MGluR-mediated calcium waves that invade the soma regulate firing in layer V medial prefrontal cortical pyramidal neurons

Cerebral Cortex

Volumn 18, Issue 2, 2008, Pages 407-423

  Hagenston, Anna M ^a   Fitzpatrick, John S ^a   Yeckel, Mark F ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Calcium release; Inositol 1,4,5 trisphosphate receptor; Neocortex physiology; SK channels; Slow afterdepolarization

Indexed keywords

CALCIUM; METABOTROPIC RECEPTOR;

AMPLITUDE MODULATION; ANIMAL CELL; ARTICLE; CALCIUM SIGNALING; CONTROLLED STUDY; DEPOLARIZATION; HYPERPOLARIZATION; NERVE CELL EXCITABILITY; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT;

ACTION POTENTIALS; ANIMALS; CALCIUM; CALCIUM SIGNALING; CELLS, CULTURED; FEEDBACK; MALE; NERVE NET; PREFRONTAL CORTEX; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, METABOTROPIC GLUTAMATE; SYNAPTIC TRANSMISSION;

EID: 38849137842     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhm075     Document Type: Article

References (73)

1. Adkins CE, Taylor CW. 1999. Lateral inhibition of inositol 1,4,5-trisphosphate receptors by cytosolic Ca(2+). Curr Biol. 9:1115-1118.
2. Anwyl R. 1999. Metabotropic glutamate receptors: electrophysiological properties and role in plasticity. Brain Res Brain Res Rev. 29:83-120.
3. Bartus RT, Levere TE. 1977. Frontal decortication in rhesus monkeys: a test of the interference hypothesis. Brain Res. 119:233-248.
4. Batuev AS, Kursina NP, Shutov AP. 1990. Unit activity of the medial wall of the frontal cortex during delayed performance in rats. Behav Brain Res. 41:95-102.
5. Bekkers JM. 2000. Distribution of slow AHP channels on hippocampal CA1 pyramidal neurons. J Neurophysiol. 83:1756-1759.
6. Benardo LS, Prince DA. 1982. Cholinergic excitation of mammalian hippocampal pyramidal cells. Brain Res. 249:315-331.
7. Berendse HW, Groenewegen HJ. 1991. Restricted cortical termination fields of the midline and intralaminar thalamic nuclei in the rat. Neuroscience. 42:73-102.
8. Berridge MJ. 1998. Neuronal calcium signaling. Neuron. 21:13-26.
9. Bezprozvanny I, Ehrlich BE. 1994. Inositol (1,4,5)-trisphosphate (InsP3)-gated Ca channels from cerebellum: conduction properties for divalent cations and regulation by intraluminal calcium. J Gen Physiol. 104:821-856.
10. Bootman M, Niggli E, Berridge M, Lipp P. 1997. Imaging the hierarchical Ca2+ signalling system in HeLa cells. J Physiol. 499(Pt 2):307-314.
11. Callamaras N, Marchant JS, Sun XP, Parker I. 1998. Activation and coordination of InsP3-mediated elementary Ca2+ events during global Ca2+ signals in Xenopus oocytes. J Physiol. 509(Pt 1):81-91.
12. Camello C, Lomax R, Petersen OH, Tepikin AV. 2002. Calcium leak from intracellular stores - the enigma of calcium signalling. Cell Calcium. 32:355-361.
13. Cobb SR, Davies CH. 2005. Cholinergic modulation of hippocampal cells and circuits. J Physiol. 562:81-88.
14. 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.
15. Crepel V, Aniksztejn L, Ben-Ari Y, Hammond C. 1994. Glutamate metabotropic receptors increase a Ca(2+)-activated nonspecific cationic current in CA1 hippocampal neurons. J Neurophysiol. 72:1561-1569.
16. Durstewitz D, Seamans JK, Sejnowski TJ. 2000. Neurocomputational models of working memory. Nat Neurosci. 3(Suppl):1184-1191.
17. Finch EA, Augustine GJ. 1998. Local calcium signalling by inositol-1,4,5-trisphosphate in Purkinje cell dendrites. Nature. 396:753-756.
18. Fiorillo CD, Williams JT. 1998. Glutamate mediates an inhibitory postsynaptic potential in dopamine neurons. Nature. 394:78-82.
19. Friel D. 2004. Interplay between ER Ca2+ uptake and release fluxes in neurons and its impact on [Ca2+] dynamics. Biol Res. 37:665-674.
20. Friel DD, Tsien RW. 1992. A caffeine- and ryanodine-sensitive Ca2+ store in bullfrog sympathetic neurones modulates effects of Ca2+ entry on [Ca2+]i. J Physiol. 450:217-246.
21. Funahashi S, Bruce CJ, Goldman-Rakic PS. 1989. Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J Neurophysiol. 61:331-349.
22. Fuster JM. 1973. Unit activity in prefrontal cortex during delayed-response performance: neuronal correlates of transient memory. J Neurophysiol. 36:61-78.
23. Fuster JM. 1985. The prefrontal cortex, mediator of cross-temporal contingencies. Hum Neurobiol. 4:169-179.
24. Gao WJ, Goldman-Rakic PS. 2006. NMDA receptor-mediated epileptiform persistent activity requires calcium release from intracellular stores in prefrontal neurons. Exp Neurol. 197:495-504.
25. 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.
26. Goldman-Rakic PS. 1995. Cellular basis of working memory. Neuron. 14:477-485.
27. Guerineau NC, Bossu JL, Gahwiler BH, Gerber U. 1995. Activation of a nonselective cationic conductance by metabotropic glutamatergic and muscarinic agonists in CA3 pyramidal neurons of the rat hippocampus. J Neurosci. 15:4395-4407.
28. Gulledge AT, Park SB, Kawaguchi Y, Stuart G. 2007. Heterogeneity of phasic cholinergic signalling in neocortical neurons. J Neurophysiol 97:2215-2229.
29. Gulledge AT, Stuart GJ. 2005. Cholinergic inhibition of neocortical pyramidal neurons. J Neurosci. 25:10308-10320.
30. Haj-Dahmane S, Andrade R. 1996. Muscarinic activation of a voltage-dependent cation nonselective current in rat association cortex. J Neurosci. 16:3848-3861.
31. Haj-Dahmane S, Andrade R. 1998. Ionic mechanism of the slow afterdepolarization induced by muscarinic receptor activation in rat prefrontal cortex. J Neurophysiol. 80:1197-1210.
32. 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.
33. Hasuo H, Phelan KD, Twery MJ, Gallagher JP. 1990. A calcium-dependent slow afterdepolarization recorded in rat dorsolateral septal nucleus neurons in vitro. J Neurophysiol. 64:1838-1846.
34. Jaffe DB, Brown TH. 1994. Metabotropic glutamate receptor activation induces calcium waves within hippocampal dendrites. J Neurophysiol. 72:471-474.
35. Johnston D, Hoffman DA, Magee JC, Poolos NP, Watanabe S, Colbert CM, Migliore M. 2000. Dendritic potassium channels in hippocampal pyramidal neurons. J Physiol. 525(Pt 1):75-81.
36. Kapur A, Yeckel M, Johnston D. 2001. Hippocampal mossy fiber activity evokes Ca2+ release in CA3 pyramidal neurons via a metabotropic glutamate receptor pathway. Neuroscience. 107:59-69.
37. Klink R, Alonso A. 1997. Ionic mechanisms of muscarinic depolarization in entorhinal cortex layer II neurons. J Neurophysiol. 77: 1829-1843.
38. Korngreen A, Sakmann B. 2000. Voltage-gated K+ channels in layer 5 neocortical pyramidal neurones from young rats: subtypes and gradients. J Physiol. 525(Pt 3):621-639.
39. Kubota K, Niki H. 1971. Prefrontal cortical unit activity and delayed alternation performance in monkeys. J Neurophysiol. 34:337-347.
40. Larkum ME, Watanabe S, Nakamura T, Lasser-Ross N, Ross WN. 2003. Synaptically activated Ca2+ waves in layer 2/3 and layer 5 rat neocortical pyramidal neurons. J Physiol. 549:471-488.
41. Malmo RB. 1942. Interference factors in delayed response in monkeys after removal of frontal lobes. Neurophys. 5:295-308.
42. McCormick DA, Connors BW, Lighthall JW, Prince DA. 1985. Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol. 54:782-806.
43. Morikawa H, Imani F, Khodakhah K, Williams JT. 2000. Inositol 1,4,5-triphosphate-evoked responses in midbrain dopamine neurons. J Neurosci. 20:RC103.
44. Morikawa H, Khodakhah K, Williams JT. 2003. Two intracellular pathways mediate metabotropic glutamate receptor-induced Ca2+ mobilization in dopamine neurons. J Neurosci. 23:149-157.
45. Murphy BL, Arnsten AFT, Goldman-Rakic PS, Roth RH. 1996. Increased dopamine turnover in the prefrontal cortex impairs spatial working memory performance in rats and monkeys. Proc Natl Acad Sci USA. 93:1325-1329.
46. Nakamura T, Barbara JG, Nakamura K, Ross WN. 1999. Synergistic release of Ca2+ from IP3-sensitive stores evoked by synaptic activation of mGluRs paired with backpropagating action potentials. Neuron. 24:727-737.
47. Nakamura T, Lasser-Ross N, Nakamura K, Ross WN. 2002. Spatial segregation and interaction of calcium signalling mechanisms in rat hippocampal CA1 pyramidal neurons. J Physiol. 543:465-480.
48. Nakamura T, Nakamura K, Lasser-Ross N, Barbara JG, Sandler VM, Ross WN. 2000. Inositol 1,4,5-trisphosphate (IP3)-mediated Ca2+ release evoked by metabotropic agonists and backpropagating action potentials in hippocampal CA1 pyramidal neurons. J Neurosci. 20:8365-8376.
49. Narayanan NS, Laubach M. 2006. Top-down control of motor cortex ensembles by dorsomedial prefrontal cortex. Neuron. 52:921-931.
50. Parker I, Ivorra I. 1990. Localized all-or-none calcium liberation by inositol trisphosphate. Science. 250:977-979.
51. Parker I, Yao Y, Ilyin V. 1996. Fast kinetics of calcium liberation induced in Xenopus oocytes by photoreleased inositol trisphosphate. Biophys J. 70:222-237.
52. Partridge LD, Valenzuela CF. 2000. Block of hippocampal CAN channels by flufenamate. Brain Res. 867:143-148.
53. Paxinos G, Watson C. 1998. The rat brain in stereotaxic coordinates. [San Diego (CA)]: Academic Press.
54. Poolos NP, Johnston D. 1999. Calcium-activated potassium conductances contribute to action potential repolarization at the soma but not the dendrites of hippocampal CA1 pyramidal neurons. J Neurosci. 19:5205-5212.
55. Power JM, Sah P. 2002. Nuclear calcium signaling evoked by cholinergic stimulation in hippocampal CA1 pyramidal neurons. J Neurosci. 22:3454-3462.
56. Power JM, Sah P. 2005. Intracellular calcium store filling by an L-type calcium current in the basolateral amygdala at subthreshold membrane potentials. J Physiol. 562:439-453.
57. Pozzo-Miller LD, Connor JA, Andrews SB. 2000. Microheterogeneity of calcium signalling in dendrites. J Physiol. 525(Pt 1):53-61.
58. Pozzo-Miller LD, Petrozzino JJ, Golarai G, Connor JA. 1996. Ca2+ release from intracellular stores induced by afferent stimulation of CA3 pyramidal neurons in hippocampal slices. J Neurophysiol. 76: 554-562.
59. Rae MG, Irving AJ. 2004. Both mGluR1 and mGluR5 mediate Ca2+ release and inward currents in hippocampal CA1 pyramidal neurons. Neuropharmacology. 46:1057-1069.
60. Rae MG, Martin DJ, Collingridge GL, Irving AJ. 2000. Role of Ca2+ stores in metabotropic L-glutamate receptor-mediated supralinear Ca2+ signaling in rat hippocampal neurons. J Neurosci. 20:8628-8636.
61. Sah P. 1996. Ca(2+)-activated K+ currents in neurones: types, physiological roles and modulation. Trends Neurosci. 19:150-154.
62. Sailer CA, Hu H, Kaufmann WA, Trieb M, Schwarzer C, Storm JF, Knaus HG. 2002. Regional differences in distribution and functional expression of small-conductance Ca2+-activated K+ channels in rat brain. J Neurosci. 22:9698-9707.
63. Sailer CA, Kaufmann WA, Marksteiner J, Knaus HG. 2004. Comparative immunohistochemical distribution of three small-conductance Ca2+-activated potassium channel subunits, SK1, SK2, and SK3 in mouse brain. Mol Cell Neurosci. 26:458-469.
64. Sawaguchi T, Goldman-Rakic PS. 1991. D1 dopamine receptors in prefrontal cortex: involvement in working memory. Science. 251:947-950.
65. Schiller Y. 2004. Activation of a calcium-activated cation current during epileptiform discharges and its possible role in sustaining seizure-like events in neocortical slices. J Neurophysiol. 92:862-872.
66. Stutzmann GE, LaFerla FM, Parker I. 2003. Ca2+ signaling in mouse cortical neurons studied by two-photon imaging and photoreleased inositol triphosphate. J Neurosci. 23:758-765.
67. Verkhratsky AJ, Petersen OH. 1998. Neuronal calcium stores. Cell Calcium. 24:333-343.
68. Wang XJ. 2001. Synaptic reverberation underlying mnemonic persistent activity. Trends Neurosci. 24:455-463.
69. 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.
70. Yamada S, Takechi H, Kanchiku I, Kita T, Kato N. 2004. Smallconductance Ca2+-dependent K+ channels are the target of spikeinduced Ca2+ release in a feedback regulation of pyramidal cell excitability. J Neurophysiol. 91:2322-2329.
71. Yamamoto K, Hashimoto K, Nakano M, Shimohama S, Kato N. 2002. A distinct form of calcium release down-regulates membrane excitability in neocortical pyramidal cells. Neuroscience. 109:665-676.
72. Yuan LL, Chen X. 2006. Diversity of potassium channels in neuronal dendrites. Prog Neurobiol. 78:374-389.
73. Zahrt J, Taylor JR, Mathew RG, Arnsten AFT. 1997. Supranormal stimulation of dopamine D1 receptors in the rodent prefrontal cortex impairs spatial working memory performance. J Neurosci. 17:8528-8535.