GABAB receptor modulation of feedforward inhibition through hippocampal neurogliaform cells

Journal of Neuroscience

Volumn 28, Issue 27, 2008, Pages 6974-6982

  Price, Christopher J ^a,c   Scott, Ricardo ^b   Rusakov, Dmitri A ^b   Capogna, Marco ^a  

^a MRC Anat Neuropharmacology Unit   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c QUEEN S UNIVERSITY   (Canada)

Author keywords

Ca2+ imaging; Feedforward inhibition; GABAB receptor; Interneuron; Synaptic transmission; Temporoammonic path

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; BACLOFEN; BENZYL[3 [[1 (3,4 DICHLOROPHENYL)ETHYL]AMINO] 2 HYDROXYPROPYL]PHOSPHINIC ACID; CALCIUM; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID RECEPTOR STIMULATING AGENT; PHOSPHINIC ACID DERIVATIVE; PROPANOLAMINE DERIVATIVE;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; CALCIUM SIGNALING; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EVOKED RESPONSE; GLIA CELL; HIPPOCAMPUS; MICROSCOPY; NERVE FIBER; NONHUMAN; POSITIVE FEEDBACK; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; SYNAPSE; ANIMAL; CYTOLOGY; DRUG EFFECT; GLIA; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; METABOLISM; NERVE CELL INHIBITION; NERVE TRACT; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; RAT; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ANIMALS; BACLOFEN; CALCIUM; CALCIUM SIGNALING; GABA AGONISTS; GABA ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; INHIBITORY POSTSYNAPTIC POTENTIALS; INTERNEURONS; NEURAL INHIBITION; NEURAL PATHWAYS; NEUROGLIA; ORGAN CULTURE TECHNIQUES; PHOSPHINIC ACIDS; PROPANOLAMINES; PYRAMIDAL CELLS; RATS; RECEPTORS, GABA-A; RECEPTORS, GABA-B; SYNAPTIC TRANSMISSION;

EID: 49049098339     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4673-07.2008     Document Type: Article

References (58)

1. Amaral DG, Witter MP (1995) Hippocampal formation, Ed 2. San Diego: Academic.
2. Ault B, Nadler JV (1982) Baclofen selectively inhibits transmission at synapses made by axons of CA3 pyramidal cells in the hippocampal slice. J Pharmacol Exp Ther 223:291-297.
3. Bertrand S, Lacaille JC (2001) Unitary synaptic currents between lacunosum-moleculare interneurones and pyramidal cells in rat hippocampus. J Physiol 532:369-384.
4. Blitz DM, Regehr WG (2005) Timing and specificity of feed-forward inhibition within the LGN. Neuron 45:917-928.
5. Brandt A, Khimich D, Moser T (2005) Few CaV1.3 channels regulate the exocytosis of a synaptic vesicle at the hair cell ribbon synapse. J Neurosci 25:11577-11585.
6. Buzsáki G (1984) Feed-forward inhibition in the hippocampal formation. Prog Neurobiol 22:131-153.
7. Buzsáki G (2002) Theta oscillations in the hippocampus. Neuron 33:325-340.
8. Colbert CM, Levy WB (1992) Electrophysiological and pharmacological characterization of perforant path synapses in CA1: mediation by glutamate receptors. J Neurophysiol 68:1-8.
9. Desmond NL, Scott CA, Jane JA Jr, Levy WB (1994) Ultrastructural identification of entorhinal cortical synapses in CA1 stratum lacunosum-moleculare of the rat. Hippocampus 4:594-600.
10. Dvorak-Carbone H, Schuman EM (1999) Patterned activity in stratum lacunosum moleculare inhibits CA1 pyramidal neuron firing. J Neurophysiol 82:3213-3222.
11. Empson RM, Heinemann U (1995a) Perforant path connections to area CA1 are predominantly inhibitory in the rat hippocampal-entorhinal cortex combined slice preparation. Hippocampus 5:104-107.
12. Empson RM, Heinemann U (1995b) The perforant path projection to hippocampal area CA1 in the rat hippocampal-entorhinal cortex combined slice. J Physiol 484:707-720.
13. Freund TF, Buzsáki G (1996) Interneurons of the hippocampus. Hippocampus 6:347-470.
14. Fuentealba P, Klausberger T, Karayannis T, Huck J, Suen W, Studer M, Capogna M, Somogyi P (2006) Firing pattern and synaptic targets of GABAergic neurogliaform cells in the hippocampus in vivo. Paper presented at Fifth Forum of European Neuroscience, Vienna, July.
15. Fuentealba P, Begum R, Capogna M, Jinno S, Márton LF, Csicsvari J, Thomson A, Somogyi P, Klausberger T (2008) Ivy cells: a population of nitric-oxide-producing, slow-spiking GABAergic neurons and their involvement in hippocampal network activity. Neuron 57:917-929.
16. Gabernet L, Jadhav SP, Feldman DE, Carandini M, Scanziani M (2005) Somatosensory integration controlled by dynamic thalamocortical feed-forward inhibition. Neuron 48:315-327.
17. + current in voltage-clamped CA3 pyramidal cells in hippocampal cultures. Proc Natl Acad Sci U S A 82:1558-1562.
18. Gloveli T, Schmitz D, Empson RM, Dugladze T, Heinemann U (1997) Morphological and electrophysiological characterization of layer III cells of the medial entorhinal cortex of the rat. Neuroscience 77:629-648.
19. + channels control action potential backpropagation. J Physiol 551:49-65.
20. Jarsky T, Roxin A, Kath WL, Spruston N (2005) Conditional dendritic spike propagation following distal synaptic activation of hippocampal CA1 pyramidal neurons. Nat Neurosci 8:1667-1676.
21. Kaiser KM, Zilberter Y, Sakmann B (2001) Back-propagating action potentials mediate calcium signalling in dendrites of bitufted interneurons in layer 2/3 of rat somatosensory cortex. J Physiol 535:17-31.
22. Kiss J, Buzsaki G, Morrow JS, Glantz SB, Leranth C (1996) Entorhinal cortical innervation of parvalbumin-containing neurons (Basket and Chandelier cells) in the rat Ammon's horn. Hippocampus 6:239-246.
23. 2+ channel clustering, and vesicle release. Science 312:1051-1054.
24. Maccaferri G, Lacaille JC (2003) Interneuron diversity series: hippocampal interneuron classifications - making things as simple as possible, not simpler. Trends Neurosci 26:564-571.
25. McBain CJ, Fisahn A (2001) Interneurons unbound. Nat Rev Neurosci 2:11-23.
26. Mittmann W, Koch U, Hausser M (2005) Feed-forward inhibition shapes the spike output of cerebellar Purkinje cells. J Physiol 563:369-378.
27. Ouardouz M, Lacaille JC (1997) Properties of unitary IPSCs in hippocampal pyramidal cells originating from different types of interneurons in young rats. J Neurophysiol 77:1939-1949.
28. Overstreet LS, Westbrook GL (2003) Synapse density regulates independence at unitary inhibitory synapses. J Neurosci 23:2618-2626.
29. A responses in rat hippocampus. Neuron 10:189-200.
30. Pouille F, Scanziani M (2001) Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293:1159-1163.
31. Price CJ, Cauli B, Kovacs ER, Kulik A, Lambolez B, Shigemoto R, Capogna M (2005) Neurogliaform neurons form a novel inhibitory network in the hippocampal CA1 area. J Neurosci 25:6775-6786.
32. Remondes M, Schuman EM (2002) Direct cortical input modulates plasticity and spiking in CA1 pyramidal neurons. Nature 416:736-740.
33. 2+ depletion contributes to fast activity-dependent modulation of synaptic transmission in the brain. Neuron 37:287-297.
34. 2+ current modulation by mGluRs at individual hippocampal synapses. Cereb Cortex 14:748-758.
35. Sakaba T, Neher E (2003) Direct modulation of synaptic vesicle priming by GABA(B) receptor activation at a glutamatergic synapse. Nature 424:775-778.
36. Scanziani M (2000) GABA spillover activates postsynaptic GABA(B) receptors to control rhythmic hippocampal activity. Neuron 25:673-681.
37. Scanziani M, Gähwiler BH, Charpak S (1998) Target cell-specific modulation of transmitter release at terminals from a single axon. Proc Natl Acad Sci U S A 95:12004-12009.
38. 2+ dynamics at individual mossy fiber-CA3 pyramidal cell synapses. J Neurosci 26:7071-7081.
39. Simon A, Oláh S, Molnár G, Szabadics J, Tamás G (2005) Gap-junctional coupling between neurogliaform cells and various interneuron types in the neocortex. J Neurosci 25:6278-6285.
40. Somogyi P, Klausberger T (2005) Defined types of cortical interneurone structure space and spike timing in the hippocampus. J Physiol (Lond) 562:9-26.
41. Swadlow HA (2003) Fast-spike interneurons and feedforward inhibition in awake sensory neocortex. Cereb Cortex 13:25-32.
42. A,fast. Proc Natl Acad Sci U S A 104:14831-14836.
43. B receptor. J Neurosci 18:3138-3146.
44. Tamás G, Lorincz A, Simon A, Szabadics J (2003) Identified sources and targets of slow inhibition in the neocortex. Science 299:1902-1905.
45. Telgkamp P, Padgett DE, Ledoux VA, Woolley CS, Raman IM (2004) Maintenance of high-frequency transmission at Purkinje to cerebellar nuclear synapses by spillover from boutons with multiple release sites. Neuron 41:113-126.
46. Thompson SM, Capogna M, Scanziani M (1993) Presynaptic inhibition in the hippocampus. Trends Neurosci 16:222-227.
47. Topolnik L, Azzi M, Morin F, Kougioumoutzakis A, Lacaille JC (2006) mGluR1/5 subtype-specific calcium signalling and induction of long-term potentiation in rat hippocampal oriens/alveus interneurones. J Physiol 575:115-131.
48. Turner DA (1990) Feed-forward inhibitory potentials and excitatory interactions in guinea-pig hippocampal pyramidal cells. J Physiol 422:333-350.
49. Vida I, Halasy K, Szinyei C, Somogyi P, Buhl EH (1998) Unitary IPSPs evoked by interneurons at the stratum radiatum-stratum lacunosum-moleculare border in the CA1 area of the rat hippocampus in vitro. J Physiol 506:755-773.
50. Vigot R, Barbieri S, Bräuner-Osborne H, Turecek R, Shigemoto R, Zhang YP, Luján R, Jacobson LH, Biermann B, Fritschy JM, Vacher CM, Müller M, Sansig G, Guetg N, Cryan JF, Kaupmann K, Gassmann M, Oertner TG, Bettler B (2006) Differential compartmentalization and distinct functions of GABAB receptor variants. Neuron 50:589-601.
51. B receptor-mediated inhibitory postsynaptic potentials evoked by electrical stimulation and by glutamate stimulation of interneurons in stratum lacunosum-moleculare in hippocampal CA1 pyramidal cells in vitro. Synapse 11:249-258.
52. Williams S, Samulack DD, Beaulieu C, LaCaille JC (1994) Membrane properties and synaptic: responses of interneurons located near the stratum lacunosum-moleculare/radiatum border of area CA1 in whole-cell recordings from rat hippocampal slices. J Neurophysiol 71:2217-2235.
53. Witter MP, Griffioen AW, Jorritsma-Byham B, Krijnen JL (1988) Entorhinal projections to the hippocampal CA1 region in the rat: an underestimated pathway. Neurosci Lett 85:193-198.
54. Wozny C, Gabriel S, Jandova K, Schulze K, Heinemann U, Behr J (2005) Entorhinal cortex entrains epileptiform activity in CA1 in pilocarpine-treated rats. Neurobiol Dis 19:451-460.
55. Yeckel MF, Berger TW (1990) Feedforward excitation of the hippocampus by afferents from the entorhinal cortex: redefinition of the role of the trisynaptic pathway. Proc Natl Acad Sci U S A 87:5832-5836.
56. Yeckel MF, Berger TW (1995) Monosynaptic excitation of hippocampal CA1 pyramidal cells by afferents from the entorhinal cortex. Hippocampus 5:108-114.
57. Zsiros V, Maccaferri G (2005) Electrical coupling between interneurons with different excitable properties in the stratum lacunosum-moleculare of the juvenile CA1 rat hippocampus. J Neurosci 25:8686-8695.
58. Zsiros V, Aradi I, Maccaferri G (2007) Propagation of postsynaptic currents and potentials via gap junctions in GABAergic networks of the rat hippocampus. J Physiol 578:527-544.