Maturation time of new granule cells in the dentate gyrus of adult macaque monkeys exceeds six months

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 25, 2011, Pages 10326-10331

  Kohler, Shawn J ^a   Williams, Nancy I ^b   Stanton, Gregory B ^a   Cameron, Judy L ^c   Greenough, William T ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Granule cell layer; Immunohistochemistry; Neuronal maturation; Neuroprogenitor cell; Subgranular zone

Indexed keywords

BETA TUBULIN; BETAIII TUBULIN; BROXURIDINE; DNA; DOUBLECORTIN; NEURON SPECIFIC NUCLEAR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; BRAIN TISSUE; CELL MATURATION; CELL MIGRATION; CELL STRUCTURE; DENTATE GYRUS; DNA REPLICATION; FEMALE; GRANULE CELL; IMMUNOHISTOCHEMISTRY; MACACA FASCICULARIS; MACACA MULATTA; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BIOLOGICAL MARKERS; BROMODEOXYURIDINE; CELL MOVEMENT; DENTATE GYRUS; FEMALE; HUMANS; MACACA; NEUROGENESIS; NEURONS; TIME FACTORS;

MACACA FASCICULARIS; MACACA MULATTA; PRIMATES; RODENTIA;

EID: 79959949607     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1017099108     Document Type: Article

References (55)

1. Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319-335.
2. Cameron HA, Woolley CS, McEwen BS, Gould E (1993) Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56:337-344. (Pubitemid 23274753)
3. Kornack DR, Rakic P (1999) Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc Natl Acad Sci USA 96:5768-5773. (Pubitemid 29234693)
4. Aimone JB, Deng W, Gage FH (2010) Adult neurogenesis: integrating theories and separating functions. Trends Cogn Sci 14:325-37.
5. Deng W, Aimone JB, Gage FH (2010) New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat Rev Neurosci 11:339-350.
6. Kempermann G (2002) Why new neurons? Possible functions for adult hippocampal neurogenesis. J Neurosci 22:635-638.
7. Bizon JL, Gallagher M (2003) Production of new cells in the rat dentate gyrus over the lifespan: relation to cognitive decline. Eur J Neurosci 18:215-219. (Pubitemid 36920862)
8. Newton SS, Duman RS (2004) Regulation of neurogenesis and angiogenesis in depression. Curr Neurovasc Res 1:261-267.
9. Balu DT, Lucki I (2009) Adult hippocampal neurogenesis: Regulation, functional implications, and contribution to disease pathology. Neurosci Biobehav Rev 33:232-252.
10. Markakis EA, Gage FH (1999) Adult-generated neurons in the dentate gyrus send axonal projections to field CA3 and are surrounded by synaptic vesicles. J Comp Neurol 406:449-460. (Pubitemid 29144933)
11. Overstreet-Wadiche LS, Westbrook GL (2006) Functional maturation of adult-generated granule cells. Hippocampus 16:208-215.
12. Ge S, et al. (2006) GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439:589-593. (Pubitemid 43185382)
13. Espósito MS, et al. (2005) Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J Neurosci 25:10074-10086. (Pubitemid 41636203)
14. Zhao C, Teng EM, Summers RG, Jr., Ming GL, Gage FH (2006) Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 26:3-11. (Pubitemid 43089515)
15. Snyder JS, et al. (2009) Adult-born hippocampal neurons are more numerous, faster maturing, and more involved in behavior in rats than in mice. J Neurosci 29:14484-14495.
16. Brown JP, et al. (2003) Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1-10. (Pubitemid 37339753)
17. Kempermann G, Gast D, Kronenberg G, Yamaguchi M, Gage FH (2003) Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 130:391-399. (Pubitemid 36175935)
18. McDonald HY, Wojtowicz JM (2005) Dynamics of neurogenesis in the dentate gyrus of adult rats. Neurosci Lett 385:70-75. (Pubitemid 40909984)
19. Aizawa K, Ageyama N, Yokoyama C, Hisatsune T (2009) Age-dependent alteration in hippocampal neurogenesis correlates with learning performance of macaque monkeys. Exp Anim 58:403-407.
20. Jabès A, Lavenex PB, Amaral DG, Lavenex P (2010) Quantitative analysis of postnatal neurogenesis and neuron number in the macaque monkey dentate gyrus. Eur J Neurosci 31:273-285.
21. Koketsu D, et al. (2006) Increased number of new neurons in the olfactory bulb and hippocampus of adult non-human primates after focal ischemia. Exp Neurol 199:92-102.
22. Perera TD, et al. (2007) Antidepressant-induced neurogenesis in the hippocampus of adult nonhuman primates. J Neurosci 27:4894-4901. (Pubitemid 46699055)
23. Gould E, Vail N, Wagers M, Gross CG (2001) Adult-generated hippocampal and neocortical neurons in macaques have a transient existence. Proc Natl Acad Sci USA 98:10910-10917. (Pubitemid 32878718)
24. Ngwenya LB, Peters A, Rosene DL (2006) Maturational sequence of newly generated neurons in the dentate gyrus of the young adult rhesus monkey. J Comp Neurol 498:204-216. (Pubitemid 44182461)
25. Rhyu IJ, et al. (2010) Effects of aerobic exercise training on cognitive function and cortical vascularity in monkeys. Neuroscience 167:1239-1248.
26. Rakic P (1995) A small step for the cell, a giant leap for mankind: A hypothesis of neocortical expansion during evolution. Trends Neurosci 18:383-388.
27. Caviness VS, Jr., Takahashi T, Nowakowski RS (1995) Numbers, time and neocortical neuronogenesis: A general developmental and evolutionary model. Trends Neurosci 18:379-383.
28. Rakic P (1974) Neurons in rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition. Science 183:425-427.
29. Rakic P, Nowakowski RS (1981) The time of origin of neurons in the hippocampal region of the rhesus monkey. J Comp Neurol 196:99-128. (Pubitemid 11098977)
30. Kornack DR, Rakic P (1998) Changes in cell-cycle kinetics during the development and evolution of primate neocortex. Proc Natl Acad Sci USA 95:1242-1246. (Pubitemid 28124943)
31. Takahashi T, Nowakowski RS, Caviness VS, Jr. (1995) The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J Neurosci 15:6046-6057.
32. Cameron HA, McKay RD (2001) Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435:406-417.
33. Mandyam CD, Harburg GC, Eisch AJ (2007) Determination of key aspects of precursor cell proliferation, cell cycle length and kinetics in the adult mouse subgranular zone. Neuroscience 146:108-122. (Pubitemid 46654600)
34. Prickaerts J, Koopmans G, Blokland A, Scheepens A (2004) Learning and adult neurogenesis: survival with or without proliferation? Neurobiol Learn Mem 81:1-11.
35. Hayes NL, Nowakowski RS (2002) Dynamics of cell proliferation in the adult dentate gyrus of two inbred strains of mice. Brain Res Dev Brain Res 134:77-85. (Pubitemid 34310238)
36. van Praag H, Kempermann G, Gage FH (1999) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2:266-270. (Pubitemid 30491298)
37. Brown J, et al. (2003) Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur J Neurosci 17:2042-2046. (Pubitemid 36713965)
38. Rhodes JS, et al. (2003) Exercise increases hippocampal neurogenesis to high levels but does not improve spatial learning in mice bred for increased voluntary wheel running. Behav Neurosci 117:1006-1016. (Pubitemid 37243783)
39. Burns KA, et al. (2007) Nestin-CreER mice reveal DNA synthesis by nonapoptotic neurons following cerebral ischemia hypoxia. Cereb Cortex 17:2585-2592. (Pubitemid 47537816)
40. Jabès A, Lavenex PB, Amaral DG, Lavenex P (2011) Postnatal development of the hippocampal formation: a stereological study in macaque monkeys. J Comp Neurol 519:1051-1070.
41. des Portes V, et al. (1998) A novel CNS gene required for neuronal migration and involved in X-linked subcortical laminar heterotopia and lissencephaly syndrome. Cell 92:51-61.
42. Francis F, et al. (1999) Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 23:247-256. (Pubitemid 29315721)
43. Gleeson JG, Lin PT, Flanagan LA, Walsh CA (1999) Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23:257-271. (Pubitemid 29315722)
44. Meyer G, Perez-Garcia CG, Gleeson JG (2002) Selective expression of doublecortin and LIS1 in developing human cortex suggests unique modes of neuronal movement. Cereb Cortex 12:1225-1236. (Pubitemid 35396960)
45. Mattson MP (1999) Establishment and plasticity of neuronal polarity. J Neurosci Res 57:577-589.
46. Feng Y, Walsh CA (2001) Protein-protein interactions, cytoskeletal regulation and neuronal migration. Nat Rev Neurosci 2:408-416. (Pubitemid 33674797)
47. Sahay A, Hen R (2007) Adult hippocampal neurogenesis in depression. Nat Neurosci 10:1110-1115. (Pubitemid 47339960)
48. Eisch AJ, et al. (2008) Adult neurogenesis, mental health, and mental illness: hope or hype? J Neurosci 28:11785-11791.
49. Malberg JE, Eisch AJ, Nestler EJ, Duman RS (2000) Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20:9104-9110. (Pubitemid 32042912)
50. Santarelli L, et al. (2003) Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301:805-809. (Pubitemid 36962615)
51. Blier P (2003) The pharmacology of putative early-onset antidepressant strategies. Eur Neuropsychopharmacol 13:57-66.
52. 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.
53. Leuner B, Glasper ER, Gould E (2009) Thymidine analog methods for studies of adult neurogenesis are not equally sensitive. J Comp Neurol 517:123-133.
54. Clifton DK, Bremner WJ, Steiner RA (1982) An automated technique for the radiographic determination of bone age. J Med Primatol 11:147-154. (Pubitemid 13194422)
55. Kempermann G, Kuhn HG, Gage FH (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature 386:493-495. (Pubitemid 27164074)