and I. Gonzalez-Burgos Place-learning, but not cue-learning training, modifies the hippocampal theta rhythm in rats Brain Res. Bull. 58 2002 261 270
40. E. Olvera-Cortes, M.A. Guevara, and I. Gonzalez-Burgos Increase of the hippocampal theta activity in the Morris water maze reflects learning rather than motor activity Brain Res. Bull. 62 2004 379 384
41. M.E. Olvera-Cortes, P. Anguiano-Rodriguez, M.A. Lopez-Vazquez, and J.M. Alfaro Serotonin/dopamine interaction in learning Prog. Brain Res. 172 2008 567 602
42. N.A. Otmakhova, J. Lewey, B. Asrican, and J.E. Lisman Inhibition of perforant path input to the CA1 region by serotonin and noradrenaline J. Neurophysiol. 94 2005 1413 1422
43. W.X. Pan, and N. McNaughton The medial supramammillary nucleus, spatial learning and the frequency of hippocampal theta activity Brain Res. 764 1997 101 108
44. G. Paxinos, and C. Watson The rat brain in stereotaxic coordinates 2nd ed. 1986 Academic Press San Diego, CA
45. M.I. Perez-Vega, A. Feria-Velasco, and I. Gonzalez-Burgos Prefrontocortical serotonin depletion results in plastic changes of prefrontocortical pyramidal neurons, underlying a greater efficiency of short-term memory Brain Res. Bull. 53 2000 291 300
46. P. Piguet, and M. Galvan Transient and long-lasting actions of 5-HT on rat dentate gyrus neurones in vitro J. Physiol. 481 Pt 3 1994 629 639
47. G. Richter-Levin, and M. Segal Spatial performance is severely impaired in rats with combined reduction of serotonergic and cholinergic transmission Brain Res. 477 1989 404 407
48. G. Richter-Levin, and M. Segal The effects of serotonin depletion and raphe grafts on hippocampal electrophysiology and behavior J. Neurosci. 11 1991 1585 1596
49. G. Richter-Levin, V. Greenberger, and M. Segal Regional specificity of raphe graft-induced recovery of behavioral functions impaired by combined serotonergic/cholinergic lesions Exp. Neurol. 121 1993 256 260
50. W.J. Riedel, T. Klaassen, N.E. Deutz, A. van Someren, and H.M. van Praag Tryptophan depletion in normal volunteers produces selective impairment in memory consolidation Psychopharmacology (Berl) 141 1999 362 369
51. W.J. Riedel, T. Klaassen, and J.A. Schmitt Tryptophan, mood, and cognitive function Brain Behav. Immun. 16 2002 581 589
52. P. Riekkinen Jr., J. Sirvio, and P. Riekkinen Interaction between raphe dorsalis and nucleus basalis magnocellularis in spatial learning Brain Res. 527 1990 342 345
53. P. Riekkinen Jr., P. Jakala, J. Sirvio, and P. Riekkinen The effects of increased serotonergic and decreased cholinergic activities on spatial navigation performance in rats Pharmacol. Biochem. Behav. 39 1991 25 29
54. M. Segal Potassium currents activated in hippocampal neurons by serotonin are mediated by a change in intracellular calcium concentrations Eur. J. Pharmacol. 181 1990 299 301
55. P.A. Simon, F. Poindessous-Jazat, P. Dutar, J. Epelbaum, and M.H. Bassant Firing properties of anatomically identified neurons in the medial septum of anesthetized and unanesthetized restrained rats J. Neurosci. 26 2006 9038 9046
56. F. Sotty, M. Danik, F. Manseau, F. Laplante, R. Quirion, and S. Williams Distinct electrophysiological properties of glutamatergic, cholinergic and GABAergic rat septohippocampal neurons: novel implications for hippocampal rhythmicity J. Physiol. 551 2003 927 943
57. M. Stewart, and S.E. Fox Do septal neurons pace the hippocampal theta rhythm? Trends Neurosci. 13 1990 163 168
58. C.H. Vanderwolf Hippocampal electrical activity and voluntary movement in the rat Electroencephalogr. Clin. Neurophysiol. 26 1969 407 418
59. C.H. Vanderwolf Cerebral activity and behavior: control by central cholinergic and serotonergic systems Int. Rev. Neurobiol. 30 1988 225 340
60. C.H. Vanderwolf A general role for serotonin in the control of behavior: studies with intracerebral 5,7-dihydroxytryptamine Brain Res. 504 1989 192 198
61. C.H. Vanderwolf, and G.B. Baker Evidence that serotonin mediates non-cholinergic neocortical low voltage fast activity, non-cholinergic hippocampal rhythmical slow activity and contributes to intelligent behavior Brain Res. 374 1986 342 356
62. C.H. Vanderwolf, L.W. Leung, and R.K. Cooley Pathways through cingulate, neo- and entorhinal cortices mediate atropine-resistant hippocampal rhythmical slow activity Brain Res. 347 1985 58 73
63. R.P. Vertes Brainstem modulation of the hippocampus. Anatomy, physiology, and significance R.L.I.a.K.H. Pribram, The Hippocampus 1986 Plenum New York 41 75
64. R.P. Vertes Hippocampal theta rhythm: a tag for short-term memory Hippocampus 15 2005 923 935
65. R.P. Vertes, and G.F. Martin Autoradiographic analysis of ascending projections from the pontine and mesencephalic reticular formation and the median raphe nucleus in the rat J. Comp. Neurol. 275 1988 511 541
66. R.P. Vertes, W.B. Hoover, and G. Viana Di Prisco Theta rhythm of the hippocampus: subcortical control and functional significance Behav. Cogn. Neurosci. Rev 3 2004 173 200
67. G. Viana Di Prisco, Z. Albo, R.P. Vertes, and B. Kocsis Discharge properties of neurons of the median raphe nucleus during hippocampal theta rhythm in the rat Exp. Brain Res. 145 2002 383 394
68. O.S. Vinogradova Expression, control, and probable functional significance of the neuronal theta-rhythm Prog. Neurobiol. 45 1995 523 583
69. O.S. Vinogradova, V.F. Kitchigina, T.A. Kudina, and K.I. Zenchenko Spontaneous activity and sensory responses of hippocampal neurons during persistent theta-rhythm evoked by median raphe nucleus blockade in rabbit Neuroscience 94 1999 745 753
70. B.T. Volpe, C.S. Hendrix, D.H. Park, A.C. Towle, and H.P. Davis Early post-natal administration of 5,7-dihydroxytryptamine destroys 5-HT neurons but does not affect spatial memory Brain Res. 589 1992 262 267