Neuronal differentiation in the adult hippocampus recapitulates embryonic development

Journal of Neuroscience

Volumn 25, Issue 44, 2005, Pages 10074-10086

  Espósito, M Soledad ^a   Piatti, Verónica C ^a   Laplagne, Diego A ^a   Morgenstern, Nicolás A ^a   Ferrari, Carina C ^a   Pitossi, Fernando J ^a   Schinder, Alejandro F ^a  

^a FUNDACIÓN INSTITUTO LELOIR   (Argentina)

Author keywords

Dentate gyrus; GABA; Glutamate; Neurogenesis; Plasticity; Synaptogenesis

Indexed keywords

4 AMINOBUTYRIC ACID; GLUTAMIC ACID; GREEN FLUORESCENT PROTEIN;

ANIMAL CELL; ARTICLE; CELL MATURATION; CELL MIGRATION; CELLULAR DISTRIBUTION; DENDRITIC CELL; DENTATE GYRUS; EMBRYO DEVELOPMENT; FEMALE; GABAERGIC TRANSMISSION; GRANULE CELL; HIPPOCAMPUS; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; SYNAPTIC TRANSMISSION; SYNAPTOGENESIS;

AGING; ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; FEMALE; HIPPOCAMPUS; MICE; MICE, INBRED C57BL; NEURONS;

EID: 27744484327     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3114-05.2005     Document Type: Article

References (69)

1. 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 301:365-381.
2. Alvarez-Buylla A, Seri B, Doetsch F (2002) Identification of neural stem cells in the adult vertebrate brain. Brain Res Bull 57:751-758.
3. Ambrogini P, Lattanzi D, Ciuffoli S, Agostini D, Bertini L, Stocchi V, Santi S, Cuppini R (2004) Morpho-functional characterization of neuronal cells at different stages of maturation in granule cell layer of adult rat dentate gyrus. Brain Res 1017:21-31.
4. Angevine Jr JB (1965) Time of neuron origin in the hippocampal region. An autoradiographic study in the mouse. Exp Neurol Suppl 2:1-70.
5. A, slow. J Neurosci 18:1305-1317.
6. A receptor-mediated inhibitory postsynaptic currents in hippocampus. J Neurophysiol 88:3097-3107.
7. Barry PH, Lynch JW (1991) Liquid junction potentials and small cell effects in patch-clamp analysis. J Membr Biol 121:101-117.
8. Bayer SA, Yackel JW, Puri PS (1982) Neurons in the rat dentate gyrus granular layer substantially increase during juvenile and adult life. Science 216:890-892.
9. Belluzzi O, Benedusi M, Ackman J, LoTurco JJ (2003) Electrophysiological differentiation of new neurons in the olfactory bulb. J Neurosci 23:10411-10418.
10. Ben Ari Y (2002) Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci 3:728-739.
11. Brown JP, Couillard-Despres S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG (2003) Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1-10.
12. 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.
13. Carleton A, Petreanu LT, Lansford R, Alvarez-Buylla A, Lledo PM (2003) Becoming a new neuron in the adult olfactory bulb. Nat Neurosci 6:507-518.
14. Duman RS (2004) Depression: a case of neuronal life and death? Biol Psychiatry 56:140-145.
15. Dupuy ST, Houser CR (1996) Prominent expression of two forms of glutamate decarboxylase in the embryonic and early postnatal rat hippocampal formation. J Neurosci 16:6919-6932.
16. Dupuy-Davies S, Houser CR (1999) Evidence for changing positions of GABA neurons in the developing rat dentate gyrus. Hippocampus 9:186-199.
17. Freund TF (2003) Interneuron diversity series: rhythm and mood in perisomatic inhibition. Trends Neurosci 26:489-495.
18. Freund TF, Buzsaki G (1996) Interneurons of the hippocampus. Hippocampus 6:347-470.
19. Gage FH (2000) Mammalian neural stem cells. Science 287:1433-1438.
20. Ganguly K, Schinder AF, Wong ST, Poo M (2001) GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell 105:521-532.
21. Garcia AD, Doan NB, Imura T, Bush TG, Sofroniew MV (2004) GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci 7:1233-1241.
22. 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.
23. Gozlan H, Ben Ari Y (2003) Interneurons are the source and the targets of the first synapses formed in the rat developing hippocampal circuit. Cereb Cortex 13:684-692.
24. A and glutamatergic synapses on CA1 interneurons of the rat fetal hippocampus. Eur J Neurosci 16:197-208.
25. Hollrigel GS, Soltesz I (1997) Slow kinetics of miniature IPSCs during early postnatal development in granule cells of the dentate gyrus. J Neurosci 17:5119-5128.
26. - accumulation and depletion in cultured rat midbrain neurons. J Neurosci 19:4695-4704.
27. 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 13:413-427.
28. A receptor channel function in the nervous system. Prog Neurobiol 42:489-537.
29. 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.
30. Khazipov R, Esclapez M, Caillard O, Bernard C, Khalilov I, Tyzio R, Hirsch J, Dzhala V, Berger B, Ben Ari Y (2001) Early development of neuronal activity in the primate hippocampus in utero. J Neurosci 21:9770-9781.
31. Khirug S, Huttu K, Ludwig A, Smirnov S, Voipio J, Rivera C, Kaila K, Khiroug L (2005) Distinct properties of functional KCC2 expression in immature mouse hippocampal neurons in culture and in acute slices. Eur J Neurosci 21:899-904.
32. Kokaia Z, Lindvall O (2003) Neurogenesis after ischaemic brain insults. Curr Opin Neurobiol 13:127-132.
33. A receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J Neurosci 12:4151-4172.
34. 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 23:732-736.
35. Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264:1145-1148.
36. LoTurco JJ, Owens DF, Heath MJ, Davis MB, Kriegstein AR (1995) GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15:1287-1298.
37. Lübbers K, Frotscher M (1988) Differentiation of granule cells in relation to GABAergic neurons in the rat fascia dentata. Combined Golgi/EM and immunocytochemical studies. Anat Embryol (Berl) 178:119-127.
38. Madsen TM, Kristjansen PE, Bolwig TG, Wortwein G (2003) Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience 119:635-642.
39. Marty S, Berninger B, Carroll P, Thoenen H (1996) GABAergic stimulation regulates the phenotype of hippocampal interneurons through the regulation of brain-derived neurotrophic factor. Neuron 16:565-570.
40. McCabe BK, Silveira DC, Cilio MR, Cha BH, Liu X, Sogawa Y, Holmes GL (2001) Reduced neurogenesis after neonatal seizures. J Neurosci 21:2094-2103.
41. Miles R, Toth K, Gulyas AI, Hajos N, Freund TF (1996) Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16:815-823.
42. Morozov YM, Freund TF (2003) Postnatal development and migration of cholecystokinin-immunoreactive interneurons in rat hippocampus. Neuroscience 120:923-939.
43. Mullen RJ, Buck CR, Smith AM (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201-211.
44. Nottebohm F (2002) Neuronal replacement in adult brain. Brain Res Bull 57:737-749.
45. Overstreet Wadiche LS, Bromberg DA, Bensen AL, Westbrook GL (2005) GABAergic signaling to newborn neurons in dentate gyrus. J Neurophysiol, in press.
46. Owens DF, Boyce LH, Davis MB, Kriegstein AR (1996) Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. J Neurosci 16:6414-6423.
47. Parent JM, Lowenstein DH (2002) Seizure-induced neurogenesis: are more new neurons good for an adult brain? Prog Brain Res 135:121-131.
48. Parent JM, Yu TW, Leibowitz RT, Geschwind DH, Sloviter RS, Lowenstein DH (1997) Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 17:3727-3738.
49. A responses in rat hippocampus. Neuron 10:189-200.
50. - co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397:251-255.
51. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S, Weisstaub N, Lee J, Duman R, Arancio O, Belzung C, Hen R (2003) Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301:805-809.
52. Schinder AF, Gage FH (2004) A hypothesis about the role of adult neurogenesis in hippocampal function. Physiology (Bethesda) 19:253-261.
53. Schmidt-Hieber C, Jonas P, Bischofberger J (2004) Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429:184-187.
54. Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A (2001) Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21:7153-7160.
55. Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E (2001) Neurogenesis in the adult is involved in the formation of trace memories. Nature 410:372-376.
56. Soltesz I, Smetters DK, Mody I (1995) Tonic inhibition originates from synapses close to the soma. Neuron 14:1273-1283.
57. Song HJ, Stevens CF, Gage FH (2002) Neural stem cells from adult hippocampus develop essential properties of functional CNS neurons. Nat Neurosci 5:438-445.
58. Super H, Soriano E (1994) The organization of the embryonic and early postnatal murine hippocampus. II. Development of entorhinal, commissural, and septal connections studied with the lipophilic tracer DiI. J Comp Neurol 344:101-120.
59. Tanaka T, Serneo FF, Tseng HC, Kulkarni AB, Tsai LH, Gleeson JG (2004) Cdk5 phosphorylation of doublecortin ser297 regulates its effect on neuronal migration. Neuron 41:215-227.
60. Toda H, Takahashi J, Mizoguchi A, Koyano K, Hashimoto N (2000) Neurons generated from adult rat hippocampal stem cells form functional glutamatergic and GABAergic synapses in vitro. Exp Neurol 165:66-76.
61. Tyzio R, Represa A, Jorquera I, Ben Ari Y, Gozlan H, Aniksztejn L (1999) The establishment of GABAergic and glutamatergic synapses on CA1 pyramidal neurons is sequential and correlates with the development of the apical dendrite. J Neurosci 19:10372-10382.
62. Tyzio R, Ivanov A, Bernard C, Holmes GL, Ben Ari Y, Khazipov R (2003) Membrane potential of CA3 hippocampal pyramidal cells during postnatal development. J Neurophysiol 90:2964-2972.
63. 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.
64. van Praag H, Kempermann G, Gage FH (2000) Neural consequences of environmental enrichment. Nat Rev Neurosci 1:191-198.
65. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH (2002) Functional neurogenesis in the adult hippocampus. Nature 415:1030-1034.
66. Wang LP, Kempermann G, Kettenmann H (2005) A subpopulation of precursor cells in the mouse dentate gyrus receives synaptic GABAergic input. Mol Cell Neurosci 29:181-189.
67. Xu L, Yee JK, Wolff JA, Friedmann T (1989) Factors affecting long-term stability of Moloney murine leukemia virus-based vectors. Virology 171:331-341.
68. Ye GL, Yi S, Gamkrelidze G, Pasternak JF, Trommer BL (2005) AMPA and NMDA receptor-mediated currents in developing dentate gyrus granule cells. Brain Res Dev Brain Res 155:26-32.
69. Zhang ZW (2004) Maturation of layer V pyramidal neurons in the rat prefrontal cortex: intrinsic properties and synaptic function. J Neurophysiol 91:1171-1182.