Imipramine treatment increases the number of hippocampal synapses and neurons in a genetic animal model of depression

Hippocampus

Volumn 20, Issue 12, 2010, Pages 1376-1384

  Chen, Fenghua ^a   Madsen, Torsten M ^a,b   Wegener, Gregers ^a   Nyengaard, Jens R ^a  

^a AARHUS UNIVERSITY HOSPITAL   (Denmark)

^b H LUNDBECK A S   (Denmark)

Author keywords

FSL rats; Hippocampus; Neurogenesis; Stereology; Synaptogenesis

Indexed keywords

IMIPRAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL VIABILITY; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; DEPRESSION; FORCED SWIMMING TEST; GENETIC MODEL; GENETIC SUSCEPTIBILITY; GRANULE CELL; HIPPOCAMPUS; IMMOBILIZATION; MALE; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; STEREOLOGY; SYNAPSE; SYNAPTOGENESIS;

ANALYSIS OF VARIANCE; ANIMALS; ANTIDEPRESSIVE AGENTS; CELL COUNT; DEPRESSION; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; IMIPRAMINE; MALE; NEURONAL PLASTICITY; NEURONS; RATS; SYNAPSES;

EID: 78649555853     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.20718     Document Type: Article

References (73)

1. Baks-Te BL, Wouterlood FG, Vinkenoog M, Witter MP. 2005. Entorhinal projections terminate onto principal neurons and interneurons in the subiculum: A quantitative electron microscopical analysis in the rat. Neuroscience 136: 729-739.
2. Bjornebekk A, Mathe AA, Brene S. 2005. The antidepressant effect of running is associated with increased hippocampal cell proliferation. Int J Neuropsychopharmacol 8: 357-368.
3. Burwell RD, Witter MP, Amaral DG. 1995. Perirhinal and postrhinal cortices of the rat: A review of the neuroanatomical literature and comparison with findings from the monkey brain. Hippocampus 5: 390-408.
4. Calverley RK, Jones DG. 1990. Contributions of dendritic spines and perforated synapses to synaptic plasticity. Brain Res Brain Res Rev 15: 215-249.
5. Campbell S, Macqueen G. 2004. The role of the hippocampus in the pathophysiology of major depression. J Psychiatry Neurosci 29: 417-426.
6. Carlisle HJ, Kennedy MB. 2005. Spine architecture and synaptic plasticity. Trends Neurosci 28: 182-187.
7. Castren E, Voikar V, Rantamaki T. 2007. Role of neurotrophic factors in depression. Curr Opin Pharmacol 7: 18-21.
8. Chen F, Madsen TM, Wegener G, Nyengaard JR. 2008. Changes in rat hippocampal CA1 synapses following imipramine treatment. Hippocampus 18: 631-639.
9. Chen F, Madsen TM, Wegener G, Nyengaard JR. 2009. Repeated electroconvulsive seizures increase the total number of synapses in adult male rat hippocampus. Eur Neuropsychopharmacol 19: 329-338.
10. Czeh B, Michaelis T, Watanabe T, Frahm J, de Biurrun G, van Kampen M, Bartolomucci A, Fuchs E. 2001. Stress-induced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressant treatment with tianeptine. Proc Natl Acad Sci USA 98: 12796-12801.
11. Dorph-Petersen KA, Nyengaard JR, Gundersen HJ. 2001. Tissue shrinkage and unbiased stereological estimation of particle number and size. J Microsci 204: 232-246.
12. Duman RS. 2002a. Structural alterations in depression: Cellular mechanisms underlying pathology and treatment of mood disorders. CNS Spectr 7: 140-147.
13. Duman RS. 2002b. Synaptic plasticity and mood disorders. Mol Psychiatry 7(Suppl 1): S29-S34.
14. Duman RS. 2004. Depression: A case of neuronal life and death? Biol Psychiatry 56: 140-145.
15. Freund TF, Buzsaki G. 1996. Interneurons of the hippocampus. Hippocampus 6: 347-470.
16. Frodl T, Meisenzahl EM, Zetzsche T, Born C, Groll C, Jager M, Leinsinger G, Bottlender R, Hahn K, Moller HJ. 2002. Hippocampal changes in patients with a first episode of major depression. Am J Psychiatry 159: 1112-1118.
17. Fuchs E, Czeh B, Kole MH, Michaelis T, Lucassen PJ. 2004. Alterations of neuroplasticity in depression: The hippocampus and beyond. Eur Neuropsychopharmacol 14(Suppl 5): S481-S490.
18. Fuchs E, Czeh B, Michaelis T, de Biurrun G, Watanabe T, Frahm J. 2002. Synaptic plasticity and tianeptine: structural regulation. Eur Psychiatry 17(Suppl 3): 311-317.
19. Ganeshina O, Berry RW, Petralia RS, Nicholson DA, Geinisman Y. 2004. Differences in the expression of AMPA and NMDA receptors between axospinous perforated and nonperforated synapses are related to the configuration and size of postsynaptic densities. J Comp Neurol 468: 86-95.
20. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H. 2006. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439: 589-593.
21. Geinisman Y. 2000. Structural synaptic modifications associated with hippocampal LTP, behavioral learning. Cereb Cortex 10: 952-962.
22. Geinisman Y, Berry RW, Disterhoft JF, Power JM, van der Zee EA. 2001. Associative learning elicits the formation of multiple-synapse boutons. J Neurosci 21: 5568-5573.
23. Grady MS, Charleston JS, Maris D, Witgen BM, Lifshitz J. 2003. Neuronal and glial cell number in the hippocampus after experimental traumatic brain injury: Analysis by stereological estimation. J Neurotrauma 20: 929-941.
24. Gresack JE, Frick KM. 2004. Environmental enrichment reduces the mnemonic and neural benefits of estrogen. Neuroscience 128: 459-471.
25. Gundersen HJ. 1986. Stereology of arbitrary particles. A review of unbiased number and size estimators and the presentation of some new ones, in memory of William R. Thompson. J Microsci 143(Part 1): 3-45.
26. Hajszan T, MacLusky NJ, Leranth C. 2005. Short-term treatment with the antidepressant fluoxetine triggers pyramidal dendritic spine synapse formation in rat hippocampus. Eur J Neurosci 21: 1299-1303.
27. Hajszan T, Dow A, Warner-Schmidt JL, Szigeti-Buck K, Sallam NL, Parducz A, Leranth C, Duman RS. 2009. Remodeling of hippocampal spine synapses in the rat learned helplessness model of depression. Biol Psychiatry 65: 392-400.
28. Hellsten J, Wennstrom M, Mohapel P, Ekdahl CT, Bengzon J, Tingstrom A. 2002. Electroconvulsive seizures increase hippocampal neurogenesis after chronic corticosterone treatment. Eur J Neurosci 16: 283-290.
29. Hering H, Sheng M. 2001. Dendritic spines: Structure, dynamics and regulation. Nat Rev Neurosci 2: 880-888.
30. Jessberger S, Kempermann G. 2003. Adult-born hippocampal neurons mature into activity-dependent responsiveness. Eur J Neurosci 18: 2707-2712.
31. Lucassen PJ, Muller MB, Holsboer F, Bauer J, Holtrop A, Wouda J, Hoogendijk WJ, De Kloet ER, Swaab DF. 2001. Hippocampal apoptosis in major depression is a minor event and absent from subareas at risk for glucocorticoid overexposure. Am J Pathol 158: 453-468.
32. Luscher C, Nicoll RA, Malenka RC, Muller D. 2000. Synaptic plasticity and dynamic modulation of the postsynaptic membrane. Nat Neurosci 3: 545-550.
33. MacQueen GM, Campbell S, McEwen BS, Macdonald K, Amano S, Joffe RT, Nahmias C, Young LT. 2003a. Course of illness, hippocampal function, and hippocampal volume in major depression. Proc Natl Acad Sci USA 100: 1387-1392.
34. MacQueen GM, Ramakrishnan K, Ratnasingan R, Chen B, Young LT. 2003b. Desipramine treatment reduces the long-term behavioural and neurochemical sequelae of early-life maternal separation. Int J Neuropsychopharmacol 6: 391-396.
35. Madsen TM, Treschow A, Bengzon J, Bolwig TG, Lindvall O, Tingstrom A. 2000. Increased neurogenesis in a model of electroconvulsive therapy. Biol Psychiatry 47: 1043-1049.
36. Magarinos AM, Orchinik M, McEwen BS. 1998. Morphological changes in the hippocampal CA3 region induced by non-invasive glucocorticoid administration: A paradox. Brain Res 809: 314-318.
37. Malberg JE, Eisch AJ, Nestler EJ, Duman RS. 2000. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20: 9104-9110.
38. Manji HK, Drevets WC, Charney DS. 2001. The cellular neurobiology of depression. Nat Med 7: 541-547.
39. McEwen BS. 1999. Stress and hippocampal plasticity. Annu Rev Neurosci 22: 105-122.
40. McEwen BS. 2000. The neurobiology of stress: From serendipity to clinical relevance. Brain Res 886: 172-189.
41. McEwen BS, Magarinos AM. 2001. Stress and hippocampal plasticity: Implications for the pathophysiology of affective disorders. Hum Psychopharmacol 16: S7-S19.
42. McEwen BS, Magarinos AM, Reagan LP. 2002. Structural plasticity and tianeptine: Cellular and molecular targets. Eur Psychiatry 17(Suppl 3): 318-330.
43. Megias M, Emri Z, Freund TF, Gulyas AI. 2001. Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102: 527-540.
44. Nestler EJ, Barrot M, DiLeone RJ, Eisch AJ, Gold SJ, Monteggia LM. 2002. Neurobiology of depression. Neuron 34: 13-25.
45. O'Connor JJ, Rowan MJ, Anwyl R. 1993. Use-dependent effects of acute and chronic treatment with imipramine and buspirone on excitatory synaptic transmission in the rat hippocampus in vivo. Naunyn Schmiedebergs Arch Pharmacol 348: 158-163.
46. Overstreet DH. 1993. The Flinders sensitive line rats: A genetic animal model of depression. Neurosci Biobehav Rev 17: 51-68.
47. Overstreet DH. 2002. Behavioral characteristics of rat lines selected for differential hypothermic responses to cholinergic or serotonergic agonists. Behav Genet 32: 335-348.
48. Overstreet DH, Friedman E, Mathe AA, Yadid G. 2005. The Flinders Sensitive Line rat: A selectively bred putative animal model of depression. Neurosci Biobehav Rev 29: 739-759.
49. Overstreet DH, Pucilowski O, Rezvani AH, Janowsky DS. 1995. Administration of antidepressants, diazepam and psychomotor stimulants further confirms the utility of Flinders Sensitive Line rats as an animal model of depression. Psychopharmacology (Berl) 121: 27-37.
50. Perera TD, Coplan JD, Lisanby SH, Lipira CM, Arif M, Carpio C, Spitzer G, Santarelli L, Scharf B, Hen R, Rosoklija G, Sackeim HA, Dwork AJ. 2007. Antidepressant-induced neurogenesis in the hippocampus of adult nonhuman primates. J Neurosci 27: 4894-4901.
51. Petersen A, Wortwein G, Gruber SH, Mathe AA. 2008. Escitalopram reduces increased hippocampal cytogenesis in a genetic rat depression model. Neurosci Lett 436: 305-308.
52. Pittenger C, Duman RS. 2008. Stress, depression, and neuroplasticity: A convergence of mechanisms. Neuropsychopharmacology 33: 88-109.
53. Popoli M, Gennarelli M, Racagni G. 2002. Modulation of synaptic plasticity by stress and antidepressants. Bipolar Disord 4: 166-182.
54. Porsolt RD, Anton G, Blavet N, Jalfre M. 1978. Behavioural despair in rats: A new model sensitive to antidepressant treatments. Eur J Pharmacol 47: 379-391.
55. Prange-Kiel J, Rune GM. 2006. Direct and indirect effects of estrogen on rat hippocampus. Neuroscience 138: 765-772.
56. Prange-Kiel J, Rune GM, Leranth C. 2004. Median raphe mediates estrogenic effects to the hippocampus in female rats. Eur J Neurosci 19: 309-317.
57. Reif A, Fritzen S, Finger M, Strobel A, Lauer M, Schmitt A, Lesch KP. 2006. Neural stem cell proliferation is decreased in schizophrenia, but not in depression. Mol Psychiatry 11: 514-522.
58. Ressler KJ, Nemeroff CB. 2000. Role of serotonergic and noradrenergic systems in the pathophysiology of depression and anxiety disorders. Depress Anxiety 12(Suppl 1): 2-19.
59. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S, Weisstaub N, Lee J, Duman R, Arancio O, Belzung C, Hen R. 2003. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301: 805-809.
60. Scott BW, Wojtowicz JM, Burnham WM. 2000. Neurogenesis in the dentate gyrus of the rat following electroconvulsive shock seizures. Exp Neurol 165: 231-236.
61. Sheline YI, Gado MH, Kraemer HC. 2003. Untreated depression and hippocampal volume loss. Am J Psychiatry 160: 1516-1518.
62. Small JV. 1968. Measurement of section thickness. Fourth European Conference on Electron Microscopy. pp 609-610.
63. Sousa N, Lukoyanov NV, Madeira MD, Almeida OF, Paula-Barbosa MM. 2000. Erratum to "Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement". Neuroscience 101: 483
64. Steffens DC, Byrum CE, McQuoid DR, Greenberg DL, Payne ME, Blitchington TF, MacFall JR, Krishnan KR. 2000. Hippocampal volume in geriatric depression. Biol Psychiatry 48: 301-309.
65. Sterio DC. 1984. The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsci 134(Part 2): 127-136.
66. Tang Y, Nyengaard JR, De Groot DM, Gundersen HJ. 2001. Total regional and global number of synapses in the human brain neocortex. Synapse 41: 258-273.
67. Toni N, Buchs PA, Nikonenko I, Bron CR, Muller D. 1999. LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature 402: 421-425.
68. Toni N, Buchs PA, Nikonenko I, Povilaitite P, Parisi L, Muller D. 2001. Remodeling of synaptic membranes after induction of long-term potentiation. J Neurosci 21: 6245-6251.
69. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH. 2002. Functional neurogenesis in the adult hippocampus. Nature 415: 1030-1034.
70. Vollmayr B, Simonis C, Weber S, Gass P, Henn F. 2003. Reduced cell proliferation in the dentate gyrus is not correlated with the development of learned helplessness. Biol Psychiatry 54: 1035-1040.
71. Warner-Schmidt JL, Duman RS. 2006. Hippocampal neurogenesis: opposing effects of stress and antidepressant treatment. Hippocampus 16: 239-249.
72. West MJ, Slomianka L, Gundersen HJ. 1991. Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231: 482-497.
73. Zhao C, Deng W, Gage FH. 2008. Mechanisms and functional implications of adult neurogenesis. Cell 132: 645-660.