Development of synaptic connectivity onto interneurons in stratum radiatum in the CA1 region of the rat hippocampus

BMC Neuroscience

Volumn 13, Issue 1, 2012, Pages

  Riebe, Ilse ^a   Hanse, Eric ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; AMPA RECEPTOR; 2 AMINO 5 PHOSPHONOVALERIC ACID; AMINO ACID RECEPTOR BLOCKING AGENT; DRUG DERIVATIVE; LIDOCAINE; LIDOCAINE ETHOBROMIDE; LOCAL ANESTHETIC AGENT; QX-314; SODIUM CHANNEL BLOCKING AGENT; TETRODOTOXIN;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; FEMALE; GABAERGIC SYSTEM; HIPPOCAMPAL CA1 REGION; INTERNEURON; MALE; NERVE CELL DIFFERENTIATION; NEWBORN; NONHUMAN; PYRAMIDAL NERVE CELL; RAT; STRATUM RADIATUM; SYNAPTIC TRANSMISSION; AGE; ANIMAL; BIOPHYSICS; CORPUS STRIATUM; CYTOLOGY; DRUG EFFECT; ELECTROSTIMULATION; GROWTH, DEVELOPMENT AND AGING; IN VITRO STUDY; NERVE TRACT; PATCH CLAMP; PHYSIOLOGY; SYNAPSE; SYNAPTIC POTENTIAL; WISTAR RAT;

2-AMINO-5-PHOSPHONOVALERATE; AGE FACTORS; ANESTHETICS, LOCAL; ANIMALS; ANIMALS, NEWBORN; BIOPHYSICS; CA1 REGION, HIPPOCAMPAL; CORPUS STRIATUM; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; INTERNEURONS; LIDOCAINE; MALE; NEURAL PATHWAYS; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; SODIUM CHANNEL BLOCKERS; SYNAPSES; SYNAPTIC POTENTIALS; TETRODOTOXIN;

EID: 84856097311     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-13-14     Document Type: Article

References (41)

1. Loebel A, Silberberg G, Helbig D, Markram H, Tsodyks M, Richardson MJ. Multiquantal release underlies the distribution of synaptic efficacies in the neocortex. Front Comput Neurosci 2009, 3:27. 2786302, 19956403.
2. Bagnall MW, Hull C, Bushong EA, Ellisman MH, Scanziani M. Multiple clusters of release sites formed by individual thalamic afferents onto cortical interneurons ensure reliable transmission. Neuron 2011, 71:180-194. 10.1016/j.neuron.2011.05.032, 21745647.
3. Branco T, Staras K. The probability of neurotransmitter release: variability and feedback control at single synapses. Nat Rev Neurosci 2009, 10:373-383.
4. Hsia AY, Malenka RC, Nicoll RA. Development of excitatory circuitry in the hippocampus. J Neurophysiol 1998, 79:2013-2024.
5. Groc L, Gustafsson B, Hanse E. Early establishment of multiple release site connectivity between interneurons and pyramidal neurons in the developing hippocampus. Eur J Neurosci 2003, 17:1873-1880. 10.1046/j.1460-9568.2003.02635.x, 12752787.
6. Durand GM, Kovalchuk Y, Konnerth A. Long-term potentiation and functional synapse induction in developing hippocampus. Nature 1996, 381:71-75. 10.1038/381071a0, 8609991.
7. Liao D, Malinow R. Deficiency in induction but not expression of LTP in hippocampal slices from young rats. Learn Mem 1996, 3:138-149. 10.1101/lm.3.2-3.138, 10456084.
8. Hanse E, Gustafsson B. Quantal variability at glutamatergic synapses in area CA1 of the rat neonatal hippocampus. J Physiol 2001, 531:467-480. 10.1111/j.1469-7793.2001.0467i.x, 2278484, 11230519.
9. Gasparini S, Saviane C, Voronin LL, Cherubini E. Silent synapses in the developing hippocampus: lack of functional AMPA receptors or low probability of glutamate release?. Proc Natl Acad Sci USA 2000, 97:9741-9746. 16935, 10931951.
10. Buhl EH, Cobb SR, Halasy K, Somogyi P. Properties of unitary IPSPs evoked by anatomically identified basket cells in the rat hippocampus. Eur J Neurosci 1995, 7:1989-2004. 10.1111/j.1460-9568.1995.tb00721.x, 8528474.
11. Buhl EH, Halasy K, Somogyi P. Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature 1994, 368:823-828. 10.1038/368823a0, 8159242.
12. Gulyas AI, Miles R, Sik A, Toth K, Tamamaki N, Freund TF. Hippocampal pyramidal cells excite inhibitory neurons through a single release site. Nature 1993, 366:683-687. 10.1038/366683a0, 8259211.
13. Arancio O, Korn H, Gulyas A, Freund T, Miles R. Excitatory synaptic connections onto rat hippocampal inhibitory cells may involve a single transmitter release site. J Physiol 1994, 481(Pt 2):395-405. 1155938, 7738832.
14. Biro AA, Holderith NB, Nusser Z. Quantal size is independent of the release probability at hippocampal excitatory synapses. J Neurosci 2005, 25:223-232. 10.1523/JNEUROSCI.3688-04.2005, 15634785.
15. Groc L, Gustafsson B, Hanse E. Spontaneous unitary synaptic activity in CA1 pyramidal neurons during early postnatal development: constant contribution of AMPA and NMDA receptors. J Neurosci 2002, 22:5552-5562.
16. Sun HY, Lyons SA, Dobrunz LE. Mechanisms of target-cell specific short-term plasticity at Schaffer collateral synapses onto interneurones versus pyramidal cells in juvenile rats. J Physiol 2005, 568:815-840. 10.1113/jphysiol.2005.093948, 1464188, 16109728.
17. Wierenga CJ, Wadman WJ. Excitatory inputs to CA1 interneurons show selective synaptic dynamics. J Neurophysiol 2003, 90:811-821. 10.1152/jn.00865.2002, 12904494.
18. Klausberger T, Somogyi P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 2008, 321:53-57. 10.1126/science.1149381, 18599766.
19. Soltesz I, Smetters DK, Mody I. Tonic inhibition originates from synapses close to the soma. Neuron 1995, 14:1273-1283. 10.1016/0896-6273(95)90274-0, 7605636.
20. Williams SR, Mitchell SJ. Direct measurement of somatic voltage clamp errors in central neurons. Nat Neurosci 2008, 11:790-798. 10.1038/nn.2137, 18552844.
21. Markram H, Lubke J, Frotscher M, Roth A, Sakmann B. Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J Physiol 1997, 500(Pt 2):409-440. 1159394, 9147328.
22. Thomson AM, Lamy C. Functional maps of neocortical local circuitry. Front Neurosci 2007, 1:19-42. 10.3389/neuro.01.1.1.002.2007, 2518047, 18982117.
23. Sorra KE, Harris KM. Occurrence and three-dimensional structure of multiple synapses between individual radiatum axons and their target pyramidal cells in hippocampal area CA1. J Neurosci 1993, 13:3736-3748.
24. Biro AA, Holderith NB, Nusser Z. Release probability-dependent scaling of the postsynaptic responses at single hippocampal GABAergic synapses. J Neurosci 2006, 26:12487-12496. 10.1523/JNEUROSCI.3106-06.2006, 2630420, 17135411.
25. Christie JM, Jahr CE. Multivesicular release at Schaffer collateral-CA1 hippocampal synapses. J Neurosci 2006, 26:210-216. 10.1523/JNEUROSCI.4307-05.2006, 2670931, 16399689.
26. Oertner TG, Sabatini BL, Nimchinsky EA, Svoboda K. Facilitation at single synapses probed with optical quantal analysis. Nat Neurosci 2002, 5:657-664.
27. Lisman J, Raghavachari S. A unified model of the presynaptic and postsynaptic changes during LTP at CA1 synapses. Sci STKE 2006, 2006:re11. 10.1126/stke.3562006re11, 17033044.
28. Raastad M, Storm JF, Andersen P. Putative Single Quantum and Single Fibre Excitatory Postsynaptic Currents Show Similar Amplitude Range and Variability in Rat Hippocampal Slices. Eur J Neurosci 1992, 4:113-117. 10.1111/j.1460-9568.1992.tb00114.x, 12106447.
29. Bourne J, Harris KM. Do thin spines learn to be mushroom spines that remember?. Curr Opin Neurobiol 2007, 17:381-386. 10.1016/j.conb.2007.04.009, 17498943.
30. Groc L, Gustafsson B, Hanse E. In vivo evidence for an activity-independent maturation of AMPA/NMDA signaling in the developing hippocampus. Neuroscience 2003, 121:65-72. 10.1016/S0306-4522(03)00366-X, 12946700.
31. Yuste R, Bonhoeffer T. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 2001, 24:1071-1089. 10.1146/annurev.neuro.24.1.1071, 11520928.
32. Kullmann DM, Lamsa KP. Long-term synaptic plasticity in hippocampal interneurons. Nat Rev Neurosci 2007, 8:687-699. 10.1038/nrn2207, 17704811.
33. Riebe I, Gustafsson B, Hanse E. Silent synapses on interneurons in the CA1 stratum radiatum. Eur J Neurosci 2009, 29:1870-1882. 10.1111/j.1460-9568.2009.06734.x, 19473239.
34. Lamsa KP, Heeroma JH, Somogyi P, Rusakov DA, Kullmann DM. Anti-Hebbian long-term potentiation in the hippocampal feedback inhibitory circuit. Science 2007, 315:1262-1266. 10.1126/science.1137450, 17332410.
35. Pelletier JG, Lacaille JC. Long-term synaptic plasticity in hippocampal feedback inhibitory networks. Prog Brain Res 2008, 169:241-250.
36. Lamsa K, Heeroma JH, Kullmann DM. Hebbian LTP in feed-forward inhibitory interneurons and the temporal fidelity of input discrimination. Nat Neurosci 2005, 8:916-924.
37. Abrahamsson T, Gustafsson B, Hanse E. AMPA silencing is a prerequisite for developmental long-term potentiation in the hippocampal CA1 region. J Neurophysiol 2008, 100:2605-2614. 10.1152/jn.90476.2008, 18799599.
38. Xiao MY, Wasling P, Hanse E, Gustafsson B. Creation of AMPA-silent synapses in the neonatal hippocampus. Nat Neurosci 2004, 7:236-243. 10.1038/nn1196, 14966524.
39. Gulyas AI, Toth K, McBain CJ, Freund TF. Stratum radiatum giant cells: a type of principal cell in the rat hippocampus. Eur J Neurosci 1998, 10:3813-3822. 10.1046/j.1460-9568.1998.00402.x, 9875359.
40. Cossart R, Hirsch JC, Cannon RC, Dinoncourt C, Wheal HV, Ben-Ari Y, Esclapez M, Bernard C. Distribution of spontaneous currents along the somato-dendritic axis of rat hippocampal CA1 pyramidal neurons. Neuroscience 2000, 99:593-603. 10.1016/S0306-4522(00)00231-1, 10974423.
41. Kim J, Alger BE. Random response fluctuations lead to spurious paired-pulse facilitation. J Neurosci 2001, 21:9608-9618.