Abstract
This paper summarizes the results of our studies on adult neurogenesis in some key structures of the monkey and human brain. These results stem from multiple immunocytochemical investigations undertaken with antigens raised against various molecular markers of neurogenesis, either alone or in combination with the DNA synthesis indicator bromodeoxyuridine (BrdU). This approach has allowed us to provide the first detailed picture of the organization of the rostral migratory stream (RMS) in adult squirrel monkeys. Furthermore, studies on human postmortem tissue have revealed, for the first time, that the adult human olfactory bulb is the recipient of neuroblasts that migrate along the RMS and progressively develop a GABAergic or dopaminergic phenotype. A new migratory stream that provides newborn neurons to the amygdala and adjacent piriform cortex has also been visualized in squirrel monkeys. Finally, the striatum of normal adult squirrel monkeys was found to harbor newly generated cells that eventually become projection neurons. The recruitment of such striatal neurons was markedly increased in the presence of brain-derived neurotrophic factor (BDNF), a finding that raises hope for the development of novel therapeutic approaches for the treatment of certain neurodegenerative diseases.
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Abbreviations
- ac:
-
Anterior commissure
- AdBDNF:
-
Adenoviral vector overexpressing BDNF
- AMY:
-
Amygdala
- BDNF:
-
Brain-derived neurotrophic factor
- BrdU:
-
Bromodeoxyuridine
- c:
-
Caudal (posterior)
- CB:
-
Calbindin
- cc:
-
Corpus callosum
- CD:
-
Caudate nucleus
- ChAT:
-
Choline acetyltransferase
- CMV:
-
Cytomegalovirus
- CR:
-
Calretinin
- CT:
-
Cortex
- DARPP-32:
-
Dopamine- and cAMP-regulated phosphoprotein of 32 kDa
- DCX:
-
Doublecortin
- EPL:
-
External plexiform layer
- FL:
-
Fiber layer
- GAD:
-
Glutamic acid decarboxylase
- GAD65/67 :
-
GAD 65 and 67 isoforms
- GCL:
-
Granular cell layer
- GFAP:
-
Glial fibrillary acidic protein
- GL:
-
Glomerular layer
- HIPPO:
-
Hippocampus
- HL:
-
Horizontal limb
- ic:
-
Internal capsule
- Ki-67:
-
Cell cycle-associated protein
- LV:
-
Lateral ventricle
- MAP-2:
-
Microtubule-associated protein 2
- MCL:
-
Mitral cell layer
- NA:
-
Nucleus accumbens
- NeuN:
-
Neuronal nuclear protein
- NeuroD:
-
Neuronal determination and differentiation transcription factor
- OB:
-
Olfactory bulb
- ONL:
-
Olfactory nerve layer
- OT:
-
Olfactory tubercle
- PCNA:
-
Proliferating cell nuclear antigen
- PIRI:
-
Piriform cortex
- PL:
-
Posterior limb
- PSA-NCAM:
-
Polysialylated neural cell adhesion
- PUT:
-
Putamen
- PV:
-
Parvalbumin
- r:
-
Rostral (anterior)
- RMS:
-
Rostral migratory stream
- SS:
-
Somatostatin
- SVZ:
-
Subventricular zone
- SVZa:
-
Anterior part of SVZ
- TH:
-
Tyrosine hydroxylase
- tLV:
-
Temporal horn of LV
- TS:
-
Temporal migratory stream
- TUC-4:
-
Collapsin response mediator protein-4
- TuJ1:
-
β-Tubulin-III
- VL:
-
Vertical limb
References
Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319–336.
Arvidsson A, Collin T, Kirik D et al (2002) Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 8:963–970.
Bédard A, Parent A (2004) Evidence of newly generated neurons in the human olfactory bulb. Dev Brain Res 151:159–168.
Bédard A, Cossette M, Lévesque M et al (2002a) Proliferating cells can differentiate into neurons in the striatum of normal adult monkey. Neurosci Lett 328:213–216.
Bédard A, Lévesque M, Bernier PJ et al (2002b) The rostral migratory stream in adult squirrel monkeys: contribution of new neurons to the olfactory tubercle and involvement of the antiapoptotic protein Bcl-2. Eur J Neurosci 16:1917–1924.
Bédard A, Gravel C, Parent A (2006) Chemical characterization of newly generated neurons in the striatum of adult primates. Exp Brain Res 170:501–512.
Bernier PJ, Parent A (1998a) Bcl-2 protein as a marker of neuronal immaturity in postnatal primate brain. J Neurosci 18:2486–2497.
Bernier PJ, Parent A (1998b) The anti-apoptosis bcl-2 proto-oncogene is preferentially expressed in limbic structures of the primate brain. Neuroscience 82:635–640.
Bernier PJ, Vinet J, Cossette M et al (2000) Characterization of the subventricular zone in the adult human brain: evidence for Bcl-2 involvement. Neurosci Res 37:67–78.
Bernier PJ, Bédard A, Vinet J et al (2002) Newly generated neurons in the amygdala and adjoining cortex of adult primates. Proc Natl Acad Sci USA 99:11464–11469.
Cameron HA, Dayer AG (2008) New interneurons in the adult neocortex: small, sparse, but significant? Biol Psychiatry 63:650–655.
Cameron HA, Woolley CS, McEwen BS et al (1993) Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56:337–344.
Chmielnicki E, Benraiss A, Economides AN et al (2004) Adenovirally expressed noggin and brain-derived neurotrophic factor cooperate to induce new medium spiny neurons from resident progenitor cells in the adult striatal ventricular zone. J Neurosci 24: 2133–2142.
Craig CG, Tropepe V, Morshead CM et al (1996) In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J Neurosci 16: 2649–2658.
Curtis MA, Kam M, Nannmark U et al (2007) Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315:1243–1249.
Doestch F, Alvarez-Buylla A (1996) Network of tangential pathways for neuronal migration in adult mammalian brain. Proc Natl Acad Sci USA 93:14895–14900.
Eriksson PS, Perfilieva E, Björk-Eriksson T et al (1998) Neurogenesis in the adult human hippocampus, Nat Med 4:1313–1317.
Feess-Higgins A, Larroche JC (1987) Development of the human foetal brain, an anatomical atlas. Masson, Paris.
Gould E (2007) How widespread is adult neurogenesis in mammals? Nat Rev Neurosci 8:481–488.
Gould E, Tanapat P, McEwen BS et al (1998) Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc Natl Acad Sci USA 95:3168–3171.
Gould E, Reeves AJ, Fallah M et al (1999a) Hippocampal neurogenesis in adult Old World primates. Proc Natl Acad Sci USA 96:5263–5267.
Gould E, Reeves AJ, Graziano MS et al (1999b) Neurogenesis in the neocortex of adult primates. Science 286:548–552.
Gould E, Vail N, Wagers M et al (2001) Adult-generated hippocampal and neocortical neurons in macaques have a transient existence. Proc Natl Acad Sci USA 98:10910–10917.
Gravel C, Gotz R, Lorrain A et al (1997) Adenoviral gene transfer of ciliary neurotrophic factor and brain-derived neurotrophic factor leads to long-term survival of axotomized motor neurons. Nat Med 3:765–770.
Kaplan MS, Hinds JW (1977) Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197:1092–1094.
Kempermann G, Kuhn HG, Gage FH (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature 386:493–495.
Kornack DR, Rakic P (1999) Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc Natl Acad Sci USA 96:5768–5773.
Kornack DR, Rakic P (2001) The generation, migration, and differentiation of olfactory neurons in the adult primate brain. Proc Natl Acad Sci USA 98:4752–4757.
Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027–2033.
Luskin MB (1993) Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11:173–189.
Mizuno K, Carnahan J, Nawa H (1994) Brain-derived neurotrophic factor promotes differentiation of striatal GABAergic neurons. Dev Biol 165:243–256.
Pencea V, Bingaman KD, Freedman LJ et al (2001a) Neurogenesis in the subventricular zone and rostral migratory stream of the neonatal and adult primate forebrain. Exp Neurol 172:1–16.
Pencea V, Bingaman KD, Wiegand SJ et al (2001b) Infusion of brain-derived neurotrophic factor into lateral ventricle of the adult rat leads to new neurons in the parenchyma of the striatum, septum, thalamus and hypothalamus. J Neurosci 21:6706–6717.
Reynolds BA, Tetzlaff W, Weiss S (1992) A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J Neurosci 12:4565–4574.
Saghatelyan A, Roux P, Migliore M et al (2005) Activity-dependent adjustments of the inhibitory network in the olfactory bulb following early postnatal deprivation. Neuron 46:103–116
Sanai N, Berger MS, Garcia-Verdugo JM et al (2007) Comment on “Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension”. Science 318:393.
Seki T (2002) Hippocampal adult neurogenesis occurs in a microenvironment provided by PSA-NCAM-expressing immature neurons. J Neurosci Res 69:772–783.
Steiner B, Wolf S, Kempermann G (2006) Adult neurogenesis and neurodegenerative disease. Regen Med 1:15–28.
Ventimiglia R, Mather PE, Jones BE et al (1995) The neurotrophins BDNF, NT-3 and NT-4/5 promote survival and morphological and biochemical differentiation of striatal neurons in vitro. Eur J Neurosci 7:213–222.
Acknowledgments
This study was supported by grant MT-8756 of the Canadian Institutes for Health Research (CIHR) to A. Parent. A. Bédard and P.J. Bernier were recipients of CIHR Studentships.
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Bédard, A., Bernier, P.J., Parent, A. (2011). Neurogenesis in Monkey and Human Adult Brain. In: Seki, T., Sawamoto, K., Parent, J.M., Alvarez-Buylla, A. (eds) Neurogenesis in the Adult Brain II. Springer, Tokyo. https://doi.org/10.1007/978-4-431-53945-2_1
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DOI: https://doi.org/10.1007/978-4-431-53945-2_1
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