Cell type-specific and activity-dependent dynamics of action potential-evoked Ca2+ signals in dendrites of hippocampal inhibitory interneurons

Journal of Physiology

Volumn 589, Issue 8, 2011, Pages 1957-1977

  Evstratova, Alesya ^a   Chamberland, Simon ^a   Topolnik, Lisa ^a  

^a UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION;

ACTION POTENTIAL; AMPLITUDE MODULATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL TYPE; CONTROLLED STUDY; DENDRITE; HIPPOCAMPUS; HYPERPOLARIZATION; INTERNEURON; LONG TERM POTENTIATION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC INHIBITION; PRIORITY JOURNAL; SPIKE; SYNAPSE;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; CALCIUM SIGNALING; DENDRITES; ELECTRIC STIMULATION; FEEDBACK, PHYSIOLOGICAL; HIPPOCAMPUS; INHIBITORY POSTSYNAPTIC POTENTIALS; INTERNEURONS; KINETICS; MICE; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; NERVE NET; NEURAL INHIBITION; NEURAL PATHWAYS; NEURONAL PLASTICITY; PATCH-CLAMP TECHNIQUES; SYNAPTIC TRANSMISSION; THETA RHYTHM;

EID: 79954506572     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2010.204255     Document Type: Article

References (67)

1. A receptor-mediated unitary IPSPs by cannabinoid receptors at synapses between CCK-positive interneurons in rat hippocampus. J Neurophysiol 98, 861-869.
2. 2+ buffering in fast-spiking basket cells of rat hippocampus. J Physiol 586, 2061-2075.
3. Bragin A, Jandó G, Nádasdy Z, van Landeghem M & Buzsáki G (1995). Dentate EEG spikes and associated interneuronal population bursts in the hippocampal hilar region of the rat. J Neurophysiol 73, 1691-1705.
4. Bredt DS & Snyder SH (1990). Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc Natl Acad Sci U S A 87, 682-685.
5. Caillard O, Ben-Ari Y & Gaiarsa JL (1999). Long-term potentiation of GABAergic synaptic transmission in neonatal rat hippocampus. J Physiol 518, 109-119.
6. Callaway JC & Ross WN (1995). Frequency-dependent propagation of sodium action potentials in dendrites of hippocampal CA1 pyramidal neurons. J Neurophysiol 74, 1395-1403.
7. Carter AG & Sabatini BL (2004). State-dependent calcium signaling in dendritic spines of striatal medium spiny neurons. Neuron 44, 483-493.
8. Cope DW, Maccaferri G, Márton 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.
9. Csicsvari J, Hirase H, Czurko A & Buzsáki G (1998). Reliability and state dependence of pyramidal cell-interneuron synapses in the hippocampus: an ensemble approach in the behaving rat. Neuron 21, 179-189.
10. Daw MI, Tricoire L, Erdelyi F, Szabo G & McBain CJ (2009). Asynchronous transmitter release from cholecystokinin-containing inhibitory interneurons is widespread and target-cell independent. J Neurosci 29, 11112-11122.
11. Denk W, Sugimori M & Llinás R (1995). Two types of calcium response limited to single spines in cerebellar Purkinje cells. Proc Natl Acad Sci U S A 92, 8279-8282.
12. Egger V, Svoboda K & Mainen ZF (2003). Mechanisms of lateral inhibition in the olfactory bulb: efficiency and modulation of spike-evoked calcium influx into granule cells. J Neurosci 23, 7551-7558.
13. + channels control action potential backpropagation. J Physiol 551, 49-65.
14. Goldberg JH, Lacefield CO & Yuste R (2004). Global dendritic calcium spikes in mouse layer 5 low threshold spiking interneurones: implications for control of pyramidal cell bursting. J Physiol 558, 465-478.
15. Gulyas AI, Megias M, Emri Z & Freund TF (1999). Total number and ratio of excitatory and inhibitory synapses converging onto single interneurons of different types in the CA1 area of the rat hippocampus. J Neurosci 19, 10082-10097.
16. Hefft S & Jonas P (2005). Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron-principal neuron synapse. Nat Neurosci 8, 1319-1328.
17. 2+ signaling in dendrites of pyramidal neurons. Biophys J 70, 1069-1081.
18. Hu H, Martina M & Jonas P (2010). Dendritic mechanisms underlying rapid synaptic activation of fast-spiking hippocampal interneurons. Science 327, 52-58.
19. Huang L, Keyser BM, Tagmose TM, Hansen JB, Taylor JT, Zhuang H, Zhang M, Ragsdale DS & Li M (2004). NNC 55-0396 [(1S, 2S)-2-(2-(N-[(3-benzimidazol-2-yl)propyl]-N-methylamino)ethyl)-6-fluoro-1, 2, 3, 4-tetrahydro-1-isopropyl-2-naphtyl cyclopropanecarboxylate dihydrochloride]: a new selective inhibitor of T-type calcium channels. J Pharmacol Exp Ther 309, 193-199.
20. Jinno S & Kosaka T (2002). Patterns of expression of calcium binding proteins and neuronal nitric oxide synthase in different populations of hippocampal GABAergic neurons in mice. J Comp Neurol 449, 1-25.
21. Katona I, Sperlagh B, Sík A, Kafalvi A, Vizi ES, Mackie K & Freund TF (1999). Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci 19, 4544-4558.
22. 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.
23. Kerr AM, Reisinger E & Jonas P (2008). Differential dependence of phasic transmitter release on synaptotagmin 1 at GABAergic and glutamatergic hippocampal synapses. Proc Natl Acad Sci U S A 105, 15581-15586.
24. Klausberger T, Magill P, Márton LF, Roberts JD, Cobden PM, Buzsáki G & Somogyi P (2003). Brain-state- and Cell type-specific firing of hippocampal interneurons in vivo. Nature 421, 844-848.
25. Klausberger T, Marton LF, O'Neill J, Huck JHJ, Dalezios Y, Fuentealba P, Suen WY, Papp E, Kaneko T, Watanabe M, Csicsvari J & Somogyi P (2005). Complementary roles of cholecystokinin- and parvalbumin- expressing GABAergic neurons in hippocampal network oscillations. J Neurosci 25, 9782-9793.
26. Klausberger T (2009). GABAergic interneurons targeting dendrites of pyramidal cells in the CA1 area of the hippocampus. Eur J Neurosci 30, 947-957.
27. Kraushaar U & Jonas P (2000). Efficacy and stability of quantal GABA release at a hippocampal interneuron-principal neuron synapse. J Neurosci 20, 5594-5607.
28. Kuczewski N, Porcher C, Ferrand N, Fiorentino H, Pellegrino C, Kolarow R, Lessmann V, Medina I & Gaiarsa JL (2008). Backpropagating action potentials trigger dendritic release of BDNF during spontaneous network activity. J Neurosci 28, 7013-7023.
29. Lamsa KP, Heeroma JH & Kullmann DM (2005). Hebbian LTP in feed-forward inhibitory interneurons and the temporal fidelity of input discrimination. Nat Neurosci 8, 916-924.
30. 2+/calmodulin-dependent kinases. J Physiol 584, 885-894.
31. Lapointe V, Morin F, Ratte S, Croce A, Conquet F & Lacaille J-C (2004). Synapse-specific mGluR1-dependent long-term potentiation in interneurones regulates mouse hippocampal inhibition. J Physiol 15, 125-135.
32. 2+ buffering properties between excitatory and inhibitory hippocampal neurons from the rat. J Physiol 525, 405-418.
33. Lei S & McBain CJ (2002). Distinct NMDA receptors provide differential modes of transmission at mossy fiber-interneuron synapses. Neuron 33, 921-933.
34. Li M, Hansen JB, Huang L, Keyser BM & Taylor JT (2005). Towards selective antagonists of T-type calcium channels: design, characterization and potential applications of NNC 55-0396. Cardiovasc Drug Rev 23, 173-196.
35. Liu XB & Jones EG (1996). Localization of α type II calcium calmodulin-dependent protein kinase at glutamatergic but not γ-aminobutyric acid (GABAergic) synapses in thalamus and cerebral cortex. Proc Natl Acad Sci U S A 93, 7332-7336.
36. 2+ influx into the dendrites of hippocampal pyramidal neurons. J Neurophysiol 74, 1335-1342.
37. Maravall M, Mainen ZF, Sabatini BL & Svoboda K (2000). Estimating intracellular calcium concentrations and buffering without wavelength ratioing. Biophys J 78, 2655-2667.
38. Martina M, Vida I & Jonas P (2000). Distal initiation and active propagation of action potentials in interneuron dendrites. Science 287, 295-300.
39. McRory JE, Santi CM, Hamming KS, Mezeyova J, Sutton KG, Baillie DL, Stea A & Snutch TP (2001). Molecular and functional characterization of a family of rat brain T-type calcium channels. J Biol Chem 276, 3999-4011.
40. 2+ currents in dendritic recordings from Purkinje cells in rat cerebellar slice cultures. J Neurosci 17, 160-170.
41. 2+ microdomains in hippocampal neurons. J Neurosci 25, 558-565.
42. Neher E & Augustine GJ (1992). Calcium gradients and buffers in bovine chromaffin cells. J Physiol 450, 273-301.
43. Nugent FS, Penick EC & Kauer JA (2007). Opioids block long-term potentiation of inhibitory synapses. Nature 446, 1086-1090.
44. O'Keefe J & Recce ML (1993). Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3, 317-330.
45. Oliva C, Cohen IS & Mathias RT (1988). Calculation of time constants for intracellular diffusion in whole cell patch clamp configuration. Biophys J 54, 791-799.
46. Patenaude C, Massicotte G & Lacaille JC (2005). Cell-type specific GABA synaptic transmission and activity-dependent plasticity in rat hippocampal stratum radiatum interneurons. Eur J Neurosci 22, 179-188.
47. Pawelzik H, Hughes DI & Thomson AM (2002). Physiological and morphological diversity of immunocytochemically defined parvalbumin- and cholecystokini-positive interneurons in CA1 of the adult rat hippocampus. J Comp Neurol 443, 346-367.
48. Perez Y, Morin F & Lacaille JC (2001). A hebbian form of long-term potentiation dependent on mGluR1a in hippocampal inhibitory interneurons. Proc Natl Acad Sci U S A 98, 9401-9406.
49. Pettit DL & Augustine GJ (2000). Distribution of functional glutamate and GABA receptors on hippocampal pyramidal cells and interneurons. J Neurophysiol 84, 28-38.
50. Pusch M & Neher E (1988). Rates of diffusional exchange between small cells and a measuring patch pipette. Pflugers Arch 411, 204-211.
51. Rozsa B, Zelles T, Vizi ES & Lendvai B (2004). Distance-dependent scaling of calcium transients evoked by backpropagating spikes and synaptic activity in dendrites of hippocampal interneurons. J Neurosci 24, 661-670.
52. Sabatini B & Svoboda K (2000). Analysis of calcium channels in single spines using optical fluctuation analysis. Nature 408, 589-593.
53. 2+ ions in dendritic spines. Neuron 33, 439-452.
54. 2+ extrusion. J Neurosci 26, 8183-8194.
55. Pollock JS, Förstermann U, Mitchell JA, Warner TD, Schmidt HH, Nakane M & Murad F (1991). Purification and characterization of particulate endothelium-derived relaxing factor synthase from cultured and native bovine aortic endothelial cells. Proc Natl Acad Sci U S A 88, 10480-10484.
56. 2+ signaling pathway in GABAergic neurons of the hippocampus. Proc Natl Acad Sci U S A 95, 3245-3250.
57. Soltesz I & Deschênes M (1993). Low- and high-frequency membrane potential oscillations during theta activity in CA1 and CA3 pyramidal neurons of the rat hippocampus under ketamine-xylazine anesthesia. J Neurophysiol 70, 97-116.
58. 2+-sensor model for neurotransmitter release in a central synapse. Nature 450, 676-682.
59. 2+ signalling and long-term potentiation in rat hippocampal oriens/alveus interneurons. J Physiol 575, 115-131.
60. 2+ signaling in hippocampal interneurons. J Neurosci 29, 4658-4663.
61. 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.
62. Vinet J & Sík A (2006). Expression pattern of voltage-dependent calcium channel subunits in hippocampal inhibitory neurons in mice. Neuroscience 143, 189-212.
63. Woodruff ML, Sampath AP, Matthews HR, Krasnoperova NV, Lem J & Fain GL (2002). Measurement of cytoplasmic calcium concentration in the rods of wild-type and transducin knock-out mice. J Physiol 542, 843-854.
64. Yasuda R, Sabatini BL & Svoboda K (2003). Plasticity of calcium channels in dendritic spines. Nat Neurosci 6, 948-955.
65. Yasuda R, Nimchinsky EA, Scheuss V, Pologruto TA, Oertner TG, Sabatini BL & Svoboda K (2004). Imaging calcium concentration dynamics in small neuronal compartments. Sci STKE 219, l5.
66. Yuste R & Denk W (1995). Dendritic spines as basic functional units of neuronal integration. Nature 375, 682-684.
67. Zhou Z & Neher E (1993). Mobile and immobile calcium buffers in bovine adrenal chromaffin cells. J Physiol 469, 245-273.