Distinct structural plasticity in the hippocampus and amygdala of the middle-aged common marmoset (Callithrix jacchus)

Experimental Neurology

Volumn 230, Issue 2, 2011, Pages 291-301

  Marlatt, Michael W ^a   Philippens, Ingrid ^b   Manders, Erik ^c   Czéh, Boldizsár ^d   Joels, Marian ^a,e   Krugers, Harm ^a   Lucassen, Paul J ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b BIOMEDICAL PRIMATE RESEARCH CENTRE   (Netherlands)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d GERMAN PRIMATE CENTER   (Germany)

^e UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Adult neurogenesis; Aging; Doublecortin; Nonhuman primate; PSA NCAM; Stress

Indexed keywords

DOUBLECORTIN;

AGING; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALLITRICHINAE; CELL COUNT; CELL DENSITY; CELL MIGRATION; CELL SUBPOPULATION; CONTROLLED STUDY; DENTATE GYRUS; FEMALE; HIPPOCAMPUS; MALE; MENTAL STRESS; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NONHUMAN; PRIORITY JOURNAL; SOCIAL ISOLATION; SUBVENTRICULAR ZONE;

AGING; AMYGDALA; ANIMALS; CALLITHRIX; CELL COUNT; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MICROTUBULE-ASSOCIATED PROTEINS; NEUROGENESIS; NEURONAL PLASTICITY; NEURONS; NEUROPEPTIDES;

EID: 79958727585     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2011.05.008     Document Type: Article

References (61)

1. Bai J., Ramos R.L., Ackman J.B., Thomas A.M., Lee R.V., LoTurco J.J. RNAi reveals doublecortin is required for radial migration in rat neocortex. Nat. Neurosci. 2003, 6:1277-1283.
2. Bedard A., Gravel C., Parent A. Chemical characterization of newly generated neurons in the striatum of adult primates. Exp. Brain Res. 2006, 170:501-512.
3. Bernier P.J., Bedard A., Vinet J., Levesque M., Parent A. Newly generated neurons in the amygdala and adjoining cortex of adult primates. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:11464-11469.
4. Bernier P.J., Vinet J., Cossette M., Parent A. Characterization of the subventricular zone of the adult human brain: evidence for the involvement of Bcl-2. Neurosci. Res. 2000, 37:67-78.
5. Bonfanti L. PSA-NCAM in mammalian structural plasticity and neurogenesis. Prog. Neurobiol. 2006, 80:129-164.
6. Brown J.P., Couillard-Despres S., Cooper-Kuhn C.M., Winkler J., Aigner L., Kuhn H.G. Transient expression of doublecortin during adult neurogenesis. J. Comp. Neurol. 2003, 467:1-10.
7. Buwalda B., Kole M.H., Veenema A.H., Huininga M., de Boer S.F., Korte S.M., Koolhaas J.M. Long-term effects of social stress on brain and behavior: a focus on hippocampal functioning. Neurosci. Biobehav. Rev. 2005, 29:83-97.
8. Cai Y., Xiong K., Chu Y., Luo D.W., Luo X.G., Yuan X.Y., Struble R.G., Clough R.W., Spencer D.D., Williamson A., Kordower J.H., Patrylo P.R., Yan X.X. Doublecortin expression in adult cat and primate cerebral cortex relates to immature neurons that develop into GABAergic subgroups. Exp. Neurol. 2009, 216:342-356.
9. Cameron H.A., McKay R.D. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J. Comp. Neurol. 2001, 435:406-417.
10. Couillard-Despres S., Winner B., Schaubeck S., Aigner R., Vroemen M., Weidner N., Bogdahn U., Winkler J., Kuhn H.G., Aigner L. Doublecortin expression levels in adult brain reflect neurogenesis. Eur. J. Neurosci. 2005, 21:1-14.
11. Curtis M.A., Kam M., Nannmark U., Anderson M.F., Axell M.Z., Wikkelso C., Holtas S., van Roon-Mom W.M., Bjork-Eriksson T., Nordborg C., Frisen J., Dragunow M., Faull R.L., Eriksson P.S. Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 2007, 315:1243-1249.
12. Czeh B., Muller-Keuker J.I., Rygula R., Abumaria N., Hiemke C., Domenici E., Fuchs E. Chronic social stress inhibits cell proliferation in the adult medial prefrontal cortex: hemispheric asymmetry and reversal by fluoxetine treatment. Neuropsychopharmacology 2007, 32:1490-1503.
13. Czeh B., Welt T., Fischer A.K., Erhardt A., Schmitt W., Muller M.B., Toschi N., Fuchs E., Keck M.E. Chronic psychosocial stress and concomitant repetitive transcranial magnetic stimulation: effects on stress hormone levels and adult hippocampal neurogenesis. Biol. Psychiatry 2002, 52:1057-1065.
14. Doetsch F., Alvarez-Buylla A. Network of tangential pathways for neuronal migration in adult mammalian brain. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:14895-14900.
15. Dupret D., Revest J.M., Koehl M., Ichas F., De Giorgi F., Costet P., Abrous D.N., Piazza P.V. Spatial relational memory requires hippocampal adult neurogenesis. PLoS One 2008, 3:e1959.
16. Finne J. Occurrence of unique polysialosyl carbohydrate units in glycoproteins of developing brain. J. Biol. Chem. 1982, 257:11966-11970.
17. Francis F., Koulakoff A., Boucher D., Chafey P., Schaar B., Vinet M.C., Friocourt G., McDonnell N., Reiner O., Kahn A., McConnell S.K., Berwald-Netter Y., Denoulet P., Chelly J. Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 1999, 23:247-256.
18. Friocourt G., Chafey P., Billuart P., Koulakoff A., Vinet M.C., Schaar B.T., McConnell S.K., Francis F., Chelly J. Doublecortin interacts with mu subunits of clathrin adaptor complexes in the developing nervous system. Mol. Cell. Neurosci. 2001, 18:307-319.
19. Friocourt G., Koulakoff A., Chafey P., Boucher D., Fauchereau F., Chelly J., Francis F. Doublecortin functions at the extremities of growing neuronal processes. Cereb. Cortex 2003, 13:620-626.
20. Gomez-Climent M.A., Castillo-Gomez E., Varea E., Guirado R., Blasco-Ibanez J.M., Crespo C., Martinez-Guijarro F.J., Nacher J. A population of prenatally generated cells in the rat paleocortex maintains an immature neuronal phenotype into adulthood. Cereb. Cortex 2008, 18:2229-2240.
21. Gomez-Climent M.A., Guirado R., Varea E., Nacher J. "Arrested development". Immature, but not recently generated, neurons in the adult brain. Arch. Ital. Biol. 2010, 148:159-172.
22. Gould E. How widespread is adult neurogenesis in mammals?. Nat. Rev. Neurosci. 2007, 8:481-488.
23. Gould E., Tanapat P., McEwen B.S., Flugge G., Fuchs E. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:3168-3171.
24. Guo F., Maeda Y., Ma J., Xu J., Horiuchi M., Miers L., Vaccarino F., Pleasure D. Pyramidal neurons are generated from oligodendroglial progenitor cells in adult piriform cortex. J. Neurosci. 2010, 30:12036-12049.
25. Heine V.M., Maslam S., Joels M., Lucassen P.J. Prominent decline of newborn cell proliferation, differentiation, and apoptosis in the aging dentate gyrus, in absence of an age-related hypothalamus-pituitary-adrenal axis activation. Neurobiol. Aging 2004, 25:361-375.
26. Heine V.M., Maslam S., Zareno J., Joels M., Lucassen P.J. Suppressed proliferation and apoptotic changes in the rat dentate gyrus after acute and chronic stress are reversible. Eur. J. Neurosci. 2004, 19:131-144.
27. Hoffman S., Sorkin B.C., White P.C., Brackenbury R., Mailhammer R., Rutishauser U., Cunningham B.A., Edelman G.M. Chemical characterization of a neural cell adhesion molecule purified from embryonic brain membranes. J. Biol. Chem. 1982, 257:7720-7729.
28. Jabes A., Lavenex P.B., Amaral D.G., Lavenex P. Quantitative analysis of postnatal neurogenesis and neuron number in the macaque monkey dentate gyrus. Eur. J. Neurosci. 2010, 31:273-285.
29. Kam M., Curtis M.A., McGlashan S.R., Connor B., Nannmark U., Faull R.L. The cellular composition and morphological organization of the rostral migratory stream in the adult human brain. J. Chem. Neuroanat. 2009, 37:196-205.
30. Knabe W., Kuhn H.J. Capillary-contacting horizontal cells in the retina of the tree shrew Tupaia belangeri belong to the mammalian type A. Cell Tissue Res. 2000, 299:307-311.
31. Kornack D.R., Rakic P. The generation, migration, and differentiation of olfactory neurons in the adult primate brain. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:4752-4757.
32. Leuner B., Kozorovitskiy Y., Gross C.G., Gould E. Diminished adult neurogenesis in the marmoset brain precedes old age. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:17169-17173.
33. Lledo P.M., Alonso M., Grubb M.S. Adult neurogenesis and functional plasticity in neuronal circuits. Nat. Rev. Neurosci. 2006, 7:179-193.
34. Lois C., Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science 1994, 264:1145-1148.
35. Lucassen P.J., Meerlo P., Naylor A.S., van Dam A.M., Dayer A.G., Fuchs E., Oomen C.A., Czeh B. Regulation of adult neurogenesis by stress, sleep disruption, exercise and inflammation: implications for depression and antidepressant action. Eur. Neuropsychopharmacol. 2010, 20:1-17.
36. Luzzati F., Peretto P., Aimar P., Ponti G., Fasolo A., Bonfanti L. Glia-independent chains of neuroblasts through the subcortical parenchyma of the adult rabbit brain. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:13036-13041.
37. Nacher J., Crespo C., McEwen B.S. Doublecortin expression in the adult rat telencephalon. Eur. J. Neurosci. 2001, 14:629-644.
38. Nacher J., Lanuza E., McEwen B.S. Distribution of PSA-NCAM expression in the amygdala of the adult rat. Neuroscience 2002, 113:479-484.
39. Oomen C.A., Mayer J.L., de Kloet E.R., Joels M., Lucassen P.J. Brief treatment with the glucocorticoid receptor antagonist mifepristone normalizes the reduction in neurogenesis after chronic stress. Eur. J. Neurosci. 2007, 26:3395-3401.
40. Oomen C.A., Soeters H., Audureau N., Vermunt L., van Hasselt F.N., Manders E.M., Joels M., Lucassen P.J., Krugers H. Severe early life stress hampers spatial learning and neurogenesis, but improves hippocampal synaptic plasticity and emotional learning under high-stress conditions in adulthood. J. Neurosci. 2010, 30:6635-6645.
41. Palazzi X., Bordier N. The Marmoset Brain in Stereotaxic Coordinates 2008, 64. Springer.
42. Palmer T.D., Willhoite A.R., Gage F.H. Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol. 2000, 425:479-494.
43. Pencea V., Bingaman K.D., Freedman L.J., Luskin M.B. Neurogenesis in the subventricular zone and rostral migratory stream of the neonatal and adult primate forebrain. Exp. Neurol. 2001, 172:1-16.
44. Pieribone V.A., Porton B., Rendon B., Feng J., Greengard P., Kao H.T. Expression of synapsin III in nerve terminals and neurogenic regions of the adult brain. J. Comp. Neurol. 2002, 454:105-114.
45. Ponti G., Aimar P., Bonfanti L. Cellular composition and cytoarchitecture of the rabbit subventricular zone and its extensions in the forebrain. J. Comp. Neurol. 2006, 498:491-507.
46. Rao M.S., Hattiangady B., Shetty A.K. The window and mechanisms of major age-related decline in the production of new neurons within the dentate gyrus of the hippocampus. Aging Cell 2006, 5:545-558.
47. Rao M.S., Shetty A.K. Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus. Eur. J. Neurosci. 2004, 19:234-246.
48. Ribak C.E., Korn M.J., Shan Z., Obenaus A. Dendritic growth cones and recurrent basal dendrites are typical features of newly generated dentate granule cells in the adult hippocampus. Brain Res. 2004, 1000:195-199.
49. Roozendaal B., McEwen B.S., Chattarji S. Stress, memory and the amygdala. Nat. Rev. Neurosci. 2009, 10:423-433.
50. Rougon G., Dubois C., Buckley N., Magnani J.L., Zollinger W. A monoclonal antibody against meningococcus group B polysaccharides distinguishes embryonic from adult N-CAM. J. Cell Biol. 1986, 103:2429-2437.
51. Sanai N., Tramontin A.D., Quinones-Hinojosa A., Barbaro N.M., Gupta N., Kunwar S., Lawton M.T., McDermott M.W., Parsa A.T., Manuel-Garcia Verdugo J., Berger M.S., Alvarez-Buylla A. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 2004, 427:740-744.
52. Suzuki S., Gerhold L.M., Bottner M., Rau S.W., Dela Cruz C., Yang E., Zhu H., Yu J., Cashion A.B., Kindy M.S., Merchenthaler I., Gage F.H., Wise P.M. Estradiol enhances neurogenesis following ischemic stroke through estrogen receptors alpha and beta. J. Comp. Neurol. 2007, 500:1064-1075.
53. Tokuno H., Tanaka I., Umitsu Y., Akazawa T., Nakamura Y. Web-accessible digital brain atlas of the common marmoset (Callithrix jacchus). Neurosci. Res. 2009, 64:128-131.
54. Tonchev A.B., Yamashima T., Zhao L., Okano H. Differential proliferative response in the postischemic hippocampus, temporal cortex, and olfactory bulb of young adult macaque monkeys. Glia 2003, 42:209-224.
55. van Bokhoven P., Oomen C.A., Hoogendijk W.J., Smit A.B., Lucassen P.J., Spijker S. Reduction in hippocampal neurogenesis after social defeat is long lasting and responsive to late antidepressant treatment. Eur. J. Neurosci. 2011, 33:1833-1840.
56. Verwer R.W., Sluiter A.A., Balesar R.A., Baayen J.C., Noske D.P., Dirven C.M., Wouda J., van Dam A.M., Lucassen P.J., Swaab D.F. Mature astrocytes in the adult human neocortex express the early neuronal marker doublecortin. Brain 2007, 130:3321-3335.
57. Vyas A., Pillai A.G., Chattarji S. Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior. Neuroscience 2004, 128:667-673.
58. Xiong K., Luo D.W., Patrylo P.R., Luo X.G., Struble R.G., Clough R.W., Yan X.X. Doublecortin-expressing cells are present in layer II across the adult guinea pig cerebral cortex: partial colocalization with mature interneuron markers. Exp. Neurol. 2008, 211:271-282.
59. Yang H.K., Sundholm-Peters N.L., Goings G.E., Walker A.S., Hyland K., Szele F.G. Distribution of doublecortin expressing cells near the lateral ventricles in the adult mouse brain. J. Neurosci. Res. 2004, 76:282-295.
60. Yang Y., Zhang P., Xiong Y., Li X., Qi Y., Hu H. Ectopia of meningeal fibroblasts and reactive gliosis in the cerebral cortex of the mouse model of muscle-eye-brain disease. J. Comp. Neurol. 2007, 505:459-477.
61. Zhang X.M., Cai Y., Chen E.Y., Feng J.C., Luo X.G., Xiong K., Struble R.G., Clough R.W., Patrylo P.R., Kordower J.K., Yan X.X. Doublecortin-expressing cells persist in the associative cerebral cortex and amygdala in aged nonhuman primates. Front Neuroanat. 2009, 3:17.