Plasticity of intrinsic excitability during long-term depression is mediated through mGluR-dependent changes in Ih in hippocampal CA1 pyramidal neurons

Journal of Neuroscience

Volumn 27, Issue 51, 2007, Pages 13926-13937

  Brager, Darrin H ^a   Johnston, Daniel ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

DHPG; H channels; LTD; Metabotropic; PKC; Rat

Indexed keywords

2 [1 (3 DIMETHYLAMINOPROPYL) 3 INDOLYL] 3 (3 INDOLYL)MALEIMIDE; 2 AMINO 2 (2 CARBOXYCYCLOPROPYL) 3 (XANTHEN 9 YL)PROPIONIC ACID; 3,5 DIHYDROXYPHENYLGLYCINE; 4 (N ETHYL N PHENYLAMINO) 1,2 DIMETHYL 6 (METHYLAMINO)PYRIMIDINIUM CHLORIDE; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; CALCIUM; DIZOCILPINE; GLUTAMATE RECEPTOR AGONIST; METABOTROPIC RECEPTOR; PROTEIN KINASE C; CYCLIC NUCLEOTIDE GATED CHANNEL; HYPERPOLARIZATION ACTIVATED CATION CHANNEL; HYPERPOLARIZATION-ACTIVATED CATION CHANNEL; POTASSIUM CHANNEL; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BACK PROPAGATION; CALCIUM CELL LEVEL; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; LEARNING; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; RECEPTOR UPREGULATION; STATISTICAL ANALYSIS; TEMPORAL SUMMATION; ACTION POTENTIAL; ANIMAL; COMPARATIVE STUDY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ACTION POTENTIALS; ANIMALS; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; HIPPOCAMPUS; LONG-TERM SYNAPTIC DEPRESSION; MALE; NEURONAL PLASTICITY; POTASSIUM CHANNELS; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, METABOTROPIC GLUTAMATE;

EID: 37049034282     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3520-07.2007     Document Type: Article

References (63)

1. Abbott LF, Nelson SB (2000) Synaptic plasticity: taming the beast. Nat Neurosci 3 [Suppl]:1178-1183.
2. 2+ signal transduction. J Biol Chem 267:13361-13368.
3. Abraham WC, Gustafsson B, Wigström H (1987) Long-term potentiation involves enhanced synaptic excitation relative to synaptic inhibition in guinea-pig hippocampus. J Physiol (Lond) 394:367-380.
4. Abraham WC, Mason-Parker SE, Bear MF, Webb S, Tate WP (2001) Heterosynaptic metaplasticity in the hippocampus in vivo: a BCM-like modifiable threshold for LTP. Proc Natl Acad Sci USA 98:10924-10929.
5. Aizenman CD, Linden DJ (2000) Rapid, synaptically driven increases in the intrinsic excitability of cerebellar deep nuclear neurons. Nat Neurosci 3:109-111.
6. Aponte Y, Lien CC, Reisinger E, Jonas P (2006) Hyperpolarization- activated cation channels in fast-spiking interneurons of rat hippocampus. J Physiol (Lond) 574:229-243.
7. Aramori I, Nakanishi S (1992) Signal transduction and pharmacological characteristics of a metabotropic glutamate receptor, mGluR1, in transfected CHO cells. Neuron 8:757-765.
8. Bear MF (1996) A synaptic basis for memory storage in the cerebral cortex. Proc Natl Acad Sci USA 93:13453-13459.
9. Bear MF, Malenka RC (1994) Synaptic plasticity: LTP and LTD. Curr Opin Neurobiol 4:389-399.
10. Bliss TVP, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
11. Bolshakov VY, Siegelbaum SA (1994) Postsynaptic induction and presynaptic expression of hippocampal long-term depression. Science 264:1148-1152.
12. Brager DH, Capogna M, Thompson SM (2002) Short-term synaptic plasticity, simulation of nerve terminal dynamics, and the effects of protein kinase C activation in rat hippocampus. J Physiol (Lond) 541:545-559.
13. Cathala L, Paupardin-Tritsch D (1997) Neurotensin inhibition of the hyperpolarization-activated cation current (Ih) in the rat substantia nigra pars compacta implicates the protein kinase C pathway. J Physiol (Lond) 503:87-97.
14. Charpak S, Gähwiler BH, Do KQ, Köpfel T (1990) Potassium conductances in hippocampal neurons blocked by excitatory amino-acid transmitters. Nature 347:765-767.
15. Chavez-Noriega LE, Bliss TV, Halliwell JV (1989) The EPSP-spike (E-S) component of long-term potentiation in the rat hippocampal slice is modulated by GABAergic but not cholinergic mechanisms. Neurosci Lett 104:58-64.
16. Chen X, Johnston D (2004) Properties of single voltage-dependent K+ channels in dendrites of CA1 pyramidal neurones of rat hippocampus. J Physiol (Lond) 559:187-203.
17. Chevaleyre V, Castillo PE (2002) Assessing the role of Ih channels in synaptic transmission and mossy fiber LTP. Proc Natl Acad Sci USA 99:9538-9543.
18. 2+ influx in the induction of homosynaptic long-term depression in hippocampal CA1 pyramidal neurons. Learn Mem 3:160-169.
19. Cudmore RH, Turrigiano GG (2004) Long-term potentiation of intrinsic excitability in LV visual cortical neurons. J Neurophysiol 92:341-348.
20. Desai MA, Conn PJ (1991) Excitatory effects of ACPD receptor activation in the hippocampus are mediated by direct effects on pyramidal cells and blockade of synaptic inhibition. J Neurophysiol 66:40-52.
21. Desai NS, Rutherford LC, Turrigiano GG (1999) Plasticity in the intrinsic excitability of cortical pyramidal neurons. Nat Neurosci 2:515-520.
22. DiFransesco D (1993) Pacemaker mechanisms in cardiac tissue. Annu Rev Physiol 55:455-472.
23. Dudek SM, Bear MF (1992) Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci USA 89:4363-4367.
24. Fan Y, Fricker D, Brager DH, Chen X, Lu HC, Chitwood RA, Johnston D (2005) Activity-dependent decrease of excitability in rat hippocampal neurons through increases in I(h). Nat Neurosci 8:1542-1551.
25. Frick A, Johnston D (2005) Plasticity of dendritic excitability. J Neurobiol 64:100-115.
26. Frick A, Magee J, Johnston D (2004) LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nat Neurosci 7:126-135.
27. h) blocker ZD 7288 in hippocampal CA1 neurons. Pflügers Arch 435:99-106.
28. Gereau RW, Conn PJ (1995) Roles of specific metabotropic glutamate receptor subtypes in regulation of hippocampal CA1 pyramidal cell excitability. J Neurophysiol 74:122-129.
29. Golowasch J, Abbott LF, Marder E (1999) Activity-dependent regulation of potassium currents in an identified neuron of the stomatogastric ganglion of the crab Cancer borealis. J Neurosci 19:RC33.
30. Hess G, Gustafsson B (1990) Changes in field excitatory postsynaptic potential shape induced by tetanization in the CA1 region of the guinea-pig hippocampal slice. Neuroscience 37:61-69.
31. Huber KM, Kayser MS, Bear MF (2000) Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288:1254-1257.
32. Huber KM, Gallagher SM, Warren ST, Bear MF (2002) Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proc Natl Acad Sci USA 99:7746-7750.
33. Hutcheon B, Yarom Y (2000) Resonance, oscillation and the intrinsic frequency preferences of neurons. Trends Neurosci 23:216-222.
34. Hutcheon B, Miura RM, Puil E (1996) Subthreshold membrane resonance in neocortical neurons. J Neurophysiol 76:683-697.
35. Kaczorowski CC, Disterhoft J, Spruston N (2007) Stability and plasticity of intrinsic membrane properties in hippocampal CA1 pyramidal neurons: effects of internal anions. J Physiol (Lond) 578:799-818.
36. Kim J, Jung SC, Clemens AM, Petralia RS, Hoffman DA (2007) Regulation of dendritic excitability by activity-dependent trafficking of the A-type K+ channel subunit Kv4.2 in hippocampal neurons. Neuron 54:933-947.
37. Kole MH, Hallermann S, Stuart GJ (2006) Single Ih channels in pyramidal neuron dendrites: properties, distribution, and impact on action potential output. J Neurosci 26:1677-1687.
38. Luján R, Roberts JD, Shigemoto R, Ohishi H, Somogyi P (1997) Differential plasma membrane distribution of metabotropic glutamate receptors mGluR1 alpha, mGluR2 and mGluR5, relative to neurotransmitter release sites. J Chem Neuroanat 13:219-241.
39. Lüthi A, Bal T, McCormick DA (1998) Periodicity of thalamic spindle waves is abolished by ZD7288, a blocker of Ih. J Neurophysiol 79:3284-3289.
40. Maccaferri G, McBain CJ (1996) The hyperpolarization-activated current (Ih) and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens-alveus interneurones. J Physiol (Lond) 497:119-130.
41. Magee JC (1998) Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci 18:7613-7624.
42. Magee JC (1999) Dendritic lh normalizes temporal summation in hippocampal CA1 neurons. Nat Neurosci 2:508-514.
43. 2+ channels in apical dendrites of rat CA1 pyramidal neurons. J Physiol (Lond) 487:67-90.
44. Magee JC, Johnston D (1997) A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275:209-213.
45. Malenka RC, Bear MF (2004) LTP and LTD: an embarrassment of riches. Neuron 44:5-21.
46. 2+. Nature 325:156-159.
47. Mulkey RM, Malenka RC (1992) Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron 9 (5):967-975.
48. Narayanan R, Johnston D (2007) Long-term potentiation in rat hippocampal neurons is accompanied by spatially widespread changes in intrinsic oscillatory dynamics and excitability. Neuron, in press.
49. 2+ channels. J Neurosci 20:8290-8297.
50. Ohishi H, Akazawa C, Shigemoto R, Nakanishi S, Mizuno N (1995a) Distribution of the mRNAs for L-2-amino-4-phosphobutyrate-sensitive metabotropic glutamate receptors, mGluR4 and mGluR7, in the rat brain. J Comp Neurol 360:555-570.
51. Ohishi H, Nomura S, Ding YQ, Shigemoto R, Wada E, Kinoshita A, Li JL, Neki A, Nakanishi S, Mizuno N (1995b) Presynaptic localization of a metabotropic glutamate receptor, mGluR7, in the primary afferent neurons: an immunohistochemical study in the rat. Neurosci Lett 202:85-88.
52. Oliet SHR, Malenka RC, Nicoll RA (1997) Two distinct forms of long-term depression coexist in CA1 hippocampal pyramidal cells. Neuron 18:969-982.
53. Pape HC (1996) Queer current and pacemaker: the hyperpolarization- activated cation current in neurons. Annu Rev Physiol 58:299-327.
54. Poolos NP, Migliore M, Johnston D (2002) Pharmacological upregulation of h-channels reduces the excitability of pyramidal neuron dendrites. Nat Neurosci 5:767-774.
55. Rammes G, Palmer M, Eder M, Dodt HU, Zieglgänsberger W, Collingridge GL (2003) Activation of mGlu receptors induces LTD without affecting postsynaptic sensitivity of CA1 neurons in rat hippocampal slices. J Physiol (Lond) 546:455-460.
56. Selig DK, Lee HK, Bear MF, Malenka RC (1995) Reexamination of the effects of MCPG on hippocampal LTP, LTD, and depotentiation. J Neurophysiol 74:1075-1082.
57. Taube JS, Schwartzkroin PA (1988) Mechanisms of long-term potentiation: EPSP/spike dissociation, intradendritic recordings, and glutamate sensitivity. J Neurosci 8:1632-1644.
58. Turrigiano G, Abbott LF, Marder E (1994) Activity-dependent changes in the intrinsic properties of cultured neurons. Science 264:974-977.
59. Turrigiano GG, Nelson SB (2000) Hebb and homeostasis in neuronal plasticity. Curr Opin Neurobiol 10:358-364.
60. Wang Y, Wu J, Rowan MJ, Anwyl R (1998) Role of protein kinase C in the induction of homosynaptic long-term depression by brief low frequency stimulation in the dentate gyrus of the rat hippocampus in vitro. J Physiol (Lond) 513:467-475.
61. Wang Z, Xu NL, Wu CP, Duan S, Poo MM (2003) Bidirectional changes in spatial dendritic integration accompanying long-term synaptic modifications. Neuron 37:463-472.
62. Wilson RC (1981) Changes in translation of synaptic excitation to dentate granule cell discharge accompanying long-term potentiation. I. Differences between normal and reinnervated dentate gyrus. J Neurophysiol 46:324-338.
63. Xu J, Kang N, Jiang L, Nedergaard M, Kang J (2005) Activity-dependent long-term potentiation of intrinsic excitability in hippocampal CA1 pyramidal neurons. J Neurosci 25:1750-1760.