Lateralized hippocampal effects of vasoactive intestinal peptide on learning and memory in rats in a model of depression

Psychopharmacology

Volumn 221, Issue 4, 2012, Pages 561-574

  Ivanova, Margarita ^a   Belcheva, Stiliana ^b,c   Belcheva, Iren ^b   Negrev, Negrin ^a   Tashev, Roman ^b  

^a MEDICAL UNIVERSITY OF VARNA   (Bulgaria)

^b BULGARIAN ACADEMY OF SCIENCES   (Bulgaria)

^c Faculty of Pre School and Primary School Education   (Bulgaria)

Author keywords

Depression; Hippocampus; Lateralization; Learning and memory; Olfactory bulbectomy; Vasoactive intestinal peptide

Indexed keywords

SODIUM CHLORIDE; UNCLASSIFIED DRUG; VASOACTIVE INTESTINAL POLYPEPTIDE; VASOACTIVE INTESTINAL POLYPEPTIDE ANTAGONIST; VASOACTIVE INTESTINAL POLYPEPTIDE RECEPTOR 1; VASOACTIVE INTESTINAL POLYPEPTIDE[6-28];

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AVOIDANCE BEHAVIOR; COGNITION; CONTROLLED STUDY; DEPRESSION; HEMISPHERIC DOMINANCE; HIPPOCAMPAL CA1 REGION; HORMONE ACTION; HORMONE DETERMINATION; LEARNING; MALE; MEMORY; MICROINJECTION; NEUROMODULATION; NONHUMAN; OLFACTORY BULBECTOMY; PASSIVE AVOIDANCE; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; RECEPTOR DENSITY; TASK PERFORMANCE;

ANIMALS; AVOIDANCE LEARNING; COGNITION; DEPRESSION; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; LEARNING; MALE; MEMORY; NEUROPROTECTIVE AGENTS; PEPTIDE FRAGMENTS; RATS; RATS, WISTAR; RECEPTORS, VASOACTIVE INTESTINAL PEPTIDE; VASOACTIVE INTESTINAL PEPTIDE;

EID: 84862690083     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-011-2600-1     Document Type: Article

References (78)

1. Acsády L, Arabadzisz D, Freund TF (1996) Correlated morphological and neurochemical features identify different subsets of vasoactive intestinal polypeptide-immunoreactive interneurons in rat hippocampus. Neuroscience 73:299-315
2. Adamik A, Telegdy G (2005) Effects of pituitary adenylate cyclase polypeptide (PACAP) on extinction of active avoidance learning in rats: involvement of neurotransmitters. Regul Pept 127:55-62
3. Bakalkin G (1989) Neuropeptides induce directional asymmetry in brain and spinal cord: facts and hypotheses. Int J Neurosci 48:105-124
4. Belcheva I, Ternianov A, Georgiev V (2000) Lateralized learning and memory effects of angiotensin II microinjected into the rat CA1 hippocampal area. Peptides 21:407-411
5. Belcheva I, Tashev R, Belcheva S (2007) Hippocampal asymmetry in serotonergic modulation of learning and memory in rats. Laterality 12:475-486
6. Belcheva I, Ivanova M, Tashev R, Belcheva S (2009) Differential involvement of hippocampal vasoactive intestinal peptide in nociception of rats with a model of depression. Peptides 30:1497-1501
7. Bobkova N, Vorobyov V, Medvinskaya N, Aleksandrova I, Nesterova I (2008) Interhemispheric EEG differences in olfactory bulbectomized rats with different cognitive abilities and brain beta-amyloid levels. Brain Res 1232:185-194
8. Borghi C, Nicosia S, Gishetti A, Said SI (1979) Vasoactive intestinal polypeptide (VIP) stimulates adenylate cyclase in selected areas of rat brain. Life Sci 24:65-70
9. Bremner JD (2002) Structural changes in the brain in depression and relationship to symptom recurrence. CNS Spectr 7:129-139
10. Brenneman DE, Gozes I (1996) A femtomolar-acting neuroprotective peptide. J Clin Invest 97:2299-2307
11. Brenneman DE, Hauser J, Phillips TM, Davidson A, Bassan M, Gozes I (1999) Vasoactive intestinal peptide. Link between electrical activity and glia-mediated neurotrophism. Ann NYAcad Sci 897:17-26
12. Buresova O, Bures J (1983) Learning and memory. In: Bures J, Burisova O, Hustan JP (eds) Techniques and basic experiments for the study of brain and behavior. Elsevier, Amsterdam, pp 135-208
13. Chaudhury D, Loh DH, Dragich JM, Hagopian A, Colwell CS (2008) Select cognitive deficits in vasoactive intestinal peptide deficient mice. BMC Neurosci 9:63
14. Chen HX, Otmakhov N, Strack S, Colbran RJ, Lisman JE (2001) Is persistent activity of calcium/calmodulin-dependent kinase required for the maintenance of LTP? J Neurophysiol 85:1368-1376
15. Cottrell GA, Veldhuis HD, Rostene WH, de Kloet ER (1984) Behavioural actions of vasoactive intestinal peptide (VIP). Neuropeptides 4:331-341
16. Dewberry RG, Lipsey JR, Saad K, Moran TH, Robinson RG (1986) Lateralized response to cortical injury in the rat: interhemispheric interaction. Behav Neurosci 100:556-562
17. Diamond MC, Johnson RE, Ingham CA (1975) Morphological changes in the young, adult and aging rat cerebral cortex, hippocampus and diencephalon. Behav Biol 14:163-164
18. Diamond MC, Johnson RE, Young D, Singh SS (1983) Age-related morphologic differences in the rat cerebral cortex and hippocampus: male-female; right-left. Exp Neurol 81:1-13
19. Dickson L, Finlayson K (2009) VPAC and PAC receptors: from ligands to function. Pharmacol Ther 121(3):294-316
20. Dluzen DE, Kreutzberg JD (1996) Norepinephrine is lateralized within the olfactory bulbs of male mice. J Neurochem 66:1222-1226
21. Drevets WC, Price JL, Furey ML (2008) Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression. Brain Struct Funct 213:93-118
22. Ekblad E, Jongsma H, Brabet P, Bockaert J, Sundler F (2000) Characterization of intestinal receptors for VIP and PACAP in rat and in PAC1 receptor knockout mouse. Ann NY Acad Sci 921:137-147
23. Fishbein VA, Coy DH, Hocart SJ, Jiang NY, Mrozinski JE Jr, Mantey SA, Jensen RT (1994) A chimeric VIP-PACAP analogue but not VIP pseudopeptides function as VIP receptor antagonists. Peptides 15:95-100
24. Flood JF, Garland JS, Morley JE (1990) Vasoactive intestinal peptide (VIP): an amnestic neuropeptide. Peptides 11:933-938
25. Gjerris A (1988) Do concentrations of neurotransmitters in lumbar CSF reflect cerebral dysfunction in depression? Acta Psychiatr Scand Suppl 345:21-24
26. Gjerris A, Rafaelsen OJ, Vendsbor GP, Fahrenkrug J, Rehfeld JF (1984) Vasoactive intestinal polypeptide decreased in cerebrospinal fluid (CSF) in atypical depression. Vasoactive intestinal polypeptide, cholecystokinin and gastrin in CSF in psychiatric disorders. J Affect Disord 7:325-337
27. Glick SD, Ross DA (1981) Lateralization of function in the rat brain. Trends Neurosci 4:196-199
28. Glowa JR, Panlilio LV, Brenneman DE, Gozes I, Fridkin M, Hill JM (1992) Learning impairment following intracerebral administration of the HIV envelope protein gp120 or a VIP antagonist. Brain Res 570:49-53
29. Gozes I, Glowa J, Brenneman DE, McCune SK, Lee E, Westphal H (1993) Learning and sexual deficiencies in transgenic mice carrying a chimeric vasoactive intestinal peptide gene. J Mol Neurosci 4:185-193
30. Gozzani IL, Isquierdo I (1976) Possible peripheral adrenergic and central dopaminergic influences in memory consolidation. Psychopharmacology 49:109-111
31. Harmar AJ, Arimura A, Gozes I, Journot L, Laburthe M, Pisegna JR, Rawlings SR, Robberecht P, Said SI, Sreedharan SP, Wank SA, Waschek JA (1998) International Union of Pharmacology. XVIII. Nomenclature of receptors for vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide. Pharmacol Rev 50:265-270
32. Heine O, Galaburda AM (1986) Olfactory asymmetry in the rat brain. Exp Neurol 91:392-398
33. Hozumi S, Nakagawasai O, Tan-No K, Niijima F, Yamadera F, Murata A, Arai Y, Yasuhara H, Tadano T (2003) Characteristics of changes in cholinergic function and impairment of learning and memory-related behavior induced by olfactory bulbectomy. Behav Brain Res 138:9-15
34. Itoh S, Takashima A, Morimoto T (1994) Impaired spatial learning by vasoactive intestinal peptide in Morris water maze task in the rat. Can J Physiol Pharmacol 72:25-29
35. Ivanova M, Ternianov A, Belcheva S, Tashev R, Negrev N, Belcheva I (2008) Hippocampal asymmetry in exploratory behavior to vasoactive intestinal polypeptide. Peptides 29:940-947
36. Ivanova M, Ternianov A, Tashev R, Belcheva S, Belcheva I (2009) Lateralized learning and memory effects of vasoactive intestinal peptide infused into the rat hippocampal CA1 area. Regul Pept 156:42-46
37. Kelly JP, Wrynn A, Leonard BE (1997) The olfactory bulbectomized rat as a model of depression: an update. Pharmacol Ther 74:299-316
38. Khanna J, Sengupta P (2001) Morphological asymmetry in olfactory bulbs in rat. J Anat Soc India 50:31-33
39. King M, Cairncross KD (1974) Effects of olfactory bulb protections to the para hippocampal area of the rat. J Comp Neurol 198:467-482
40. Kolb B, Sutherland RJ, Nonneman AJ, Whishaw IQ (1982) Asymmetry in the cerebral hemispheres of the rat, mouse, rabbit, and cat: the right hemisphere is larger. Exp Neurol 78:348-359
41. Kronmüller KT, Schröder J, Köhler S, Götz B, Victor D, Unger J, Giesel F, Magnotta V, Mundt C, Essig M, Pantel J (2009) Hippocampal volume in first episode and recurrent depression. Psychiatry Res 174:62-66
42. Kruglikov RI, Orlova NV, Getsova VM (1992) Content of norepinephrine and serotonin in symmetrical divisions of the brain of rats in the norm during learning and with the administration of peptides. Neurosci Behav Physiol 22:128-131
43. Kryzhanovskiǐ GN, Lutsenko VK, Karganov MIu, Beliaev SV (1984) Lateralization of peptide distribution in the brain and the asymmetry of motor control. Patol Fiziol Eksp Ter 3:68-71
44. Loren I, Emson PC, Fahrenkrug J, Bjorklund A, Alumets J, Hakanson R, Sundler F (1979) Distribution of vasoactive intestinal polypeptide in the rat and mouse brain. Neuroscience 4:1953-1976
45. Magistretti PJ, Sorg O, Yu N, Martin JL, Pellerin L (1993) Neurotransmitters regulate energy metabolism in astrocytes: implications for the metabolic trafficking between neural cells. Dev Neurosci 5:306-312
46. Magistretti PJ, Cardinaux JR, Martin JL (1998) VIP and PACAP in the CNS: regulators of glial energy metabolism and modulators of glutamatergic signaling. Ann N Y Acad Sci 865:213-225
47. Malinow R, Schulman H, Tsien RW (1989) Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP. Science 245:862-866
48. Masuo Y, Matsumoto Y, Tokito F, Tsuda M, Fujino M (1993) Effects of vasoactive intestinal polypeptide (VIP) and pituitary adenylate cyclase activating polypeptide (PACAP) on the spontaneous release of acetylcholine from the rat hippocampus by brain microdialysis. Brain Res 611:207-215
49. Matsuyama S, Matsumoto A, Hashimoto H, Shintani N, Baba A (2003) Impaired long-term potentiation in vivo in the dentate gyrus of pituitary adenylate cyclase-activating polypeptide (PACAP) or PACAP type 1 receptor-mutant mice. Neuroreport 14:2095-2098
50. McCulloch J, Kelly PA (1983) A functional role for vasoactive intestinal polypeptide in anterior cingulate cortex. Nature 304:438-440
51. Moriguchi S, Han F, Nakagawasai O, Tadano T, Fukunaga K (2006) Decreased calcium/calmoculin-dependent protein kinase II and protein kinase C activities mediate impairment of hippocampal long-term potentiation in the olfactory bulbectomized mice. J Neurochem 97:22-29
52. Niewiadomski P, Nowak JZ, Sedkowska P, Zawilska JB (2002) Rapid desensitization of receptors for pituitary adenylate cyclase-activating polypeptide (PACAP) in chick cerebral cortex. Pol J Pharmacol 54:717-721
53. Otto C, Kovalchuk Y, Wolfer DP, Gass P, Martin M, Zuschratter W, Grone HJ, Kellendonk C, Tronche F, Maldonado R, Lipp HP, Konnerth A, Schutz G (2001) Impairment of mossy fiber long-term potentiation and associative learning in pituitary adenylate cyclase activating polypeptide type I receptor-deficient mice. J Neurosci 21:5520-5527
54. Pearlson GD, Robinson RG (1981) Suction lesions of the frontal cerebral cortex in the rat induce asymmetrical behavioral and catecholaminergic responses. Brain Res 218:233-242
55. Pellegrino LJ, Cushman AJ (1967) A stereotaxic atlas of the rat brain. Appleton-Century-Crofts, New York
56. Petkov VD, Kehayov R, Belcheva S, Konstantinova E, Petkov VV, Getova D, Markovska V (1993) Memory effects of standardized extracts of Panax ginseng (G115), Ginkgo biloba (GK501) and their combination Gincosan (PHL-00701). Planta Med 59:106-114
57. Rafaelsen OJ, Gjerris A (1985) Neuropeptides in the cerebrospinal fluid (CSF) in psychiatric disorders. Prog Neuropsychopharmacol Biol Psychiatry 9:533-538
58. Ramírez M, Prieto I, Vives F, de Gasparo M, Alba F (2004) Neuropeptides, neuropeptidases and brain asymmetry. Curr Protein Pept Sci 5:497-506
59. Roberto M, Scuri R, Brunelli M (2001) Differential effects of PACAP-38 on synaptic responses in rat hippocampal CA1 region. Learn Mem 8:265-271
60. Rosselin G, Maletti M, Besson J, Rostène W (1982) A new neuroregulator: the vasoactive intestinal peptide or VIP. Mol Cell Endocrinol 27:243-262
61. Said SI, Rosenberg R (1976) Vasoactive intestinal polypeptide: abundant immunoreactivity in neural cell lines and normal nervous tissues. Science 192:907-908
62. Saiz Ruiz J, Carrasco Perera JL, Hernanz A (1992) Plasma neuropeptides in affective and anxiety disorders. Arch Neurobiol (Madr) 55:1-5
63. Sauvage M, Brabet P, Holsboer F, Bockaert J, Steckler T (2000) Mild deficits in mice lacking pituitary adenylate cyclase-activating polypeptide receptor type 1 (PAC1) performing on memory tasks. Brain Res Mol Brain Res 84:79-89
64. Sexton PM,MorfisM, Tilakaratne N, Hay DL, Udawela M, Christopoulos G, Christopoulos A (2006) Complexing receptor pharmacology: modulation of family B G protein-coupled receptor function by RAMPs. Ann N YAcad Sci 1070:90-104
65. Shinohara Y, Hirase H,WatanabeM, Itakura M, TakahashiM, Shigemoto R (2008) Left-right asymmetry of the hippocampal synapses with differential subunit allocation of glutamate receptors. Proc Natl Acad Sci U S A 105:19498-19503
66. Shinohara Y, Hosoya A, Yamasaki N, Ahmed H, Hattori S Eguchi M, Yamaguchi S, Miyakawa T, Hirase H, Shigemoto R (2010) Righthemispheric dominance of spatial memory in split-brain mice. Hippocampus. Nov 10. [Epub ahead of print]
67. Shintani N, Hashimoto H, Kunugi A, Koyama Y, Yamamoto K, Tomimoto S, Mori W, Matsuda T, Baba A (2000) Desensitization, surface expression, and glycosylation of a functional, epitope-tagged type I PACAP (PAC(1)) receptor. Biochim Biophys Acta 1509:195-202
68. Skelin I, Sato H, Diksic M (2008) Olfactory bulbectomy reduces cerebral glucose utilization: 2-[14 C] deoxyglucose autoradiographic study. Brain Res Bull 76:485-492
69. Tadano T, Hozumi S, Yamadera F, Murata A, Niijima F, Tan-No K, Nakagawasai O, Kisara K (2004) Effects of NMDA receptor-related agonists on learning and memory impairment in olfactory bulbectomized mice. Methods Find Exp Clin Pharmacol 26:93-97
70. Takashima A, Maeda Y, Itoh S (1993) Influence of chronic intracerebro-vascular infusion of vasoactive intestinal peptide on memory processes in Morris water pool test in the rat. Peptides 14:1073-1078
71. Tang AC, Reeb BC, Romeo RD, McEwen BS (2003) Modification of social memory, hypothalamic-pituitary-adrenal axis, and brain asymmetry by neonatal novelty exposure. J Neurosci 23:8254-8260
72. Telegdy G, Kokavszky K (2000) The action of pituitary adenylate cyclase activating polypeptide (PACAP) on passive avoidance learning. The role of transmitters. Brain Res 874:194-199
73. van Riezen H, Leonard BE (1990) Effects of psychotropic drugs on the behavior and neurochemistry of olfactory bulbectomized rats. Pharmacol Ther 47:21-34
74. Van Riezen H, Schnieden H, Wren AF (1977) Olfactory bulb ablation in the rat: behavioural changes and their reversal by antidepressant drugs. Br J Pharmacol 60:521-528
75. Vaudry D, Gonzalez BJ, Basille M, Yon L, Fournier A, Vaudry H (2000) Pituitary adenylate cyclase-activating polypeptide and its receptors: from structure to functions. Pharmacol Rev 52:269-324
76. Yamaguchi Y, Kobayashi H (1994) Effects of vasoactive intestinal peptide (VIP) on scopolamine-induced amnesia in the rat. Neuropeptides 26:153-158
77. Yang K, Trepanier CH, Li H, Beazely MA, Lerner EA, Jackson MF, Macdonald JF (2009) Vasoactive intestinal peptide acts via multiple signal pathways to regulate hippocampal NMDA receptors and synaptic transmission. Hippocampus 19:779-789
78. Yang K, Lei G, Jackson MF, Macdonald JF (2010) The involvement of PACAP/VIP system in the synaptic transmission in the hippocampus. J Mol Neurosci 42:319-326