Interneurons are the source and the targets of the first synapses formed in the rat developing hippocampal circuit

Cerebral Cortex

Volumn 13, Issue 6, 2003, Pages 684-692

  Gozlan, Henri ^a   Ben Ari, Yehezkel ^a  

^a Turing Center for Living Systems CENTURI Aix Marseille University   (France)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR; EXCITATORY AMINO ACID RECEPTOR; GLUTAMATE RECEPTOR;

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN ELECTROPHYSIOLOGY; CELL FUNCTION; CELL MATURATION; CELL STRUCTURE; CELL TYPE; DENDRITE; EMBRYO; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; INTERNEURON; NERVE CELL NETWORK; NERVE CELL STIMULATION; NEWBORN; NONHUMAN; PERIKARYON; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPTOGENESIS;

ANIMALS; ANIMALS, NEWBORN; CELL DIFFERENTIATION; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; INTERNEURONS; NERVE NET; NEURAL PATHWAYS; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; RECEPTORS, GABA-A; SYNAPSES;

EID: 0038580972     PISSN: 10473211     EISSN: None     Source Type: Journal    
DOI: 10.1093/cercor/13.6.684     Document Type: Article

References (37)

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. Ben-Ari Y (2002) Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci 3:728-739.
3. Chen G, Trombley PQ, Van den Pol AN (1995) GABA receptors precede glutamate receptors in hypothalamic development: differential regulation by astrocytes. J Neurophysiol 74:1473-1484.
4. Cope DW, Maccaferri G, Marton LF, Roberts JD, Cobden PM, Somogyi P (2002) Cholecystokinin-immunopositive basket and Schaffer collateral-associated interneurones target different domains of pyramidal cells in the CA1 area of the rat hippocampus. Neuroscience 109:63-80.
5. Diabira D, Hennou S, Chevassus-au-Louis N, Ben-Ari Y, Gozlan H (1999) Late embryonic expression of AMPA receptor function in the CA1 region of the intact hippocampus in vitro. Eur J Neurosci 11:4015-4023.
6. Fletcher TL, De Camilli P, Banker G (1994) Synaptogenesis in hippocampal cultures: evidence indicating that axons and dendrites become competent to form synapses at different stages of neuronal development. J Neurosci 14:6695-6706.
7. Freund TF, Buzsáki G (1996) Interneurons of the hippocampus. Hippocampus 6:347-470.
8. Gubellini P, Ben Ari Y, Gaiarsa JL (2001) Activity- and age-dependent GABAergic synaptic plasticity in the developing rat hippocampus. Eur J Neurosci 14:1937-1946.
9. Gulyás AI, Freund TF (1996) Pyramidal cell dendrites are the primary targets of calbindin D28k-immunoreactive interneurons in the hippocampus. Hippocampus 6:525-534.
10. Gulyás AI, Hájos N, Freund TF (1996) Interneurons containing calretinin are specialized to control other interneurons in the rat hippocampus. J Neurosci 16:3397-3411.
11. Isaac JT, Nicoll RA, Malenka RC (1999) Silent glutamatergic synapses in the mammalian brain. Can J Physiol Pharmacol 77:735-737.
12. Jiang M, Swann JW (1997) Expression of calretinin in diverse neuronal populations during development of rat hippocampus. Neuroscience 81:1137-1154.
13. 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.
14. Khazipov R, Desfreres L, Khalilov I, Ben-Ari Y (1999) Three-independent-compartment chamber to study in vitro commissural synapses. J Neurophysiol 81:921-924.
15. Khazipov R, Esclapez M, Caillard O, Bernard C, Khalilov I, Hirsch J, 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.
16. Koller H, Siebler M, Schmalenbach C, Muller HW (1990) GABA and glutamate receptor development of cultured neurons from rat hippocampus, septal region, and neocortex. Synapse 5:59-64.
17. 2+ rise in pyramidal cells and interneurons from rat neonatal hippocampal slices. J Physiol (Lond) 487:319-329.
18. Miles R, Toth K, Gulyás AI, Hajos N, Freund TF (1996) Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16:815-823.
19. Nishimaru H, Iizuka M, Ozaki S, Kudo N (1996) Spontaneous motoneuronal activity mediated by glycine and GABA in the spinal cord of rat fetuses in vitro. J Physiol (Lond) 497:131-143.
20. Nitsch R, Bergmann I, Kuppers K, Mueller G, Frotscher M (1990) Late appearance of parvalbumin-immunoreactivity in the development of GABAergic neurons in the rat hippocampus. Neurosci Lett 118:147-150.
21. Owens DF, Liu X, Kriegstein AR (1999) Changing properties of GABA(A) receptor-mediated signaling during early neocortical development. J Neurophysiol 82:570-583.
22. Parra P, Gulyás AI, Miles R (1998) How many subtypes of inhibitory cells in the hippocampus? Neuron 20:983-993.
23. Pawelzik H, Hughes DI, Thomson AM (2002) Physiological and morphological diversity of immunocytochemically defined parvalbumin- and cholecystokinin-positive interneurones in CA1 of the adult rat hippocampus. J Comp Neurol 443:346-367.
24. Pena F, Tapia R (1999) Relationships among seizures, extracellular amino acid changes, and neurodegeneration induced by 4-aminopyridine in rat hippocampus: a microdialysis and electroencephalographic study. J Neurochem 72:2006-2014.
25. Perreault P, Avoli M (1991) Physiology and pharmacology of epileptiform activity induced by 4-aminopyridine in rat hippocampal slices. J Neurophysiol 65:771-785.
26. Pleasure SJ, Anderson S, Hevner R, Bagri A, Marin O, Lowenstein DH, Rubenstein JL (2000) Cell migration from the ganglionic eminences is required for the development of hippocampal GABAergic interneurons. Neuron 28:727-740.
27. Solbach S, Celio MR (1991) Ontogeny of the calcium binding protein parvalbumin in the rat nervous system. Anat Embryol (Berl) 184:103-124.
28. Soriano E, Cobas A, Fairen A (1986) Asynchronism in the neurogenesis of GABAergic and non-GABAergic neurons in the mouse hippocampus. Brain Res 395:88-92.
29. Soriano E, Del Rio JA, Martinez A, Super H (1994) Organization of the embryonic and early postnatal murine hippocampus. I. Immunocytochemical characterization of neuronal populations in the subplate and marginal zone. J Comp Neurol 342:571-595.
30. + current in hippocampal neurons. Nature 336:379-381.
31. Sudhof TC (2001) Alpha-latrotoxin and its receptors: neurexins and CIRL/latrophilins. Annu Rev Neurosci 24:933-962.
32. 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.
33. Super H, Martinez A, Del Rio JA, Soriano E (1998) Involvement of distinct pioneer neurons in the formation of layer-specific connections in the hippocampus. J Neurosci 18:4616-4626.
34. 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.
35. Voigt T, Opitz T, de Lima AD (2001) Synchronous oscillatory activity in immature cortical network is driven by GABAergic preplate neurons. J Neurosci 21:8895-8905.
36. Walton MK, Schaffner AE, Barker JL (1993) Sodium channels, GABAA receptors, and glutamate receptors develop sequentially on embryonic rat spinal cord cells. J Neurosci 13:2068-2084.
37. Wang YF, Gao XB, Van den Pol AN (2001) Membrane properties underlying patterns of GABA-dependent action potentials in developing mouse hypothalamic neurons. J Neurophysiol 86:1252-1265.