Metabotropic glutamate receptors regulate hippocampal CA1 pyramidal neuron excitability via Ca 2+ wave-dependent activation of SK and TRPC channels

Journal of Physiology

Volumn 589, Issue 13, 2011, Pages 3211-3229

  El Hassar, Lynda ^a   Hagenston, Anna M ^a   D'Angelo, Lisa Bertetto ^a   Yeckel, Mark F ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; CALCIUM ION; CYCLIC AMP; METABOTROPIC RECEPTOR; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR 4; METABOTROPIC RECEPTOR 5; SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTISM; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FLUORESCENCE IMAGING; HIPPOCAMPAL CA1 REGION; HYPERPOLARIZATION; MENTAL DEFICIENCY; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ANIMALS; CA1 REGION, HIPPOCAMPAL; CALCIUM SIGNALING; MALE; NEURONS; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, METABOTROPIC GLUTAMATE; SMALL-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; TRPC CATION CHANNELS;

EID: 79959742217     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2011.209783     Document Type: Article

References (97)

1. BDNF, a nonselective cationic current mediated by TRPC channels. J Neurophysiol 98, 2476-2482.
2. Amaral MD & Pozzo-Miller L (2007b). TRPC3 channels are necessary for brain-derived neurotrophic factor to activate a nonselective cationic current and to induce dendritic spine formation. J Neurosci 27, 5179-5189.
3. Anwyl R (2009). Metabotropic glutamate receptor-dependent long-term potentiation. Neuropharmacology 56, 735-740.
4. Axmacher N, Elger CE & Fell J (2008). Ripples in the medial temporal lobe are relevant for human memory consolidation. Brain 131, 1806-1817.
5. Baude A, Nusser Z, Roberts JD, Mulvihill E, McIlhinney RA & Somogyi P (1993). The metabotropic glutamate receptor (mGluR1α) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11, 771-787.
6. Berger TW, Alger B & Thompson RF (1976). Neuronal substrate of classical conditioning in the hippocampus. Science 192, 483-485.
7. Berridge MJ (1998). Neuronal calcium signalling. Neuron 21, 13-26.
8. Berridge MJ, Bootman MD & Lipp P (1998). Calcium - a life and death signal. Nature 395, 645-648.
9. Blair NT, Kaczmarek JS & Clapham DE (2009). Intracellular calcium strongly potentiates agonist-activated TRPC5 channels. J Gen Physiol 133, 525-546.
10. Blumenthal EM & Kaczmarek LK (1992). Modulation by cAMP of a slowly activating potassium channel expressed in Xenopus oocytes. J Neurosci 12, 290-296.
11. Blumenthal EM & Kaczmarek LK (1994). The minK potassium channel exists in functional and nonfunctional forms when expressed in the plasma membrane of Xenopus oocytes. J Neurosci 14, 3097-3105.
12. Boulay G, Zhu X, Peyton M, Jiang M, Hurst R, Stefani E & Birnbaumer L (1997). Cloning and expression of a novel mammalian homolog of Drosophila transient receptor potential (Trp) involved in calcium entry secondary to activation of receptors coupled by the Gq class of G protein. J Biol Chem 272, 29672-29680.
13. Buzsaki G, Horvath Z, Urioste R, Hetke J & Wise K (1992). High-frequency network oscillation in the hippocampus. Science 256, 1025-1027.
14. Camperi M & Wang XJ (1998). A model of visuospatial working memory in prefrontal cortex: recurrent network and cellular bistability. J Comput Neurosci 5, 383-405.
15. Chrobak JJ & Buzsaki G (1994). Selective activation of deep layer (V-VI) retrohippocampal cortical neurons during hippocampal sharp waves in the behaving rat. J Neurosci 14, 6160-6170.
16. Chuang SC, Bianchi R, Kim D, Shin HS & Wong RK (2001). Group I metabotropic glutamate receptors elicit epileptiform discharges in the hippocampus through PLCβ1 signalling. J Neurosci 21, 6387-6394.
17. Chung YH, Sun Ahn H, Kim D, Hoon Shin D, Su Kim S, Yong Kim K, Bok Lee W & Ik Cha C (2006). Immunohistochemical study on the distribution of TRPC channels in the rat hippocampus. Brain Res 1085, 132-137.
18. Congar P, Leinekugel X, Ben-Ari Y & Crepel V (1997). A long-lasting calcium-activated nonselective cationic current is generated by synaptic stimulation or exogenous activation of group I metabotropic glutamate receptors in CA1 pyramidal neurons. J Neurosci 17, 5366-5379.
19. Conquet F, Bashir ZI, Davies CH, Daniel H, Ferraguti F, Bordi F et al (1994). Motor deficit and impairment of synaptic plasticity in mice lacking mGluR1. Nature 372, 237-243.
20. 2+-activated nonspecific cationic current in CA1 hippocampal neurons. J Neurophysiol 72, 1561-1569.
21. Csicsvari J, Hirase H, Mamiya A & Buzsaki G (2000). Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events. Neuron 28, 585-594.
22. Csicsvari J, O'Neill J, Allen K & Senior T (2007). Place-selective firing contributes to the reverse-order reactivation of CA1 pyramidal cells during sharp waves in open-field exploration. Eur J Neurosci 26, 704-716.
23. Disterhoft JF, Coulter DA & Alkon DL (1986). Conditioning-specific membrane changes of rabbit hippocampal neurons measured in vitro. Proc Natl Acad Sci U S A 83, 2733-2737.
24. Dolen G & Bear MF (2008). Role for metabotropic glutamate receptor 5 (mGluR5) in the pathogenesis of fragile X syndrome. J Physiol 586, 1503-1508.
25. Dolen G, Osterweil E, Rao BS, Smith GB, Auerbach BD, Chattarji S & Bear MF (2007). Correction of fragile X syndrome in mice. Neuron 56, 955-962.
26. Egorov AV, Hamam BN, Fransen E, Hasselmo ME & Alonso AA (2002). Graded persistent activity in entorhinal cortex neurons. Nature 420, 173-178.
27. Faber ES, Sedlak P, Vidovic M & Sah P (2006). Synaptic activation of transient receptor potential channels by metabotropic glutamate receptors in the lateral amygdala. Neuroscience 137, 781-794.
28. 2 metabolism and KCNQ2/3 channel regulation studied with a voltage-sensitive phosphatase in living cells. J Gen Physiol 135, 99-114.
29. Finch EA & Augustine GJ (1998). Local calcium signalling by inositol-1, 4, 5-trisphosphate in Purkinje cell dendrites. Nature 396, 753-756.
30. 2+ waves in pyramidal neuron dendrites propagate through hot spots and cold spots. J Physiol 587, 1439-1459.
31. Fowler MA, Sidiropoulou K, Ozkan ED, Phillips CW & Cooper DC (2007). Corticolimbic expression of TRPC4 and TRPC5 channels in the rodent brain. PLoS One 2, e573.
32. Gee CE, Benquet P & Gerber U (2003). Group I metabotropic glutamate receptors activate a calcium-sensitive transient receptor potential-like conductance in rat hippocampus. J Physiol 546, 655-664.
33. Gil-Sanz C, Delgado-Garcia JM, Fairen A & Gruart A (2008). Involvement of the mGluR1 receptor in hippocampal synaptic plasticity and associative learning in behaving mice. Cereb Cortex 18, 1653-1663.
34. Gipson KE & Yeckel MF (2007). Coincident glutamatergic and cholinergic inputs transiently depress glutamate release at rat schaffer collateral synapses. J Neurophysiol 97, 4108-4119.
35. Goel M, Sinkins WG & Schilling WP (2002). Selective association of TRPC channel subunits in rat brain synaptosomes. J Biol Chem 277, 48303-48310.
36. Gulledge AT & Kawaguchi Y (2007). Phasic cholinergic signalling in the hippocampus: functional homology with the neocortex? Hippocampus 17, 327-332.
37. Gulledge AT & Stuart GJ (2005). Cholinergic inhibition of neocortical pyramidal neurons. J Neurosci 25, 10308-10320.
38. Hagenston AM, Fitzpatrick JS & Yeckel MF (2008). MGluR-mediated calcium waves that invade the soma regulate firing in layer V medial prefrontal cortical pyramidal neurons. Cereb Cortex 18, 407-423.
39. Hagenston AM, Rudnick ND, Boone CE & Yeckel MF (2009). 2-Aminoethoxydiphenyl-borate (2-APB) increases excitability in pyramidal neurons. Cell Calcium 45, 310-317.
40. Haj-Dahmane S & Andrade R (1999). Muscarinic receptors regulate two different calcium-dependent non-selective cation currents in rat prefrontal cortex. Eur J Neurosci 11, 1973-1980.
41. Hardie RC (2003). Regulation of TRP channels via lipid second messengers. Annu Rev Physiol 65, 735-759.
42. Hayashi K, Yoshihara T & Ichitani Y (2007). Involvement of hippocampal metabotropic glutamate receptors in radial maze performance. Neuroreport 18, 719-723.
43. Hertle DN & Yeckel MF (2007). Distribution of inositol-1, 4, 5-trisphosphate receptor isotypes and ryanodine receptor isotypes during maturation of the rat hippocampus. Neuroscience 150, 625-638.
44. Hofmann T, Obukhov AG, Schaefer M, Harteneck C, Gudermann T & Schultz G (1999). Direct activation of human TRPC6 and TRPC3 channels by diacylglycerol. Nature 397, 259-263.
45. Hofmann T, Schaefer M, Schultz G & Gudermann T (2002). Subunit composition of mammalian transient receptor potential channels in living cells. Proc Natl Acad Sci U S A 99, 7461-7466.
46. Hong M & Ross WN (2007). Priming of intracellular calcium stores in rat CA1 pyramidal neurons. J Physiol 584, 75-87.
47. Huber KM, Kayser MS & Bear MF (2000). Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288, 1254-1257.
48. Jaffe DB & Brown TH (1994). Metabotropic glutamate receptor activation induces calcium waves within hippocampal dendrites. J Neurophysiol 72, 471-474.
49. 2+ release in CA3 pyramidal neurons via a metabotropic glutamate receptor pathway. Neuroscience 107, 59-69.
50. Kelliher M, Fastbom J, Cowburn RF, Bonkale W, Ohm TG, Ravid R, Sorrentino V & O'Neill C (1999). Alterations in the ryanodine receptor calcium release channel correlate with Alzheimer's disease neurofibrillary and β-amyloid pathologies. Neuroscience 92, 499-513.
51. + currents and spike-frequency adaptation in medial entorhinal cortex layer II stellate cells. Hippocampus 17, 1143-1148.
52. Kim SJ, Kim YS, Yuan JP, Petralia RS, Worley PF & Linden DJ (2003). Activation of the TRPC1 cation channel by metabotropic glutamate receptor mGluR1. Nature 426, 285-291.
53. Kleppisch T, Voigt V, Allmann R & Offermanns S (2001). Gαq-deficient mice lack metabotropic glutamate receptor-dependent long-term depression but show normal long-term potentiation in the hippocampal CA1 region. J Neurosci 21, 4943-4948.
54. Lee AC, Wong RK, Chuang SC, Shin HS & Bianchi R (2002). Role of synaptic metabotropic glutamate receptors in epileptiform discharges in hippocampal slices. J Neurophysiol 88, 1625-1633.
55. Lee YM, Kim BJ, Kim HJ, Yang DK, Zhu MH, Lee KP, So I & Kim KW (2003). TRPC5 as a candidate for the nonselective cation channel activated by muscarinic stimulation in murine stomach. Am J Physiol Gastrointest Liver Physiol 284, G604-G616.
56. 2+-sensitive cation channels. J Biol Chem 275, 27799-27805.
57. Lujan R, Nusser Z, Roberts JD, Shigemoto R & Somogyi P (1996). Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus. Eur J Neurosci 8, 1488-1500.
58. Madison DV & Nicoll RA (1986). Actions of noradrenaline recorded intracellularly in rat hippocampal CA1 pyramidal neurones, in vitro. J Physiol 372, 221-244.
59. Marder E, Abbott LF, Turrigiano GG, Liu Z & Golowasch J (1996). Memory from the dynamics of intrinsic membrane currents. Proc Natl Acad Sci U S A 93, 13481-13486.
60. Merlin LR & Wong RK (1997). Role of group I metabotropic glutamate receptors in the patterning of epileptiform activities in vitro. J Neurophysiol 78, 539-544.
61. Morikawa H, Imani F, Khodakhah K & Williams JT (2000). Inositol 1, 4, 5-triphosphate-evoked responses in midbrain dopamine neurons. J Neurosci 20, RC103.
62. Naie K & Manahan-Vaughan D (2004). Regulation by metabotropic glutamate receptor 5 of LTP in the dentate gyrus of freely moving rats: relevance for learning and memory formation. Cereb Cortex 14, 189-198.
63. 2+ from IP3-sensitive stores evoked by synaptic activation of mGluRs paired with backpropagating action potentials. Neuron 24, 727-737.
64. Niswender CM & Conn PJ (2010). Metabotropic glutamate receptors: physiology, pharmacology, and disease. Annu Rev Pharmacol Toxicol 50, 295-322.
65. 2+ increase in isolated frog taste cells. Eur J Neurosci 10, 1376-1382.
66. O'Neill J, Senior T & Csicsvari J (2006). Place-selective firing of CA1 pyramidal cells during sharp wave/ripple network patterns in exploratory behaviour. Neuron 49, 143-155.
67. Parekh AB & Putney JW Jr (2005). Store-operated calcium channels. Physiol Rev 85, 757-810.
68. Partridge LD, Swandulla D & Muller TH (1990). Modulation of calcium-activated non-specific cation currents by cyclic AMP-dependent phosphorylation in neurones of Helix. J Physiol 429, 131-145.
69. Partridge LD & Valenzuela CF (2000). Block of hippocampal CAN channels by flufenamate. Brain Res 867, 143-148.
70. + current underlying the slow spike frequency adaptation in hippocampal neurons. Neuron 11, 1023-1035.
71. Power JM & Sah P (2002). Nuclear calcium signalling evoked by cholinergic stimulation in hippocampal CA1 pyramidal neurons. J Neurosci 22, 3454-3462.
72. Ramsey IS, Delling M & Clapham DE (2006). An introduction to TRP channels. Annu Rev Physiol 68, 619-647.
73. Raymond CR, Thompson VL, Tate WP & Abraham WC (2000). Metabotropic glutamate receptors trigger homosynaptic protein synthesis to prolong long-term potentiation. J Neurosci 20, 969-976.
74. Rutecki PA, Sayin U, Yang Y & Hadar E (2002). Determinants of ictal epileptiform patterns in the hippocampal slice. Epilepsia 43, 179-183.
75. 2+-permeable channels in animal cells. In Handbook of Experimental Pharmacology, vol. 179, part I, pp. 23-52. Springer.
76. Ryu SH, Kim UH, Wahl MI, Brown AB, Carpenter G, Huang KP & Rhee SG (1990). Feedback regulation of phospholipase C-β by protein kinase C. J Biol Chem 265, 17941-17945.
77. + channels in rat brain. J Neurosci 22, 9698-9707.
78. Sandler VM & Barbara JG (1999). Calcium-induced calcium release contributes to action potential-evoked calcium transients in hippocampal CA1 pyramidal neurons. J Neurosci 19, 4325-4336.
79. 2+-ATPase of sarcoplasmic reticulum. J Biol Chem 264, 17816-17823.
80. Strubing C, Krapivinsky G, Krapivinsky L & Clapham DE (2001). TRPC1 and TRPC5 form a novel cation channel in mammalian brain. Neuron 29, 645-655.
81. Stutzmann GE (2005). Calcium dysregulation, IP3 signalling, and Alzheimer's disease. Neuroscientist 11, 110-115.
82. 2+ signalling in mouse cortical neurons studied by two-photon imaging and photoreleased inositol triphosphate. J Neurosci 23, 758-765.
83. Suh BC, Horowitz LF, Hirdes W, Mackie K & Hille B (2004). Regulation of KCNQ2/KCNQ3 current by G protein cycling: the kinetics of receptor-mediated signalling by Gq. J Gen Physiol 123, 663-683.
84. Thuault SJ, Davies CH, Randall AD & Collingridge GL (2002). Group I mGluRs modulate the pattern of non-synaptic epileptiform activity in the hippocampus. Neuropharmacology 43, 141-146.
85. Vatanparast J, Janahmadi M & Asgari AR (2007). Forskolin potentiates the paraoxon-induced hyperexcitability in snail neurons by blocking afterhyperpolarization. Neurotoxicology 28, 1178-1183.
86. Wang XJ (2001). Synaptic reverberation underlying mnemonic persistent activity. Trends Neurosci 24, 455-463.
87. Watanabe S, Hong M, Lasser-Ross N & Ross WN (2006). Modulation of calcium wave propagation in the dendrites and to the soma of rat hippocampal pyramidal neurons. J Physiol 575, 455-468.
88. Wyart C, Cocco S, Bourdieu L, Leger JF, Herr C & Chatenay D (2005). Dynamics of excitatory synaptic components in sustained firing at low rates. J Neurophysiol 93, 3370-3380.
89. 2+ release in a feedback regulation of pyramidal cell excitability. J Neurophysiol 91, 2322-2329.
90. Yan HD, Villalobos C & Andrade R (2009). TRPC channels mediate a muscarinic receptor-induced afterdepolarization in cerebral cortex. J Neurosci 29, 10038-10046.
91. Yeckel MF, Kapur A & Johnston D (1999). Multiple forms of LTP in hippocampal CA3 neurons use a common postsynaptic mechanism. Nat Neurosci 2, 625-633.
92. Yeckel MF, Sleeper AA, Fitzpatrick JS, Hertle D, Hagenston AM & Garner RT (2008). Intracellular calcium waves transmit synaptic information to the nucleus in hippocampal pyramidal neurons. In Transcirptional Regulation By Neuronal Activity, ed. Dudek SM, pp. 73-89. Springer Science Publishing.
93. Yoshida M, Fransen E & Hasselmo ME (2008). mGluR-dependent persistent firing in entorhinal cortex layer III neurons. Eur J Neurosci 28, 1116-1126.
94. Yue C, Ku CY, Liu M, Simon MI & Sanborn BM (2000). Molecular mechanism of the inhibition of phospholipase C β3 by protein kinase C. J Biol Chem 275, 30220-30225.
95. Zhang C, Roepke TA, Kelly MJ & Ronnekleiv OK (2008). Kisspeptin depolarizes gonadotropin-releasing hormone neurons through activation of TRPC-like cationic channels. J Neurosci 28, 4423-4434.
96. Zho WM, You JL, Huang CC & Hsu KS (2002). The group I metabotropic glutamate receptor agonist (S)-3, 5-dihydroxyphenylglycine induces a novel form of depotentiation in the CA1 region of the hippocampus. J Neurosci 22, 8838-8849.
97. Zhou FW, Matta SG & Zhou FM (2008). Constitutively active TRPC3 channels regulate basal ganglia output neurons. J Neurosci 28, 473-482.