Electrical coupling between interneurons with different excitable properties in the stratum lacunosum-moleculare of the juvenile CA1 rat hippocampus

Journal of Neuroscience

Volumn 25, Issue 38, 2005, Pages 8686-8695

  Zsiros, Veronika ^a   Maccaferri, Gianmaria ^a,b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Connexin; GABA; Gap junction; Hippocampus; Interneuron; Pannexin

Indexed keywords

4 AMINOBUTYRIC ACID; CARBENOXOLONE; GAP JUNCTION PROTEIN;

4 AMINOBUTYRIC ACID RELEASE; ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL SYNCHRONIZATION; CONTROLLED STUDY; COUPLING FACTOR; ELECTROSTIMULATION; EVOKED RESPONSE; HIPPOCAMPUS; INTERNEURON; MOLECULAR BIOLOGY; NERVE EXCITABILITY; NONHUMAN; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; RAT; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; AGE FACTORS; ANIMALS; ELECTROPHYSIOLOGY; HIPPOCAMPUS; INTERNEURONS; NERVE NET; RATS; RATS, SPRAGUE-DAWLEY;

EID: 25444521772     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2810-05.2005     Document Type: Article

References (66)

1. Aradi I, Maccaferri G (2004) Cell type-specific synaptic dynamics of synchronized bursting in the juvenile CA3 rat hippocampus. J Neurosci 24:9681-9692.
2. Bartos M, Vida I, Frotscher M, Geiger JR, Jonas P (2001) Rapid signaling at inhibitory synapses in a dentate gyrus interneuron network. J Neurosci 21:2687-2698.
3. Bartos M, Vida I, Frotscher M, Meyer A, Monyer H, Geiger JR, Jonas P (2002) Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks. Proc Natl Acad Sci USA 99:13222-13227.
4. Beierlein M, Gibson JR, Connors BW (2000) A network of electrically coupled interneurons drives synchronized inhibition in neocortex. Nat Neurosci 3:904-910.
5. Bennett VL, Zukin SR (2004) Electrical coupling and neuronal synchronization in the mammalian brain. Neuron 41:495-511.
6. Bertrand S, Lacaille JC (2001) Unitary synaptic currents between lacunosum-moleculare interneurones and pyramidal cells in rat hippocampus. J Physiol (Lond) 532:369-384.
7. Blatow M, Rozov A, Katona I, Hormuzdi SG, Meyer AH, Whittington MA, Caputi A, Monyer H (2003) A novel network of multipolar bursting interneurons generates theta frequency oscillations in neocortex. Neuron 38:805-817.
8. Buhl DL, Harris KD, Hormuzdi SG, Monyer H, Buzsaki G (2003) Selective impairment of hippocampal gamma oscillations in connexin-36 knock-out mouse in vivo. J Neurosci 23:1013-1018.
9. Cauli B, Tong XK, Rancillac A, Serluca N, Lambolez B, Rossier J, Hamel E (2004) Cortical GABA interneurons in neurovascular coupling: relays for subcortical vasoactive pathways. J Neurosci 24:8940-8949.
10. Chow CC, Kopell N (2000) Dynamics of spiking neurons with electrical coupling. Neural Comput 12:1643-1678.
11. Chu Z, Galarreta M, Hestrin S (2003) Synaptic interactions of late-spiking neocortical neurons in layer 1. J Neurosci 23:96-102.
12. Connors BW, Long MA (2004) Electrical synapses in the mammalian brain. Annu Rev Neurosci 27:393-418.
13. Cope DW, Maccaferri G, Marton LF, Roberts JD, Cobden PM, Somogyi P (2002) Cholecystokinin-immunopositive basket and Schaffer collateral-associated interneurons target different domains of pyramidal cells in the CA1 area of the rat hippocampus. Neuroscience 109:63-80.
14. Deans MR, Gibson JR, Sellitto C, Connors BW, Paul DL (2001) Synchronous activity of inhibitory networks in neocortex requires electrical synapses containing connexin 36. Neuron 31:477-485.
15. Empson RM, Heinemann U (1995) The perforant path projection to hippocampal area CA1 in the rat hippocampal-entorhinal cortex combined slice. J Physiol (Lond) 484:707-720.
16. Freund TF, Buzsaki G (1996) Interneurons of the hippocampus. Hippocampus 6:347-470.
17. Fukuda T, Kosaka T (2000) Gap Junctions linking the dendritic network of GABAergic interneurons in the hippocampus. J Neurosci 20:1519-1528.
18. Galarreta M, Hestrin S (1999) A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402:72-75.
19. Galarreta M, Hestrin S (2001) Electrical synapses between GABA-releasing interneurons. Nat Rev Neurosci 2:425-433.
20. Galarreta M, Hestrin S (2002) Electrical and chemical synapses among parvalbumin fast-spiking GABAergic interneurons in adult mouse neocortex. Proc Natl Acad Sci USA 99:12438-12443.
21. Galarreta M, Erdelyi F, Szabo G, Hestrin S (2004) Electrical coupling among irregular-spiking GABAergic interneuron expressing cannabinoid receptors. J Neurosci 24:9770-9778.
22. Gibson JR, Beierlein M, Connors BW (1999) Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402:75-79.
23. Gupta A, Wang Y, Markram H (2000) Organizing principles for a diversity of GABAergic interneruons and synapses in the neocortex. Science 287:273-278.
24. Hestrin S, Armstrong WE (1996) Morphology and physiology of cortical neurons in layer I. J Neurosci 16:5290-5300.
25. Hormuzdi SG, Pais I, LeBeau P, Towers SK, Rozov A, Buhl EH, Whittington MA, Monyer H (2001) Impaired electrical signaling disrupts frequency oscillations in connexin 36-deficient mice. Neuron 31:487-495.
26. Hormuzdi SG, Filippov MA, Mitropoulou G, Monyer H, Bruzzone R (2004) Electrical synapses: a dynamic signaling system that shapes the activity of neuronal networks. Biochim Biophys Acta 1662:113-137.
27. Joliffe IT (1986) Principal component analysis. New York: Springer.
28. Kawaguchi Y (1995) Physiological subgroups of nonpyramidal cells with specific morphological charachteristics in layer II/III of rat frontal cortex. J Neurosci 15:2638-2655.
29. Khazipov R, Congar P, Ben-Ari Y (1995) Hippocampal CA1 lacunosum-moleculare interneurons: comparison of effects of anoxia on excitatory and inhibitory postsynaptic currents. J Neurophysiol 74:2138-2149.
30. Kosaka T, Hama K (1985) Gap junctions between non-pyramidal cell dendrites in rat hippocampus (CA1 and CA3 regions): a combined Golgi-electron microscope study. J Comp Neurol 231:150-161.
31. Krimer LS, Zaitsev AV, Czanner G, Kroner S, Gonzales-Burgos G, Povysheva NV, Iyengar S, Barrionuevo G, Lewis DA (2005) Cluster analysis-based physiological classification and morphological properties of inhibitory neurons in layers 2-3 of monkey dorsolateral prefrontal cortex. J Neurophysiol, in press.
32. Kunkel DD, Lacaille JC, Schwartzkroin PA (1988) Ultrastructure of stratum lacunosum-moleculare interneurons of hippocampal CA1 region. Synapse 2:382-394.
33. Lacaille JC, Schwartzkroin PA (1988) Stratum lacunosum-moleculare interneurons of hippocampal CA1 region. II. Intrasomatic and intradendritic recordings of local circuit synaptic interactions. J Neurosci 8:1411-1424.
34. Lewis TJ, Rinzel J (2003) Dynamics of spiking neurons connected by both inhibitory and electrical coupling. J Comput Neurosci 14:283-309.
35. Losonczy A, Somogyi P, Nusser Z (2003) Reduction of excitatory postsynaptic responses by persistently active metabotropic glutamate receptors in the hippocampus. J Neurophysiol 89:1910-1919.
36. Losonczy A, Biro AA, Nusser Z (2004) Persistently active cannabinoid receptors mute a subpopulation of hippocampal interneurons. Proc Natl Acad Sci USA 101:1362-1367.
37. Maccaferri G (2005) Stratum oriens horizontal interneurone diversity and hippocampal network dynamics. J Physiol (Lond) 562:73-80.
38. Maccaferri G, Dingledine R (2002) Control of feedforward dendritic inhibition by NMDA recptor-dependent spike timing in hippocampal interneurons. J Neurosci 22:5462-5472.
39. Maccaferri G, Lacaille JC (2003) Interneuron diversity series: hippocampal classifications-making things as simple as possible, not simpler. Trends Neurosci 26:564-571.
40. Maccaferri G, Roberts JDB, Szucs P, Cottingham C, Somogyi P (2000) Cell surface domain specific postsynaptic currents evoked by identified GABAergic neurones in rat hippocampus in vitro. J Physiol (Lond) 524:91-116.
41. Maier N, Guldenagel M, Sohl G, Siegmund H, Willecke K, Draguhn A (2002) Reduction of high-frequency network oscillations (ripples) and pathological network discharges in hippocampal slices from connexin 36-deficient mice. J Physiol (Lond) 541:521-528.
42. Mainen ZF, Sejnowski TJ (1996) Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382:363-366.
43. Meyer AH, Katona I, Blatow M, Rozov A, Monyer H (2002) in vivo labeling of parvalbumin-positive interneurons and analysis of electrical coupling in identified neurons. J Neurosci 22:7055-7064.
44. Morin F, Beaulieu C, Lacaille JC (1996) Membrane properties and synaptic currents evoked in CA1 interneuron subtypes in rat hippocampal slices. J Neurophysiol 76:1-16.
45. Mott DD, Turner DA, Okazaki MM, Lewis DV (1997) Interneurons of the dentate-hilus border of the rat dentate gyrus: morphological and electrophysiological heterogeneity. J Neurosci 17:3990-4005.
46. Neher E (1992) Correction for liquid junction potentials in patch clamp experiments. Methods Enzymol 207:123-131.
47. Pais I, Hormuzdi SG, Monyer H, Traub RD, Wood IC, Buhl EH, Whittington MA, LeBeau FE (2003) Sharp wave-like activity in the hippocampus in vitro in mice lacking the gap junction protein connexin 36. J Neurophysiol 89:2046-2054.
48. Parra P, Gulyas AI, Miles R (1998) How many subtypes of inhibitory cells in the hippocampus? Neuron 20:983-993.
49. Perez-Velazquez JL, Carlen PL, Skinner FK (2001) Artificial electro tonic coupling affects neuronal firing patterns depending upon cellular characteristics. Neuroscience 103:841-849.
50. Pfeuty B, Mato G, Golomb D, Hansel D (2003) Electrical synapses and synchrony: the role of intrinsic currents. J Neurosci 23:6280-6294.
51. 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.
52. Remondes M, Schuman EM (2002) Direct cortical input modulates plasticity and spiking in CA1 pyramidal neurons. Nature 416:736-740.
53. Remondes M, Schuman EM (2004) Role for a cortical input to the hippocampal area CA1 in the consolidation of a long-term memory. Nature 431:699-703.
54. Sherman A, Rinzel J (1992) Rhythmogenic effects of weak electrotonic coupling in neuronal models. Proc Natl Acad Sci USA 89:2471-2474.
55. Simon A, Szabolcs O, Molnar G, Szabadics J, Tamas G (2005) Gap-junctional coupling between neurogliaform cells and various interneuron types in the neocortex. J Neurosci 25:6278-6285.
56. Steward O, Scoville SA (1976) Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J Comp Neurol 169:347-370.
57. Szabadics J, Lorincz A, Tamas G (2001) β and γ frequency synchronization by dendritic GABAergic synapses and gap junctions in a network of cortical interneurons. J Neurosci 21:5824-5831.
58. Tamas G, Lorincz A, Simon A, Szabadics J (2003) Identified sources and targets of slow inhibition in the neocortex. Science 299:1902-1905.
59. Venance L, Rozov A, Blatow M, Burnashev N, Feldmayer D, Monyer H (2000) Connexin expression in electrically coupled postnatal rat brain neurons. Proc Natl Acad Sci USA 97:10260-10265.
60. Vida I, Halasy K, Szinyei C, Somogyi P, Buhl EH (1998) Unitary IPSPs evoked by interneurons at stratum radiatum-stratum lacunosum-moleculare border in the CA1 area of the rat hippocampus in vitro. J Physiol (Lond) 506:755-773.
61. Whittington MA, Traub RD (2003) Interneuron diversity series: inhibitory interneurons and network oscillations in vitro. Trends Neurosci 26:676-682.
62. 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 Neurophys 71:2217-2235.
63. Wouterlood FG, Saldana E, Witter MP (1990) Projections from the nucleus reunions thalami to the hippocampal region: light and electron microscopic tracing study in the rat with the anterograde tracer Phaeolus vulgaris-leucoagglutinin. J Comp Neurol 296:179-203.
64. Yamamoto T, Shiosaka S, Whittaker ME, Hertzberg EL, Nagy JI (1989) Gap junction protein in rat hippocampus: light microscope immunohistochemical localization. J Comp Neurol 281:282-297.
65. Yukie M, Iwai E (1988) Direct projections from the ventral TE area of the inferotemporal cortex to the hippocampal field CA1 in the monkey. Neurosci Lett 88:6-10.
66. Zhang XL, Zhang L, Carlen PL (2004) Electrotonic coupling between stratum oriens interneurones in the intact in vitro mouse juvenile hippocampus. J Physiol (Lond) 558:825-839.