The Timing of Neuronal Development in Adult Hippocampal Neurogenesis

Abstract

The granule cell layer (GCL) of the adult dentate gyrus (DG) is a heterogeneous structure formed by neurons of different ages because a significant proportion of neurons continues to be generated throughout life. The subgranular zone of the DG contains neural progenitor cells (NPCs) that divide, differentiate, and migrate to produce functional dentate granule cells (DGCs) that become incorporated into the existing hippocampal circuitry. New available tools to identify adult-born neurons in live and fixed brain sections have allowed the transition from NPC to functional neuron to be characterized in great detail. Maturation of the neuronal phenotype includes changes in membrane excitability and morphology as well as the establishment of appropriate connectivity within the existing circuits, a process that lasts several weeks. The events leading to neuronal maturation share many of the features of the developing brain, and electrical activity is emerging as a key modulator of neuronal development in the adult DG. The underlying mechanisms are now beginning to be understood.

Keywords

Adult hippocampus Differentiation Functional integration Neural progenitor cells Stem cells Synaptogenesis

Get full access to this article

View all access options for this article.

References

Abrous DN , Koehl M , Le Moal M. 2005. Adult neurogenesis: from precursors to network and physiology. Physiol Rev 85(2): 523-569.

Aimone JB , Wiles J , Gage FH. 2006. Potential role for adult neurogenesis in the encoding of time in new memories. Nat Neurosci 9(6): 723-727.

Altman J , Bayer SA. 1990. Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J Comp Neurol 301(3): 365-381.

Ambrogini P , Lattanzi D , Ciuffoli S , Agostini D , Bertini L , Stocchi V , and others. 2004. Morpho-functional characterization of neuronal cells at different stages of maturation in granule cell layer of adult rat dentate gyrus. Brain Res 1017(1-2): 21-31.

Ben Ari Y. 2002. Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci 3(9): 728-739.

Bruel-Jungerman E , Davis S , Rampon C , Laroche S. 2006. Long-term potentiation enhances neurogenesis in the adult dentate gyrus. J Neurosci 26(22): 5888-5893.

Deisseroth K , Singla S , Toda H , Monje M , Palmer TD , Malenka RC. 2004. Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 42(4): 535-552.

Espósito MS , Piatti VC , Laplagne DA , Morgenstern NA , Ferrari CC , Pitossi FJ , and others. 2005. Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J Neurosci 25(44): 10074-10086.

Ge S , Goh EL , Sailor KA , Kitabatake Y , Ming GL , Song H. 2006. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439(7076): 589-593.

10.

Hastings NB , Gould E. 1999. Rapid extension of axons into the CA3 region by adult-generated granule cells. J Comp Neurol 413(1): 146-154.

11.

Jessberger S , Kempermann G. 2003. Adult-born hippocampal neurons mature into activity-dependent responsiveness. Eur J Neurosci 18(10): 2707-2712.

12.

Jones SP , Rahimi O , O’Boyle MP , Diaz DL , Claiborne BJ. 2003. Maturation of granule cell dendrites after mossy fiber arrival in hippocampal field CA3. Hippocampus 13(3): 413-427.

13.

Karten YJ , Jones MA , Jeurling SI , Cameron HA. 2006. GABAergic signaling in young granule cells in the adult rat and mouse dentate gyrus. Hippocampus 16(3): 312-320.

14.

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(2): 391-399.

15.

Liu S , Wang J , Zhu D , Fu Y , Lukowiak K , Lu YM. 2003. Generation of functional inhibitory neurons in the adult rat hippocampus. J Neurosci 23(3): 732-736.

16.

Lledo PM , Alonso M , Grubb MS. 2006. Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 7(3): 179-193.

17.

Ming GL , Song H. 2005. Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28: 223-250.

18.

Muller D , Nikonenko I. 2003. Dynamic presynaptic varicosities: a role in activity-dependent synaptogenesis. Trends Neurosci 26(11): 573-575.

19.

Overstreet-Wadiche LS , Bensen AL , Westbrook GL. 2006. Delayed development of adult-generated granule cells in dentate gyrus. J Neurosci 26(8): 2326-2334.

20.

Overstreet-Wadiche LS , Bromberg DA , Bensen AL , Westbrook GL. 2005. GABAergic signaling to newborn neurons in dentate gyrus. J Neurophysiol 94(6): 4528-4532.

21.

Overstreet-Wadiche LS , Bromberg DA , Bensen AL , Westbrook GL. 2006. Seizures accelerate functional integration of adult-generated granule cells. J Neurosci 26(15): 4095-4103.

22.

Overstreet-Wadiche LS , Westbrook GL. 2006. Functional maturation of adult-generated granule cells. Hippocampus 16(3): 208-215.

23.

Payne JA , Rivera C , Voipio J , Kaila K. 2003. Cation-chloride co-trans-porters in neuronal communication, development and trauma. Trends Neurosci 26(4): 199-206.

24.

Schinder AF , Gage FH. 2004. A hypothesis about the role of adult neuro-genesis in hippocampal function. Physiology (Bethesda) 19: 253-261.

25.

Schmidt-Hieber C , Jonas P , Bischofberger J. 2004. Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429(6988): 184-187.

26.

Snyder JS , Kee N , Wojtowicz JM. 2001. Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. J Neurophysiol 85(6): 2423-2431.

27.

Tashiro A , Sandler VM , Toni N , Zhao C , Gage FH. NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrus. Nature. 2006 Aug 24;442(7105): 929-933. Epub 2006 Aug 13.

28.

Tozuka Y , Fukuda S , Namba T , Seki T , Hisatsune T. 2005. GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 47(6): 803-815.

29.

van Praag H , Schinder AF , Christie BR , Toni N , Palmer TD , Gage FH. 2002. Functional neurogenesis in the adult hippocampus. Nature 415(6875): 1030-1034.

30.

Wang LP , Kempermann G , Kettenmann H. 2005. A subpopulation of precursor cells in the mouse dentate gyrus receives synaptic GABAergic input. Mol Cell Neurosci 29(2): 181-189.

31.

Wang S , Scott BW , Wojtowicz JM. 2000. Heterogenous properties of dentate granule neurons in the adult rat. J Neurobiol 42(2): 248-257.

32.

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(1): 3-11.

Supplementary Material

Please find the following supplemental material available below.

For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.

For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.

0.00 MB

1.54 MB