Abstract
The production of new hippocampal neurons in adulthood has been well documented in rodents. Recent studies have extended these findings to other mammalian species, such as tree shrews and marmoset monkeys. However, hippocampal neurogenesis has not been demonstrated in adult Old World primates. To investigate this possibility, we injected 11 adult Old World monkeys of different ages (5-23 years) with the thymidine analog bromodeoxyuridine and examined the fate of the labeled cells at different survival times by using neuronal and glial markers. In the young-adult and middle-aged monkeys, we found a substantial number of cells that incorporated bromodeoxyuridine and exhibited morphological and biochemical characteristics of immature and mature neurons. New cells located in the dentate gyrus expressed a marker of immature granule neurons, Turned On After Division 64 kDa protein, as well as markers of mature granule neurons including neuron specific enolase, neuronal nuclei, and the calcium-binding protein calbindin. Fewer new cells expressed the astroglial marker glial fibrillary acidic protein. Evidence of neurogenesis was observed in the oldest monkeys (23 years) as well, but it appeared to be less robust. These results indicate that the adult brains of Old World monkeys produce new hippocampal neurons. Adult macaque monkeys may provide a useful primate model for studying the functional significance of adult neurogenesis.
MeSH Terms
Aging
Animals
Cell Count
Cell Differentiation/physiology
Cell Division/physiology
Cercopithecidae
Female
Hippocampus/cytology,physiology
Male
Microscopy, Confocal
Neurons/cytology,physiology
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Gould E
Department of Psychology, Princeton University, Princeton NJ 08544, USA. goulde@princeton.edu
Reeves A J
Fallah M
Tanapat P
Gross C G
Fuchs E
References (27)
27 references, click to expand
-
Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat.
Neuroscience. 1993 Sep;56(2):337-44
PMID: 8247264
-
The adrenocortical axis in the aged rat: impaired sensitivity to both fast and delayed feedback inhibition.
Neurobiol Aging. 1986 Sep-Oct;7(5):331-5
PMID: 3024042
-
Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats.
J Comp Neurol. 1965 Jun;124(3):319-35
PMID: 5861717
-
Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator.
Anat Rec. 1991 Dec;231(4):482-97
PMID: 1793176
-
Nature and fate of proliferative cells in the hippocampal dentate gyrus during the life span of the rhesus monkey.
J Neurosci. 1988 Aug;8(8):2729-47
PMID: 3411351
-
The hippocampus as an associator of discontiguous events.
Trends Neurosci. 1998 Aug;21(8):317-23
PMID: 9720595
-
Recruitment and replacement of hippocampal neurons in young and adult chickadees: an addition to the theory of hippocampal learning.
Proc Natl Acad Sci U S A. 1996 Jan 23;93(2):714-8
PMID: 11607626
-
On the role of the hippocampus in learning and memory in the rat.
Behav Neural Biol. 1993 Jul;60(1):9-26
PMID: 8216164
-
Limits of neurogenesis in primates.
Science. 1985 Mar 1;227(4690):1054-6
PMID: 3975601
-
Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population.
J Neurocytol. 1989 Jun;18(3):311-8
PMID: 2746304
-
Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain.
J Neurosci. 1997 Jul 1;17(13):5046-61
PMID: 9185542
-
Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus.
Neuroscience. 1994 Jul;61(2):203-9
PMID: 7969902
-
Amnesia, memory and brain systems.
Philos Trans R Soc Lond B Biol Sci. 1997 Nov 29;352(1362):1663-73
PMID: 9415918
-
Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation.
J Neurosci. 1997 Apr 1;17(7):2492-8
PMID: 9065509
-
Aging, dominance history, and social behavior in Java-monkeys (Macaca fascicularis).
Neurobiol Aging. 1997 Sep-Oct;18(5):509-15
PMID: 9390777
-
Learning enhances adult neurogenesis in the hippocampal formation.
Nat Neurosci. 1999 Mar;2(3):260-5
PMID: 10195219
-
Birth of projection neurons in the higher vocal center of the canary forebrain before, during, and after song learning.
Proc Natl Acad Sci U S A. 1988 Nov;85(22):8722-6
PMID: 3186755
-
Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees.
Proc Natl Acad Sci U S A. 1994 Nov 8;91(23):11217-21
PMID: 7972037
-
Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus.
J Neurosci. 1997 May 15;17(10):3727-38
PMID: 9133393
-
Early postmitotic neurons transiently express TOAD-64, a neural specific protein.
J Comp Neurol. 1995 May 8;355(3):369-79
PMID: 7636019
-
More hippocampal neurons in adult mice living in an enriched environment.
Nature. 1997 Apr 3;386(6624):493-5
PMID: 9087407
-
Classical conditioning and brain systems: the role of awareness.
Science. 1998 Apr 3;280(5360):77-81
PMID: 9525860
-
Embryonic (PSA) N-CAM reveals chains of migrating neuroblasts between the lateral ventricle and the olfactory bulb of adult mice.
J Comp Neurol. 1995 Jan 2;351(1):51-61
PMID: 7896939
-
Highly polysialylated neural cell adhesion molecule (NCAM-H) is expressed by newly generated granule cells in the dentate gyrus of the adult rat.
J Neurosci. 1993 Jun;13(6):2351-8
PMID: 7684771
-
Neurogenesis in the adult human hippocampus.
Nat Med. 1998 Nov;4(11):1313-7
PMID: 9809557
-
Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress.
Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):3168-71
PMID: 9501234
-
Lesion-induced proliferation of neuronal progenitors in the dentate gyrus of the adult rat.
Neuroscience. 1997 Sep;80(2):427-36
PMID: 9284346