 |
Previous Article | Next Article 
Volume 17, Number 7,
Issue of April 1, 1997
pp. 2492-2498
Copyright ©1997 Society for Neuroscience
Neurogenesis in the Dentate Gyrus of the Adult Tree Shrew Is
Regulated by Psychosocial Stress and NMDA Receptor Activation
Received Oct. 11, 1996; revised Dec. 3, 1996; accepted Jan. 10, 1997.
Elizabeth Gould1,
Bruce
S. McEwen1,
Patima Tanapat1,
Liisa A. M. Galea1, and
Eberhard Fuchs2
1 The Rockefeller University, New York, New York 10021, and 2 The German Primate Center, 37077 Göttingen,
Germany
These studies were designed to determine whether adult neurogenesis
occurs in the dentate gyrus of the tree shrew, an animal phylogenetically between insectivores and primates, and to explore the
possibility that this process is regulated by stressful experiences and
NMDA receptor activation. We performed immunohistochemistry for
cell-specific markers and the thymidine analog bromodeoxyuridine (BrdU), a marker of DNA synthesis that labels proliferating cells and
their progeny, on the brains of adult tree shrews subjected to
psychosocial stress or NMDA receptor antagonist treatment. Cells that
incorporated BrdU in the dentate gyrus of adult tree shrews were
primarily located in the subgranular zone, had morphological characteristics of granule neuron precursors, and appeared to divide
within 24 hr after BrdU injection. Three weeks after BrdU injection,
BrdU-labeled cells had neuronal morphology, expressed the neuronal
marker neuron specific enolase, and were incorporated into the granule
cell layer. Vimentin-immunoreactive radial glia were observed in the
dentate gyrus with cell bodies in the subgranular zone and processes
extending into the granule cell layer.
Exposure to acute psychosocial stress resulted in a rapid decrease in
the number of BrdU-labeled cells in the dentate gyrus. In contrast,
blockade of NMDA receptors, with the NMDA receptor antagonist MK-801,
resulted in an increase in the number of BrdU-labeled cells in the
dentate gyrus. These results indicate that adult neurogenesis occurs in
the tree shrew dentate gyrus and is regulated by a stressful experience
and NMDA receptor activation. Furthermore, we suggest that these
characteristics may be common to most mammalian species.
Key words:
neurogenesis;
tree shrew;
psychosocial stress;
granule
neurons;
dentate gyrus;
NMDA receptors
This article has been cited by other articles:

|
 |

|
 |
 
A. K. Shetty and B. Hattiangady
Concise Review: Prospects of Stem Cell Therapy for Temporal Lobe Epilepsy
Stem Cells,
October 1, 2007;
25(10):
2396 - 2407.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. S. McEwen
Physiology and Neurobiology of Stress and Adaptation: Central Role of the Brain
Physiol Rev,
July 1, 2007;
87(3):
873 - 904.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. D. Perera, J. D. Coplan, S. H. Lisanby, C. M. Lipira, M. Arif, C. Carpio, G. Spitzer, L. Santarelli, B. Scharf, R. Hen, et al.
Antidepressant-Induced Neurogenesis in the Hippocampus of Adult Nonhuman Primates
J. Neurosci.,
May 2, 2007;
27(18):
4894 - 4901.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C.-K. Song, L. M. Johnstone, M. Schmidt, C. D. Derby, and D. H. Edwards
Social domination increases neuronal survival in the brain of juvenile crayfish Procambarus clarkii
J. Exp. Biol.,
April 15, 2007;
210(8):
1311 - 1324.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. M. Thomas, G. Hotsenpiller, and D. A. Peterson
Acute Psychosocial Stress Reduces Cell Survival in Adult Hippocampal Neurogenesis without Altering Proliferation
J. Neurosci.,
March 14, 2007;
27(11):
2734 - 2743.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Kaneko, H. Okano, and K. Sawamoto
Role of the cholinergic system in regulating survival of newborn neurons in the adult mouse dentate gyrus and olfactory bulb.
Genes Cells,
October 1, 2006;
11(10):
1145 - 1159.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Bick-Sander, B. Steiner, S. A. Wolf, H. Babu, and G. Kempermann
Running in pregnancy transiently increases postnatal hippocampal neurogenesis in the offspring
PNAS,
March 7, 2006;
103(10):
3852 - 3857.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Wang, H. Rao, G. S. Wetmore, P. M. Furlan, M. Korczykowski, D. F. Dinges, and J. A. Detre
Perfusion functional MRI reveals cerebral blood flow pattern under psychological stress
PNAS,
December 6, 2005;
102(49):
17804 - 17809.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. E. Gilbert, M. E. Kelly, T. E. Samsam, and J. H. Goodman
Chronic Developmental Lead Exposure Reduces Neurogenesis in Adult Rat Hippocampus but Does Not Impair Spatial Learning
Toxicol. Sci.,
August 1, 2005;
86(2):
365 - 374.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. D. Taylor, D. C. Steffens, M. E. Payne, J. R. MacFall, D. A. Marchuk, I. K. Svenson, and K. R. R. Krishnan
Influence of Serotonin Transporter Promoter Region Polymorphisms on Hippocampal Volumes in Late-Life Depression
Arch Gen Psychiatry,
May 1, 2005;
62(5):
537 - 544.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. N. Abrous, M. Koehl, and M. Le Moal
Adult Neurogenesis: From Precursors to Network and Physiology
Physiol Rev,
April 1, 2005;
85(2):
523 - 569.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. G. Dayer, K. M. Cleaver, T. Abouantoun, and H. A. Cameron
New GABAergic interneurons in the adult neocortex and striatum are generated from different precursors
J. Cell Biol.,
January 31, 2005;
168(3):
415 - 427.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Sun, A. Winseck, S. Vinsant, O.-h. Park, H. Kim, and R. W. Oppenheim
Programmed Cell Death of Adult-Generated Hippocampal Neurons Is Mediated by the Proapoptotic Gene Bax
J. Neurosci.,
December 8, 2004;
24(49):
11205 - 11213.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Kozorovitskiy and E. Gould
Dominance Hierarchy Influences Adult Neurogenesis in the Dentate Gyrus
J. Neurosci.,
July 28, 2004;
24(30):
6755 - 6759.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Banjanin, A. Kapoor, and S. G. Matthews
Prenatal glucocorticoid exposure alters hypothalamic-pituitary-adrenal function and blood pressure in mature male guinea pigs
J. Physiol.,
July 1, 2004;
558(1):
305 - 318.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Tanaka, K. Yamashiro, H. Mochizuki, N. Cho, M. Onodera, Y. Mizuno, and T. Urabe
Neurogenesis After Transient Global Ischemia in the Adult Hippocampus Visualized by Improved Retroviral Vector
Stroke,
June 1, 2004;
35(6):
1454 - 1459.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. D. Bremner, M. Vythilingam, E. Vermetten, V. Vaccarino, and D. S. Charney
Deficits in Hippocampal and Anterior Cingulate Functioning During Verbal Declarative Memory Encoding in Midlife Major Depression
Am J Psychiatry,
April 1, 2004;
161(4):
637 - 645.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. Alvarez-Borda, B. Haripal, and F. Nottebohm
Timing of brain-derived neurotrophic factor exposure affects life expectancy of new neurons
PNAS,
March 16, 2004;
101(11):
3957 - 3961.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Rocher, M. Spedding, C. Munoz, and T. M. Jay
Acute Stress-induced Changes in Hippocampal/Prefrontal Circuits in Rats: Effects of Antidepressants
Cereb Cortex,
February 1, 2004;
14(2):
224 - 229.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Fujioka, A. Fujioka, and R. S. Duman
Activation of cAMP Signaling Facilitates the Morphological Maturation of Newborn Neurons in Adult Hippocampus
J. Neurosci.,
January 14, 2004;
24(2):
319 - 328.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. L. Monje, H. Toda, and T. D. Palmer
Inflammatory Blockade Restores Adult Hippocampal Neurogenesis
Science,
December 5, 2003;
302(5651):
1760 - 1765.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. M. Thomas and D. A. Peterson
A Neurogenic Theory of Depression Gains Momentum
Mol. Interv.,
December 1, 2003;
3(8):
441 - 444.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. S. Newton, E. F. Collier, J. Hunsberger, D. Adams, R. Terwilliger, E. Selvanayagam, and R. S. Duman
Gene Profile of Electroconvulsive Seizures: Induction of Neurotrophic and Angiogenic Factors
J. Neurosci.,
November 26, 2003;
23(34):
10841 - 10851.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Scotto-Lomassese, C. Strambi, A. Strambi, A. Aouane, R. Augier, G. Rougon, and M. Cayre
Suppression of Adult Neurogenesis Impairs Olfactory Learning and Memory in an Adult Insect
J. Neurosci.,
October 15, 2003;
23(28):
9289 - 9296.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. I. Sheline, M. H. Gado, and H. C. Kraemer
Untreated Depression and Hippocampal Volume Loss
Am J Psychiatry,
August 1, 2003;
160(8):
1516 - 1518.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Mizumatsu, M. L. Monje, D. R. Morhardt, R. Rola, T. D. Palmer, and J. R. Fike
Extreme Sensitivity of Adult Neurogenesis to Low Doses of X-Irradiation
Cancer Res.,
July 15, 2003;
63(14):
4021 - 4027.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. F. Deicken, M. P. Pegues, S. Anzalone, R. Feiwell, and B. Soher
Lower Concentration of Hippocampal N-Acetylaspartate in Familial Bipolar I Disorder
Am J Psychiatry,
May 1, 2003;
160(5):
873 - 882.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. D. Bremner, M. Vythilingam, E. Vermetten, S. M. Southwick, T. McGlashan, A. Nazeer, S. Khan, L. V. Vaccarino, R. Soufer, P. K. Garg, et al.
MRI and PET Study of Deficits in Hippocampal Structure and Function in Women With Childhood Sexual Abuse and Posttraumatic Stress Disorder
Am J Psychiatry,
May 1, 2003;
160(5):
924 - 932.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Vythilingam, C. Heim, J. Newport, A. H. Miller, E. Anderson, R. Bronen, M. Brummer, L. Staib, E. Vermetten, D. S. Charney, et al.
Childhood Trauma Associated With Smaller Hippocampal Volume in Women With Major Depression
Am J Psychiatry,
December 1, 2002;
159(12):
2072 - 2080.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Nakano, M. Wenner, M. Inagaki, A. Kugaya, T. Akechi, Y. Matsuoka, Y. Sugahara, S. Imoto, K. Murakami, and Y. Uchitomi
Relationship Between Distressing Cancer-Related Recollections and Hippocampal Volume in Cancer Survivors
Am J Psychiatry,
December 1, 2002;
159(12):
2087 - 2093.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Nakagawa, J.-E. Kim, R. Lee, J. E. Malberg, J. Chen, C. Steffen, Y.-J. Zhang, E. J. Nestler, and R. S. Duman
Regulation of Neurogenesis in Adult Mouse Hippocampus by cAMP and the cAMP Response Element-Binding Protein
J. Neurosci.,
May 1, 2002;
22(9):
3673 - 3682.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. C. Noctor, A. C. Flint, T. A. Weissman, W. S. Wong, B. K. Clinton, and A. R. Kriegstein
Dividing Precursor Cells of the Embryonic Cortical Ventricular Zone Have Morphological and Molecular Characteristics of Radial Glia
J. Neurosci.,
April 15, 2002;
22(8):
3161 - 3173.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Gould and C. G. Gross
Neurogenesis in Adult Mammals: Some Progress and Problems
J. Neurosci.,
February 1, 2002;
22(3):
619 - 623.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Kempermann
Why New Neurons? Possible Functions for Adult Hippocampal Neurogenesis
J. Neurosci.,
February 1, 2002;
22(3):
635 - 638.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Vallieres, I. L. Campbell, F. H. Gage, and P. E. Sawchenko
Reduced Hippocampal Neurogenesis in Adult Transgenic Mice with Chronic Astrocytic Production of Interleukin-6
J. Neurosci.,
January 15, 2002;
22(2):
486 - 492.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. M. Sapolsky
Depression, antidepressants, and the shrinking hippocampus
PNAS,
October 23, 2001;
98(22):
12320 - 12322.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. J. Mathew, J. D. Coplan, and J. M. Gorman
Neurobiological Mechanisms of Social Anxiety Disorder
Am J Psychiatry,
October 1, 2001;
158(10):
1558 - 1567.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. Czeh, T. Michaelis, T. Watanabe, J. Frahm, G. de Biurrun, M. van Kampen, A. Bartolomucci, and E. Fuchs
Stress-induced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressant treatment with tianeptine
PNAS,
September 26, 2001;
(2001)
211427898.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. Seri, J. M. Garcia-Verdugo, B. S. McEwen, and A. Alvarez-Buylla
Astrocytes Give Rise to New Neurons in the Adult Mammalian Hippocampus
J. Neurosci.,
September 15, 2001;
21(18):
7153 - 7160.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. C. DeVries, H.-D. Joh, O. Bernard, K. Hattori, P. D. Hurn, R. J. Traystman, and N. J. Alkayed
Social stress exacerbates stroke outcome by suppressing Bcl-2 expression
PNAS,
September 5, 2001;
(2001)
201215298.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Gould, N. Vail, M. Wagers, and C. G. Gross
Adult-generated hippocampal and neocortical neurons in macaques have a transient existence
PNAS,
August 23, 2001;
(2001)
181354698.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Katchanov, C. Harms, K. Gertz, L. Hauck, C. Waeber, L. Hirt, J. Priller, R. von Harsdorf, W. Bruck, H. Hortnagl, et al.
Mild Cerebral Ischemia Induces Loss of Cyclin-Dependent Kinase Inhibitors and Activation of Cell Cycle Machinery before Delayed Neuronal Cell Death
J. Neurosci.,
July 15, 2001;
21(14):
5045 - 5053.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. S. Snyder, N. Kee, and J. M. Wojtowicz
Effects of Adult Neurogenesis on Synaptic Plasticity in the Rat Dentate Gyrus
J Neurophysiol,
June 1, 2001;
85(6):
2423 - 2431.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. K. McCabe, D. C. Silveira, M. R. Cilio, B. H. Cha, X. Liu, Y. Sogawa, and G. L. Holmes
Reduced Neurogenesis after Neonatal Seizures
J. Neurosci.,
March 15, 2001;
21(6):
2094 - 2103.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Crisanti, B. Omri, E. J. Hughes, G. Meduri, C. Hery, E. Clauser, C. Jacquemin, and B. Saunier
The Expression of Thyrotropin Receptor in the Brain
Endocrinology,
February 1, 2001;
142(2):
812 - 822.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. E. Malberg, A. J. Eisch, E. J. Nestler, and R. S. Duman
Chronic Antidepressant Treatment Increases Neurogenesis in Adult Rat Hippocampus
J. Neurosci.,
December 15, 2000;
20(24):
9104 - 9110.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. J. Pleasure, A. E. Collins, and D. H. Lowenstein
Unique Expression Patterns of Cell Fate Molecules Delineate Sequential Stages of Dentate Gyrus Development
J. Neurosci.,
August 15, 2000;
20(16):
6095 - 6105.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. E. Scharfman, J. H. Goodman, and A. L. Sollas
Granule-Like Neurons at the Hilar/CA3 Border after Status Epilepticus and Their Synchrony with Area CA3 Pyramidal Cells: Functional Implications of Seizure-Induced Neurogenesis
J. Neurosci.,
August 15, 2000;
20(16):
6144 - 6158.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
X.-C. Li, E. D. Jarvis, B. Alvarez-Borda, D. A. Lim, and F. Nottebohm
A relationship between behavior, neurotrophin expression, and new neuron survival
PNAS,
July 5, 2000;
(2000)
140222497.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
M. A. I. Aberg, N. D. Aberg, H. Hedbacker, J. Oscarsson, and P. S. Eriksson
Peripheral Infusion of IGF-I Selectively Induces Neurogenesis in the Adult Rat Hippocampus
J. Neurosci.,
April 15, 2000;
20(8):
2896 - 2903.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Gould, A. J. Reeves, M. S. Graziano, and C. G. Gross
Neurogenesis in the Neocortex of Adult Primates
Science,
October 15, 1999;
286(5439):
548 - 552.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
P. Tanapat, N. B. Hastings, A. J. Reeves, and E. Gould
Estrogen Stimulates a Transient Increase in the Number of New Neurons in the Dentate Gyrus of the Adult Female Rat
J. Neurosci.,
July 15, 1999;
19(14):
5792 - 5801.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. P. Wagner, I. B. Black, and E. DiCicco-Bloom
Stimulation of Neonatal and Adult Brain Neurogenesis by Subcutaneous Injection of Basic Fibroblast Growth Factor
J. Neurosci.,
July 15, 1999;
19(14):
6006 - 6016.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. S. McEwen
Permanence of brain sex differences and structural plasticity of the adult brain
PNAS,
June 22, 1999;
96(13):
7128 - 7130.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. R. Kornack and P. Rakic
Continuation of neurogenesis in the hippocampus of the adult macaque monkey
PNAS,
May 11, 1999;
96(10):
5768 - 5773.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Gould, A. J. Reeves, M. Fallah, P. Tanapat, C. G. Gross, and E. Fuchs
Hippocampal neurogenesis in adult Old World primates
PNAS,
April 27, 1999;
96(9):
5263 - 5267.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. Kolb, B. Pedersen, M. Ballermann, R. Gibb, and I. Q. Whishaw
Embryonic and Postnatal Injections of Bromodeoxyuridine Produce Age-Dependent Morphological and Behavioral Abnormalities
J. Neurosci.,
March 15, 1999;
19(6):
2337 - 2346.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Liu, K. Solway, R. O. Messing, and F. R. Sharp
Increased Neurogenesis in the Dentate Gyrus After Transient Global Ischemia in Gerbils
J. Neurosci.,
October 1, 1998;
18(19):
7768 - 7778.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. R. de Kloet, E. Vreugdenhil, M. S. Oitzl, and M. Joëls
Brain Corticosteroid Receptor Balance in Health and Disease
Endocr. Rev.,
June 1, 1998;
19(3):
269 - 301.
[Abstract]
[Full Text]
|
 |
|
|