Plasticity of Burst Firing Induced by Synergistic Activation of Metabotropic Glutamate and Acetylcholine Receptors

Neuron

Volumn 61, Issue 2, 2009, Pages 287-300

  Moore, Shannon J ^a   Cooper, Donald C ^b   Spruston, Nelson ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

MOLNEURO; SIGNALING

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; CHOLINERGIC RECEPTOR; METABOTROPIC RECEPTOR; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR 5; METABOTROPIC RECEPTOR ANTAGONIST; MUSCARINIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DEPOLARIZATION; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; MALE; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RAT; SPIKE; SUBICULUM;

ACETYLCHOLINE; ACTION POTENTIALS; AFFERENT PATHWAYS; ANIMALS; CHOLINERGIC FIBERS; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; GLUTAMIC ACID; HIPPOCAMPUS; MALE; NEURONAL PLASTICITY; PYRAMIDAL CELLS; RATS; RATS, WISTAR; RECEPTORS, CHOLINERGIC; RECEPTORS, METABOTROPIC GLUTAMATE; RECEPTORS, MUSCARINIC; SEPTAL NUCLEI; SYNAPTIC TRANSMISSION; THETA RHYTHM;

EID: 58549092414     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2008.12.013     Document Type: Article

References (74)

1. Abraham W.C., Gustafsson B., and Wigstrom H. Long-term potentiation involves enhanced synaptic excitation relative to synaptic inhibition in guinea-pig hippocampus. J. Physiol. 394 (1987) 367-380
2. Aizenman C.D., and Linden D.J. Rapid, synaptically driven increases in the intrinsic excitability of cerebellar deep nuclear neurons. Nat. Neurosci. 3 (2000) 109-111
3. Azouz R., Jensen M.S., and Yaari Y. Ionic basis of spike after-depolarization and burst generation in adult rat hippocampal CA1 pyramidal cells. J. Physiol. 492 (1996) 211-223
4. Battaglia F.P., Sutherland G.R., and McNaughton B.L. Hippocampal sharp wave bursts coincide with neocortical "up-state" transitions. Learn. Mem. 11 (2004) 697-704
5. 2+ induced epileptiform activity in the subiculum before and after disconnection from rat hippocampal and entorhinal cortex slices. Neurosci. Lett. 205 (1996) 25-28
6. Benini R., and Avoli M. Rat subicular networks gate hippocampal output activity in an in vitro model of limbic seizures. J. Physiol. 566 (2005) 885-900
7. Berkeley J.L., Gomeza J., Wess J., Hamilton S.E., Nathanson N.M., and Levey A.I. M1 muscarinic acetylcholine receptors activate extracellular signal-regulated kinase in CA1 pyramidal neurons in mouse hippocampal slices. Mol. Cell Neurosci. 18 (2001) 512-524
8. Bliss T.V., and Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 232 (1973) 331-356
9. Buzsaki G. Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus 15 (2005) 827-840
10. Campanac E., and Debanne D. Spike timing-dependent plasticity: a learning rule for dendritic integration in rat CA1 pyramidal neurons. J. Physiol. 586 (2008) 779-793
11. Cattaneo A., Maffei L., and Morrone C. Patterns in the discharge of simple and complex visual cortical cells. Proc. R. Soc. Lond. B. Biol. Sci. 212 (1981) 279-297
12. Chaouloff F., Hémar A., and Manzoni O. Acute stress facilitates hippocampal CA1 metabotropic glutamate receptor-dependent long-term depression. J. Neurosci. 27 (2007) 7130-7135
13. Chavez-Noriega L.E., Halliwell J.V., and Bliss T.V. A decrease in firing threshold observed after induction of the EPSP-spike (E-S) component of long-term potentiation in rat hippocampal slices. Exp. Brain Res. 79 (1990) 633-641
14. Chevaleyre V., and Castillo P.E. Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron 38 (2003) 461-472
15. Christie B.R., Magee J.C., and Johnston D. The role of dendritic action potentials and Ca2+ influx in the induction of homosynaptic long-term depression in hippocampal CA1 pyramidal neurons. Learn. Mem. 3 (1996) 160-169
16. Ciruela F., Escriche M., Burgueno J., Angulo E., Casado V., Soloviev M.M., Canela E.I., Mallol J., Chan W.Y., Lluis C., et al. Metabotropic glutamate 1alpha and adenosine A1 receptors assemble into functionally interacting complexes. J. Biol. Chem. 276 (2001) 18345-18351
17. Cohen I., Navarro V., Clemenceau S., Baulac M., and Miles R. On the origin of interictal activity in human temporal lobe epilepsy in vitro. Science 298 (2002) 1418-1421
18. Commins S., Gigg J., Anderson M., and O'Mara S.M. The projection from hippocampal area CA1 to the subiculum sustains long-term potentiation. Neuroreport 9 (1998) 847-850
19. Cooper D.C., Moore S.J., Staff N.P., and Spruston N. Psychostimulant-induced plasticity of intrinsic neuronal excitability in ventral subiculum. J. Neurosci. 23 (2003) 9937-9946
20. Cooper D.C., Chung S., and Spruston N. Output-mode transitions are controlled by prolonged inactivation of sodium channels in pyramidal neurons of subiculum. PLoS Biol. 3 (2005) e175
21. Daoudal G., and Debanne D. Long-term plasticity of intrinsic excitability: learning rules and mechanisms. Learn. Mem. 10 (2003) 456-465
22. Disterhoft J.F., and Oh M. Modulation of cholinergic transmission enhances excitability of hippocampal pyramidal neurons and ameliorates learning impairments in aging animals. Neurobiol. Learn. Mem. 80 (2003) 223-233
23. Disterhoft J.F., Kronforst-Collins M., Oh M.M., Power J.M., Preston A.R., and Weiss C. Cholinergic facilitation of trace eyeblink conditioning in aging rabbits. Life Sci. 64 (1999) 541-548
24. Dreier J.P., and Heinemann U. Regional and time dependent variations of low Mg2+ induced epileptiform activity in rat temporal cortex slices. Exp. Brain Res. 87 (1991) 581-596
25. Enz R. The trick of the tail: protein-protein interactions of metabotropic glutamate receptors. Bioessays 29 (2007) 60-73
26. Fotuhi M., Standaert D.G., Testa C.M., Penney Jr. J.B., and Young A.B. Differential expression of metabotropic glutamate receptors in the hippocampus and entorhinal cortex of the rat. Brain Res. Mol. Brain Res. 21 (1994) 283-292
27. Frick A., Magee J., and Johnston D. LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nat. Neurosci. 7 (2004) 126-135
28. Gereau IV R.W., and Conn P.J. A cyclic AMP-dependent form of associative synaptic plasticity induced by coactivation of beta-adrenergic receptors and metabotropic glutamate receptors in rat hippocampus. J. Neurosci. 14 (1994) 3310-3318
29. Gold P.E. Acetylcholine modulation of neural systems involved in learning and memory. Neurobiol. Learn. Mem. 80 (2003) 194-210
30. Golding N.L., Kath W.L., and Spruston N. Dichotomy of action-potential backpropagation in CA1 pyramidal neuron dendrites. J. Neurophysiol. 86 (2001) 2998-3010
31. Golding N.L., Staff N.P., and Spruston N. Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 418 (2002) 326-331
32. Gustafsson B., Wigstrom H., Abraham W.C., and Huang Y.Y. Long-term potentiation in the hippocampus using depolarizing current pulses as the conditioning stimulus to single volley synaptic potentials. J. Neurosci. 7 (1987) 774-780
33. Harris E., and Stewart M. Propagation of synchronous epileptiform events from subiculum backward into area CA1 of rat brain slices. Brain Res. 895 (2001) 41-49
34. Hasselmo M.E. What is the function of hippocampal theta rhythm?-Linking behavioral data to phasic properties of field potential and unit recording data. Hippocampus 15 (2005) 936-949
35. Hess G., and Gustafsson B. Changes in field excitatory postsynaptic potential shape induced by tetanization in the CA1 region of the guinea-pig hippocampal slice. Neuroscience 37 (1990) 61-69
36. Holthoff K., Kovalchuk Y., Yuste R., and Konnerth A. Single-shock LTD by local dendritic spikes in pyramidal neurons of mouse visual cortex. J. Physiol. 560 (2004) 27-36
37. Jay T.M., and Witter M.P. Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris-leucoagglutinin. J. Comp. Neurol. 313 (1991) 574-586
38. Jester J.M., Campbell L.W., and Sejnowski T.J. Associative EPSP-spike potentiation induced by pairing orthodromic and antidromic stimulation in rat hippocampal slices. J. Physiol. 484 (1995) 689-705
39. Jung H.Y., Staff N.P., and Spruston N. Action potential bursting in subicular pyramidal neurons is driven by a calcium tail current. J. Neurosci. 21 (2001) 3312-3321
40. Kelso S.R., Ganong A.H., and Brown T.H. Hebbian synapses in hippocampus. Proc. Natl. Acad. Sci. USA 83 (1986) 5326-5330
41. Kemppainen S., Jolkkonen E., and Pitkanen A. Projections from the posterior cortical nucleus of the amygdala to the hippocampal formation and parahippocampal region in rat. Hippocampus 12 (2002) 735-755
42. Kishi T., Tsumori T., Ono K., Yokota S., Ishino H., and Yasui Y. Topographical organization of projections from the subiculum to the hypothalamus in the rat. J. Comp. Neurol. 419 (2000) 205-222
43. Lape R., and Dani J.A. Complex response to afferent excitatory bursts by nucleus accumbens medium spiny projection neurons. J. Neurophysiol. 92 (2004) 1276-1284
44. Lisman J.E. Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci. 20 (1997) 38-43
45. Livingstone M.S., Freeman D.C., and Hubel D.H. Visual responses in V1 of freely viewing monkeys. Cold Spring Harb. Symp. Quant. Biol. 61 (1996) 27-37
46. Lopes da Silva F.H., Arnolds D.E., and Neijt H.C. A functional link between the limbic cortex and ventral striatum: physiology of the subiculum accumbens pathway. Exp. Brain Res. 55 (1984) 205-214
47. Losonczy A., Makara J.K., and Magee J.C. Compartmentalized dendritic plasticity and input feature storage in neurons. Nature 452 (2008) 436-441
48. Magee J.C., and Johnston D. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275 (1997) 209-213
49. Martin S.J., Grimwood P.D., and Morris R.G. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci. 23 (2000) 649-711
50. Metz A.E., Jarsky T., Martina M., and Spruston N. R-type calcium channels contribute to afterdepolarization and bursting in hippocampal CA1 pyramidal neurons. J. Neurosci. 25 (2005) 5763-5773
51. Metz A.E., Spruston N., and Martina M. Dendritic D-type potassium currents inhibit the spike afterdepolarization in rat hippocampal CA1 pyramidal neurons. J. Physiol. 581 (2007) 175-187
52. Moyer Jr. J.R., Thompson L.T., and Disterhoft J.F. Trace eyeblink conditioning increases CA1 excitability in a transient and learning-specific manner. J. Neurosci. 16 (1996) 5536-5546
53. Muller R.U., Kubie J.L., and Ranck Jr. J.B. Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J. Neurosci. 7 (1987) 1935-1950
54. O'Mara S. The subiculum: what it does, what it might do, and what neuroanatomy has yet to tell us. J. Anat. 207 (2005) 271-282
55. O'Mara S.M., Commins S., and Anderson M. Synaptic plasticity in the hippocampal area CA1-subiculum projection: implications for theories of memory. Hippocampus 10 (2000) 447-456
56. O'Mara S.M., Commins S., Anderson M., and Gigg J. The subiculum: a review of form, physiology and function. Prog. Neurobiol. 64 (2001) 129-155
57. Pike F.G., Meredith R.M., Olding A.W., and Paulsen O. Rapid report: postsynaptic bursting is essential for 'Hebbian' induction of associative long-term potentiation at excitatory synapses in rat hippocampus. J. Physiol. 518 (1999) 571-576
58. Power A.E., Vazdarjanova A., and McGaugh J.L. Muscarinic cholinergic influences in memory consolidation. Neurobiol. Learn. Mem. 80 (2003) 178-193
59. Rhoades B.K., and Gross G.W. Potassium and calcium channel dependence of bursting in cultured neuronal networks. Brain Res. 643 (1994) 310-318
60. Robbins T.W., and Everitt B.J. Limbic-striatal memory systems and drug addiction. Neurobiol. Learn. Mem. 78 (2002) 625-636
61. Shigemoto R., Kinoshita A., Wada E., Nomura S., Ohishi H., Takada M., Flor P.J., Neki A., Abe T., Nakanishi S., et al. Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J. Neurosci. 17 (1997) 7503-7522
62. Staff N.P., and Spruston N. Intracellular correlate of EPSP-spike potentiation in CA1 pyramidal neurons is controlled by GABAergic modulation. Hippocampus 13 (2003) 801-805
63. Staff N.P., Jung H.Y., Thiagarajan T., Yao M., and Spruston N. Resting and active properties of pyramidal neurons in subiculum and CA1 of rat hippocampus. J. Neurophysiol. 84 (2000) 2398-2408
64. Stevens C.F., and Wang Y. Facilitation and depression at single central synapses. Neuron 14 (1995) 795-802
65. Su H., Alroy G., Kirson E.D., and Yaari Y. Extracellular calcium modulates persistent sodium current-dependent burst-firing in hippocampal pyramidal neurons. J. Neurosci. 21 (2001) 4173-4182
66. Sun W., and Rebec G.V. Lidocaine inactivation of ventral subiculum attenuates cocaine-seeking behavior in rats. J. Neurosci. 23 (2003) 10258-10264
67. Tabata T., Kawakami D., Hashimoto K., Kassai H., Yoshida T., Hashimotodani Y., Fredholm B.B., Sekino Y., Aiba A., and Kano M. G protein-independent neuromodulatory action of adenosine on metabotropic glutamate signalling in mouse cerebellar Purkinje cells. J. Physiol. 581 (2007) 693-708
68. Turrigiano G.G., and Nelson S.B. Homeostatic plasticity in the developing nervous system. Nat. Rev. Neurosci. 5 (2004) 97-107
69. van Welie I., van Hooft J.A., and Wadman W.J. Homeostatic scaling of neuronal excitability by synaptic modulation of somatic hyperpolarization-activated Ih channels. Proc. Natl. Acad. Sci. USA 101 (2004) 5123-5128
70. Volk L.J., Daly C.A., and Huber K.M. Differential roles for group 1 mGluR subtypes in induction and expression of chemically induced hippocampal long-term depression. J. Neurophysiol. 95 (2006) 2427-2438
71. Wittenberg G.M., and Wang S.S. Malleability of spike-timing-dependent plasticity at the CA3-CA1 synapse. J. Neurosci. 26 (2006) 6610-6617
72. Wozny C., Knopp A., Lehmann T.N., Heinemann U., and Behr J. The subiculum: a potential site of ictogenesis in human temporal lobe epilepsy. Epilepsia 46 Suppl 5 (2005) 17-21
73. Yue C., and Yaari Y. KCNQ/M channels control spike afterdepolarization and burst generation in hippocampal neurons. J. Neurosci. 24 (2004) 4614-4624
74. Zhang W., and Linden D.J. The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nat. Rev. Neurosci. 4 (2003) 885-900