The establishment of GABAergic and glutamatergic synapses on CA1 pyramidal neurons is sequential and correlates with the development of the apical dendrite

Journal of Neuroscience

Volumn 19, Issue 23, 1999, Pages 10372-10382

  Tyzio, Roman ^a   Represa, Alfonso ^a   Jorquera, Isabel ^a   Ben Ari, Yehezkel ^a   Gozlan, Henri ^a   Aniksztejn, Laurent ^a  

^a INSERM   (France)

Author keywords

AMPA receptors; CA1 pyramidal cells; Development; GABA(A) receptors; NMDA receptors; Synaptic transmission

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; AMPA RECEPTOR; GLUTAMATE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL CELL; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; DENDRITE; EMBRYO DEVELOPMENT; GABAERGIC SYSTEM; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPSE; SYNAPTIC TRANSMISSION;

EID: 0033499932     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-23-10372.1999     Document Type: Article

References (41)

1. Altman J, Bayer SA (1990) Prolonged sojourn of developing pyramidal cells in the intermediate zone of the hippocampus and their settling in the stratum pyramidale. J Comp Neurol 301:343-364.
2. 3H]thymidine autoradiography. J Comp Neurol 190:87-114.
3. Ben-Ari Y, Cherubini E, Corradetti R, Gaiarsa JL (1989) Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol (Lond) 416:303-325.
4. A, NMDA and AMPA receptors: a developmentally regulated "menage a trois". Trends Neurosci 20:523-529.
5. Blanton MG, Kriegstein AR (1992) Properties of amino acid neurotransmitter receptors of embryonic cortical neurons when activated by exogenous and endogenous agonists. J Neurophysiol 67:1185-1200.
6. Chen G, Trombley PQ, Van Den Pol AN (1995) GABA receptors precede glutamate receptors in hypothalamic development; differential regulation by astrocytes. J Neurophysiol 74:1473-1483.
7. Cherubini E, Gaiarsa JL, Ben-Ari Y (1991) GABA: an excitatory transmitter in early postnatal life. Trends Neurosci 14:515-519.
8. 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.
9. Durand GM, Kovalchuk Y, Konnerth A (1996) Long-term potentiation and functional synapse induction in developing hippocampus. Nature 381:71-75.
10. A receptor subtypes requires the gamma 2 subunit and gephryn. Nat Neurosci 1:563-571.
11. Gaiarsa JL, McLean H, Congar P, Leinekugel X, Khazipov R, Tseeb V, Ben-Ari Y (1995) Postnatal maturation of γ-aminobutyric acid A and B-mediated inhibition in the CA3 hippocampal region of the rat. J Neurobiol 26:339-349.
12. Garaschuk O, Hanse E, Konnerth A (1998) Developmental profile and synaptic origin of early network oscillations in the CA1 region of rat neonatal hippocampus. J Physiol (Lond) 507:219-236.
13. Hamill OP, Marty A, Neher E, Sakmann B (1981) Improved patch-clamp techniques for high-resolution current recording from cell and cell-free membrane patches. Pflügers Arch 391:85-100.
14. Hosokawa Y, Sciancalepore M, Stratta F, Martina M, Cherubini E (1994) Developmental changes in spontaneous GABAA-mediated synaptic events in rat hippocampal CA3 neurons. Eur J Neurosci 6:805-813.
15. Hsia AY, Malenka RC, Nicoll RA (1998) Development of excitatory circuitry in the hippocampus. J Neurophysiol 79:2013-2024.
16. Isaac JT, Crair MC, Nicoll RA, Malenka RC (1997) Silent synapses during development of thalamocortical inputs. Neuron 18:269-280.
17. Khazipov R, Leinekugel X, Khalilov I, Gaiarsa JL, Ben-Ari Y (1997) Synchronization of GABAergic interneuronal network in CA3 subfield of neonatal rat hippocampal slices. J Physiol (Lond) 498:763-772.
18. Killisch I, Dotti CG, Laurie DJ, Lüddens H, Seeburg PH (1991) Expression patterns of GABAA receptor subtypes in developing hippocampal neurons. Neuron 7:927-936.
19. Kirov SA, Harris KM (1999) Slices have more synapses than perfusion-fixed hippocampus from both young and mature rats. J Neurosci 19:2876-2886.
20. Kossel AH, Williams CV, Schweizer M, Kater SB (1997) Afferent innervation influences the development of dendritic branches and spines via both activity-dependent and non-activity-dependent mechanisms. J Neurosci 17:6314-6324.
21. 2+ oscillations mediated by the synergistic excitatory actions of GABAA and NMDA receptors in the neonatal hippocampus. Neuron 18:243-255.
22. Liao D, Zhang X, O'Brien R, Ehlers MD, Huganir RL (1999) Regulation of morphological postsynaptic silent synapses in developing hippocampal neurons. Nature 2:37-43.
23. Liu YB, Lio PA, Pasternak JF, Trommer BL (1996) Developmental changes in membrane properties and postsynaptic currents of granule cells in rat dentate gyrus. J Neurophysiol 76:1074-1088.
24. 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.
25. Malenka RC, Nicoll RA (1997) Silent synapses speak up. Neuron 19:473-476.
26. Marin-Padilla M (1992) Ontogenesis of the pyramidal cell of the mammalian neocortex and developmental cytoarchitectonics: a unifying theory. J Comp Neurol 321:223-240.
27. Martinez A, Alcantara S, Borrell V, Del RJ, Blasi J, Otal R, Campos N, Boronat A, Barbacid M, Silos-Santiago I, Soriano E (1998) TrkB and TrkC signaling are required for maturation and synaptogenesis of hippocampal connections. J Neurosci 18:7336-7350.
28. 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.
29. Petralia RS, Esteban JA, Wang YX, Partridge JG, Zhao HM, Wenthold RJ, Malinow R (1999) Selective acquisition of AMPA receptors over postnatal development suggests a molecular basis for silent synapses. Nature 2:31-36.
30. Rajan I, Cline HT (1998) Glutamate receptor activity is required for normal development of tectal cell dendrites in vivo. J Neurosci 18:7836-7846.
31. Rao A, Kim E, Sheng M, Craig AM (1998) Heterogeneity in the molecular composition of excitatory postsynaptic sites during development of hippocampal neurons in culture. J Neurosci 18:1217-1229.
32. - co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397:251-255.
33. Rozenberg F, Robain O, Jardin L, Ben-Ari Y (1989) Distribution of GABAergic neurons in late fetal and early postnatal rat hippocampus. Dev Brain Res 50:177-187.
34. - ion channels exhibit heterogenous channel properties. Eur J Neurosci 10:1771-1783.
35. Soriano E, Cobas A, Fairen A (1989) Neurogenesis of glutamic acid decarboxylase immunoreactive cells in the hippocampus of the mouse. I: Regio superior and regio inferior. J Comp Neurol 281:586-602.
36. 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.
37. Super H, Martinez A, Del RJ, Soriano E (1998) Involvement of distinct pioneer neurons in the formation of layer-specific connections in the hippocampus. J Neurosci 18:4616-4626.
38. Vicario-Abejon C, Collin C, McKay RDG, Segal M (1998) Neurotrophins induce formation of functional excitatory and inhibitory synapses between cultured hippocampal neurons. J Neurosci 18:7256-7271.
39. A receptors, and glutamate receptors develop sequentially on embryonic rat spinal cord cells. J Neurosci 2068-2084.
40. Wu G, Malinow R, Cline HT (1996) Maturation of a central glutamatergic synapse. Science 274:972-976.
41. Ziv N, Smith SJ (1996) Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 17:91-102.