Adolescent escitalopram administration modifies neurochemical alterations in the hippocampus of maternally separated rats

European Neuropsychopharmacology

Volumn 20, Issue 12, 2010, Pages 875-883

  Hui, Jiaojie ^a,b   Zhang, Zhijun ^a,b   Liu, Shanshan ^a,b   Xi, Guangjun ^a,b   Zhang, Xiangrong ^a,b   Teng, GaoJun ^a,c   Chan, Kevin C ^d   Wu, Ed X ^d   Nie, Binbin ^e,f   Shan, Baoci ^f   Li, Lingjiang ^g   Reynolds, Gavin P ^h  

^a MEDICAL SCHOOL OF SOUTHEAST UNIVERSITY   (China)

^b AFFILIATED ZHONGDA HOSPITAL OF SOUTHEAST UNIVERSITY   (China)

^c SOUTHEAST UNIVERSITY   (China)

^d UNIVERSITY OF HONG KONG   (Hong Kong)

^e ZHENGZHOU UNIVERSITY   (China)

^f INSTITUTE OF HIGH ENERGY PHYSICS   (China)

^g CENTRAL SOUTH UNIVERSITY   (China)

^h QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

Escitalopram; Hippocampus; Magnetic resonance imaging; Maternal separation; Proton magnetic resonance spectroscopy; Rat

Indexed keywords

CHOLINE; CREATINE; ESCITALOPRAM; GLUTAMIC ACID; INOSITOL; N ACETYLASPARTIC ACID;

ADOLESCENCE; ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; BRAIN SIZE; CONTROLLED STUDY; EARLY LIFE STRESS; FEMALE; HEMISPHERIC DOMINANCE; HIPPOCAMPUS; LEFT HEMISPHERE; MALE; MATERNAL DEPRIVATION; NEUROCHEMISTRY; NEWBORN; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PERINATAL PERIOD; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; RAT; RIGHT HEMISPHERE; SEX DIFFERENCE;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; CITALOPRAM; FEMALE; HIPPOCAMPUS; MAGNETIC RESONANCE IMAGING; MALE; MATERNAL DEPRIVATION; ORGAN SIZE; RATS; RATS, SPRAGUE-DAWLEY;

EID: 77958180396     PISSN: 0924977X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.euroneuro.2010.08.010     Document Type: Article

References (70)

1. Atwood T., Payne V.S., Zhao W., Brown W.R., Wheeler K.T., Zhu J.M., Robbins M.E. Quantitative magnetic resonance spectroscopy reveals a potential relationship between radiation-induced changes in rat brain metabolites and cognitive impairment. Radiat. Res. 2007, 168(5):574-581.
2. Banasr M., Duman R.S. Regulation of neurogenesis and gliogenesis by stress and antidepressant treatment. CNS Neurol. Disord. Drug Targets 2007, 6(5):311-320.
3. Baslow M.H. N-acetylaspartate in the vertebrate brain: metabolism and function. Neurochem. Res. 2003, 28(6):941-953.
4. Brand A., Richter-Landsberg C., Leibfritz D. Multinuclear NMR studies on the energy metabolism of glial and neuronal cells. Dev. Neurosci. 1993, 15(3-5):289-298.
5. Bremner J.D., Randall P., Vermetten E., Staib L., Bronen R.A., Mazure C., Capelli S., McCarthy G., Innis R.B., Charney D.S. Magnetic resonance imaging-based measurement of hippocampal volume in posttraumatic stress disorder related to childhood physical and sexual abuse - a preliminary report. Biol. Psychiatry 1997, 41(1):23-32.
6. Bremner J.D., Vythilingam M., Vermetten E., Southwick S.M., McGlashan T., Nazeer A., Khan S., Vaccarino L.V., Soufer R., Garg P.K., Ng C.K., Staib L.H., Duncan J.S., Charney D.S. MRI and PET study of deficits in hippocampal structure and function in women with childhood sexual abuse and posttraumatic stress disorder. Am. J. Psychiatry 2003, 160(5):924-932.
7. Caetano S.C., Fonseca M., Olvera R.L., Nicoletti M., Hatch J.P., Stanley J.A., Hunter K., Lafer B., Pliszka S.R., Soares J.C. Proton spectroscopy study of the left dorsolateral prefrontal cortex in pediatric depressed patients. Neurosci. Lett. 2005, 384(3):321-326.
8. Capizzano A.A., Jorge R.E., Acion L.C., Robinson R.G. In vivo proton magnetic resonance spectroscopy in patients with mood disorders: a technically oriented review. J. Magn. Reson. Imaging 2007, 26(6):1378-1389.
9. Chan J.R., Phillips L.J., Glaser M. Glucocorticoids and progestins signal the initiation and enhance the rate of myelin formation. Proc. Natl. Acad. Sci. USA 1998, 95(18):10459-10464.
10. Chan K.C., Khong P.L., Cheung M.M., Wang S., Cai K.X., Wu E.X. MRI of late microstructural and metabolic alterations in radiation-induced brain injuries. J. Magn. Reson. Imaging 2009, 29(5):1013-1020.
11. Clark R.E., Zola S.M., Squire L.R. Impaired recognition memory in rats after damage to the hippocampus. J. Neurosci. 2000, 20(23):8853-8860.
12. Cohen R.A., Grieve S., Hoth K.F., Paul R.H., Sweet L., Tate D., Gunstad J., Stroud L., McCaffery J., Hitsman B., Niaura R., Clark C.R., McFarlane A., Bryant R., Gordon E., Williams L.M. Early life stress and morphometry of the adult anterior cingulate cortex and caudate nuclei. Biol. Psychiatry 2006, 59(10):975-982.
13. Coupland N.J., Ogilvie C.J., Hegadoren K.M., Seres P., Hanstock C.C., Allen P.S. Decreased prefrontal Myo-inositol in major depressive disorder. Biol. Psychiatry 2005, 57(12):1526-1534.
14. Cudalbu C., Cavassila S., Rabeson H., van O.D., Graveron-Demilly D. Influence of measured and simulated basis sets on metabolite concentration estimates. NMR Biomed. 2008, 21(6):627-636.
15. Cui M., Yang Y., Yang J., Zhang J., Han H., Ma W., Li H., Mao R., Xu L., Hao W., Cao J. Enriched environment experience overcomes the memory deficits and depressive-like behavior induced by early life stress. Neurosci. Lett. 2006, 404(1-2):208-212.
16. Czeh B., Simon M., Schmelting B., Hiemke C., Fuchs E. Astroglial plasticity in the hippocampus is affected by chronic psychosocial stress and concomitant fluoxetine treatment. Neuropsychopharmacology 2006, 31(8):1616-1626.
17. Dave V., Kimelberg H.K. Na(+)-dependent, fluoxetine-sensitive serotonin uptake by astrocytes tissue-printed from rat cerebral cortex. J. Neurosci. 1994, 14(8):4972-4986.
18. De B.M., Keshavan M.S., Spencer S., Hall J. N-Acetylaspartate concentration in the anterior cingulate of maltreated children and adolescents with PTSD. Am. J. Psychiatry 2000, 157(7):1175-1177.
19. Deicken R.F., Zhou L., Schuff N., Fein G., Weiner M.W. Hippocampal neuronal dysfunction in schizophrenia as measured by proton magnetic resonance spectroscopy. Biol. Psychiatry 1998, 43(7):483-488.
20. Driessen M., Herrmann J., Stahl K., Zwaan M., Meier S., Hill A., Osterheider M., Petersen D. Magnetic resonance imaging volumes of the hippocampus and the amygdala in women with borderline personality disorder and early traumatization. Arch. Gen. Psychiatry 2000, 57(12):1115-1122.
21. El K.A., Gruber S.H., Mork A., Mathe A.A. Adult life behavioral consequences of early maternal separation are alleviated by escitalopram treatment in a rat model of depression. Prog. Neuropsychopharmacol. Biol. Psychiatry 2006, 30(3):535-540.
22. Eren I., Naziroglu M., Demirdas A. Protective effects of lamotrigine, aripiprazole and escitalopram on depression-induced oxidative stress in rat brain. Neurochem. Res. 2007, 32(7):1188-1195.
23. Freeman T.W., Cardwell D., Karson C.N., Komoroski R.A. In vivo proton magnetic resonance spectroscopy of the medial temporal lobes of subjects with combat-related posttraumatic stress disorder. Magn. Reson. Med. 1998, 40(1):66-71.
24. Golembiowska K., Dziubina A. Effect of acute and chronic administration of citalopram on glutamate and aspartate release in the rat prefrontal cortex. Pol. J. Pharmacol. 2000, 52(6):441-448.
25. Gruetter R. Automatic, localized in vivo adjustment of all first- and second-order shim coils. Magn. Reson. Med. 1993, 29(6):804-811.
26. Gupta R.K., Bhatia V., Poptani H., Gujral R.B. Brain metabolite changes on in vivo proton magnetic resonance spectroscopy in children with congenital hypothyroidism. J. Pediatr. 1995, 126(3):389-392.
27. Heim C., Nemeroff C.B. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol. Psychiatry 2001, 49(12):1023-1039.
28. Hollup S.A., Kjelstrup K.G., Hoff J., Moser M.B., Moser E.I. Impaired recognition of the goal location during spatial navigation in rats with hippocampal lesions. J. Neurosci. 2001, 21(12):4505-4513.
29. Huot R.L., Thrivikraman K.V., Meaney M.J., Plotsky P.M. Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment. Psychopharmacology (Berl) 2001, 158(4):366-373.
30. Inazu M., Takeda H., Ikoshi H., Sugisawa M., Uchida Y., Matsumiya T. Pharmacological characterization and visualization of the glial serotonin transporter. Neurochem. Int. 2001, 39(1):39-49.
31. Irle E., Lange C., Sachsse U. Reduced size and abnormal asymmetry of parietal cortex in women with borderline personality disorder. Biol. Psychiatry 2005, 57(2):173-182.
32. Ito A., Kikusui T., Takeuchi Y., Mori Y. Effects of early weaning on anxiety and autonomic responses to stress in rats. Behav. Brain Res. 2006, 171(1):87-93.
33. Jaako-Movits K., Zharkovsky T., Pedersen M., Zharkovsky A. Decreased hippocampal neurogenesis following olfactory bulbectomy is reversed by repeated citalopram administration. Cell. Mol. Neurobiol. 2006, 26(7-8):1559-1570.
34. Jayatissa M.N., Bisgaard C., Tingstrom A., Papp M., Wiborg O. Hippocampal cytogenesis correlates to escitalopram-mediated recovery in a chronic mild stress rat model of depression. Neuropsychopharmacology 2006, 31(11):2395-2404.
35. Jayatissa M.N., Bisgaard C.F., West M.J., Wiborg O. The number of granule cells in rat hippocampus is reduced after chronic mild stress and re-established after chronic escitalopram treatment. Neuropharmacology 2008, 54(3):530-541.
36. Jin Y., Lim C.M., Kim S.W., Park J.Y., Seo J.S., Han P.L., Yoon S.H., Lee J.K. Fluoxetine attenuates kainic acid-induced neuronal cell death in the mouse hippocampus. Brain Res. 2009, 1281:108-116.
37. Jung R.E., Brooks W.M., Yeo R.A., Chiulli S.J., Weers D.C., Sibbitt W.L. Biochemical markers of intelligence: a proton MR spectroscopy study of normal human brain. Proc. Biol. Sci. 1999, 266(1426):1375-1379.
38. Kalinichev M., Easterling K.W., Plotsky P.M., Holtzman S.G. Long-lasting changes in stress-induced corticosterone response and anxiety-like behaviors as a consequence of neonatal maternal separation in Long-Evans rats. Pharmacol. Biochem. Behav. 2002, 73(1):131-140.
39. Kubota N., Kiuchi Y., Nemoto M., Oyamada H., Ohno M., Funahashi H., Shioda S., Oguchi K. Regulation of serotonin transporter gene expression in human glial cells by growth factors. Eur. J. Pharmacol. 2001, 417(1-2):69-76.
40. Laakso M.P., Vaurio O., Savolainen L., Repo E., Soininen H., Aronen H.J., Tiihonen J. A volumetric MRI study of the hippocampus in type 1 and 2 alcoholism. Behav. Brain Res. 2000, 109(2):177-186.
41. Leventopoulos M., Ruedi-Bettschen D., Knuesel I., Feldon J., Pryce C.R., Opacka-Juffry J. Long-term effects of early life deprivation on brain glia in Fischer rats. Brain Res. 2007, 1142:119-126.
42. Leventopoulos M., Russig H., Feldon J., Pryce C.R., Opacka-Juffry J. Early deprivation leads to long-term reductions in motivation for reward and 5-HT1A binding and both effects are reversed by fluoxetine. Neuropharmacology 2009, 56(3):692-701.
43. Lyons D.M., Afarian H., Schatzberg A.F., Sawyer-Glover A., Moseley M.E. Experience-dependent asymmetric variation in primate prefrontal morphology. Behav. Brain Res. 2002, 136(1):51-59.
44. Lyoo I.K., Renshaw P.F. Magnetic resonance spectroscopy: current and future applications in psychiatric research. Biol. Psychiatry 2002, 51(3):195-207.
45. Mahmutyazicioglu K., Konuk N., Ozdemir H., Atasoy N., Atik L., Gundogdu S. Evaluation of the hippocampus and the anterior cingulate gyrus by proton MR spectroscopy in patients with post-traumatic stress disorder. Diagn. Interv. Radiol. 2005, 11(3):125-129.
46. Malberg J.E., Eisch A.J., Nestler E.J., Duman R.S. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 2000, 20(24):9104-9110.
47. Marais L., Hattingh S.M., Stein D.J., Daniels W.M. A proteomic analysis of the ventral hippocampus of rats subjected to maternal separation and escitalopram treatment. Metab. Brain Dis. 2009, 24(4):569-586.
48. Marco E.M., Adriani W., Canese R., Podo F., Viveros M.P., Laviola G. Enhancement of endocannabinoid signalling during adolescence: modulation of impulsivity and long-term consequences on metabolic brain parameters in early maternally deprived rats. Pharmacol. Biochem. Behav. 2007, 86(2):334-345.
49. Mathew S.J., Shungu D.C., Mao X., Smith E.L., Perera G.M., Kegeles L.S., Perera T., Lisanby S.H., Rosenblum L.A., Gorman J.M., Coplan J.D. A magnetic resonance spectroscopic imaging study of adult nonhuman primates exposed to early-life stressors. Biol. Psychiatry 2003, 54(7):727-735.
50. Mathew S.J., Price R.B., Mao X., Smith E.L., Coplan J.D., Charney D.S., Shungu D.C. Hippocampal N-acetylaspartate concentration and response to riluzole in generalized anxiety disorder. Biol. Psychiatry 2008, 63(9):891-898.
51. Miller B.L. A review of chemical issues in 1H NMR spectroscopy: N-acetyl-l-aspartate, creatine and choline. NMR Biomed. 1991, 4(2):47-52.
52. Mirescu C., Peters J.D., Gould E. Early life experience alters response of adult neurogenesis to stress. Nat. Neurosci. 2004, 7(8):841-846.
53. Mohanakrishnan M.P., Nasrallah H.A., Lyons J.A., Scott M.F., Liberto V. Single-voxel proton MR spectroscopy of right versus left hippocampi in PTSD. Psychiatry Res. 2003, 123(2):101-108.
54. Murugavel M., Sullivan J.M. Automatic cropping of MRI rat brain volumes using pulse coupled neural networks. Neuroimage 2009, 45(3):845-854.
55. Newman E.A. New roles for astrocytes: regulation of synaptic transmission. Trends Neurosci. 2003, 26(10):536-542.
56. Rosenberg D.R., Macmaster F.P., Mirza Y., Smith J.M., Easter P.C., Banerjee S.P., Bhandari R., Boyd C., Lynch M., Rose M., Ivey J., Villafuerte R.A., Moore G.J., Renshaw P. Reduced anterior cingulate glutamate in pediatric major depression: a magnetic resonance spectroscopy study. Biol. Psychiatry 2005, 58(9):700-704.
57. Sanchez M.M., Ladd C.O., Plotsky P.M. Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models. Dev. Psychopathol. 2001, 13(3):419-449.
58. Schuff N., Neylan T.C., Lenoci M.A., Du A.T., Weiss D.S., Marmar C.R., Weiner M.W. Decreased hippocampal N-acetylaspartate in the absence of atrophy in posttraumatic stress disorder. Biol. Psychiatry 2001, 50(12):952-959.
59. Schuff N., Neylan T.C., Fox-Bosetti S., Lenoci M., Samuelson K.W., Studholme C., Kornak J., Marmar C.R., Weiner M.W. Abnormal N-acetylaspartate in hippocampus and anterior cingulate in posttraumatic stress disorder. Psychiatry Res. 2008, 162(2):147-157.
60. Spinelli S., Chefer S., Suomi S.J., Higley J.D., Barr C.S., Stein E. Early-life stress induces long-term morphologic changes in primate brain. Arch. Gen. Psychiatry 2009, 66(6):658-665.
61. Stevenson C.W., Halliday D.M., Marsden C.A., Mason R. Early life programming of hemispheric lateralization and synchronization in the adult medial prefrontal cortex. Neuroscience 2008, 155(3):852-863.
62. Tsai G., Passani L.A., Slusher B.S., Carter R., Baer L., Kleinman J.E., Coyle J.T. Abnormal excitatory neurotransmitter metabolism in schizophrenic brains. Arch. Gen. Psychiatry 1995, 52(10):829-836.
63. Villarreal G., Petropoulos H., Hamilton D.A., Rowland L.M., Horan W.P., Griego J.A., Moreshead M., Hart B.L., Brooks W.M. Proton magnetic resonance spectroscopy of the hippocampus and occipital white matter in PTSD: preliminary results. Can. J. Psychiatry 2002, 47(7):666-670.
64. Vythilingam M., Heim C., Newport J., Miller A.H., Anderson E., Bronen R., Brummer M., Staib L., Vermetten E., Charney D.S., Nemeroff C.B., Bremner J.D. Childhood trauma associated with smaller hippocampal volume in women with major depression. Am. J. Psychiatry 2002, 159(12):2072-2080.
65. Wang J.W., David D.J., Monckton J.E., Battaglia F., Hen R. Chronic fluoxetine stimulates maturation and synaptic plasticity of adult-born hippocampal granule cells. J. Neurosci. 2008, 28(6):1374-1384.
66. Watson C., Andermann F., Gloor P., Jones-Gotman M., Peters T., Evans A., Olivier A., Melanson D., Leroux G. Anatomic basis of amygdaloid and hippocampal volume measurement by magnetic resonance imaging. Neurology 1992, 42(9):1743-1750.
67. Weniger G., Lange C., Sachsse U., Irle E. Amygdala and hippocampal volumes and cognition in adult survivors of childhood abuse with dissociative disorders. Acta Psychiatr. Scand. 2008, 118(4):281-290.
68. Woon F.L., Hedges D.W. Hippocampal and amygdala volumes in children and adults with childhood maltreatment-related posttraumatic stress disorder: a meta-analysis. Hippocampus 2008, 18(8):729-736.
69. Yildiz-Yesiloglu A., Ankerst D.P. Review of 1H magnetic resonance spectroscopy findings in major depressive disorder: a meta-analysis. Psychiatry Res. 2006, 147(1):1-25.
70. Young E.A., Kornstein S.G., Marcus S.M., Harvey A.T., Warden D., Wisniewski S.R., Balasubramani G.K., Fava M., Trivedi M.H., John R.A. Sex differences in response to citalopram: a STAR*D report. J. Psychiatr. Res. 2009, 43(5):503-511.