Enhanced Excitatory Transmission at Cortical Synapses as the Basis for Facilitated Spreading Depression in CaV2.1 Knockin Migraine Mice

Neuron

Volumn 61, Issue 5, 2009, Pages 762-773

  Tottene, Angelita ^a   Conti, Rossella ^a   Fabbro, Alessandra ^a   Vecchia, Dania ^a   Shapovalova, Maryna ^a   Santello, Mirko ^a   van den Maagdenberg, Arn M J M ^b   Ferrari, Michel D ^b   Pietrobon, Daniela ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

HUMDISEASE; MOLNEURO; SYSNEURO

Indexed keywords

CALCIUM CHANNEL P TYPE; CALCIUM CHANNEL Q TYPE; GLUTAMIC ACID; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX; BRAIN SLICE; CALCIUM TRANSPORT; CELL CULTURE; CONTROLLED STUDY; CORRELATION ANALYSIS; ELECTROPHYSIOLOGY; EXCITATION; FHM1 GENE; GENE; GENE MUTATION; IN VITRO STUDY; KNOCKOUT MOUSE; MIGRAINE; MOUSE; NERVE CELL; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SPREADING CORTICAL DEPRESSION; SYNAPSE; SYNAPTIC TRANSMISSION; WILD TYPE;

ANIMALS; ANIMALS, NEWBORN; ARGININE; BIOPHYSICAL PROCESSES; CALCIUM; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, N-TYPE; CEREBRAL CORTEX; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMINE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MIGRAINE DISORDERS; MUTATION; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; SPREADING CORTICAL DEPRESSION; SYNAPSES;

EID: 61549136416     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2009.01.027     Document Type: Article

References (63)

1. Anderson T.R., and Andrew R.D. Spreading depression: imaging and blockade in the rat neocortical brain slice. J. Neurophysiol. 88 (2002) 2713-2725
2. Aurora S.K., and Wilkinson F. The brain is hyperexcitable in migraine. Cephalalgia 27 (2007) 1442-1453
3. 1A subunit of P/Q type calcium channels. Neuroscience 95 (2000) 639-645
4. Ayata C., Jin H., Kudo C., Dalkara T., and Moskowitz M.A. Suppression of cortical spreading depression in migraine prophylaxis. Ann. Neurol. 59 (2006) 652-661
5. Bekkers J.M., and Stevens C.F. Excitatory and inhibitory autaptic currents in isolated hippocampal neurons maintained in cell culture. Proc. Natl. Acad. Sci. USA 88 (1991) 7834-7838
6. Bolay H., Reuter U., Dunn A.K., Huang Z., Boas D.A., and Moskowitz M.A. Intrinsic brain activity triggers trigeminal meningeal afferents in a migraine model. Nat. Med. 8 (2002) 136-142
7. Bowyer S.M., Aurora K.S., Moran J.E., Tepley N., and Welch K.M. Magnetoencephalographic fields from patients with spontaneous and induced migraine aura. Ann. Neurol. 50 (2001) 582-587
8. Canals S., Makarova I., Lopez-Aguado L., Largo C., Ibarz J.M., and Herreras O. Longitudinal depolarization gradients along the somatodendritic axis of CA1 pyramidal cells: a novel feature of spreading depression. J. Neurophysiol. 94 (2005) 943-951
9. 2+ channelopathy. Neuron 43 (2004) 387-400
10. Coppola G., Pierelli F., and Schoenen J. Is the cerebral cortex hyperexcitable or hyperresponsive in migraine?. Cephalalgia 27 (2007) 1427-1439
11. Faber D.S., and Korn H. Applicability of the coefficient of variation method for analyzing synaptic plasticity. Biophys. J. 60 (1991) 1288-1294
12. Fletcher C.F., Tottene A., Lennon V.A., Wilson S.M., Dubel S.J., Paylor R., Hosford D.A., Tessarollo L., McEnery M.W., Pietrobon D., et al. Dystonia and cerebellar atrophy in Cacna1a null mice lacking P/Q calcium channel activity. FASEB J. 15 (2001) 1288-1290
13. Footitt D.R., and Newberry N.R. Cortical spreading depression induces an LTP-like effect in rat neocortex in vitro. Brain Res. 781 (1998) 339-342
14. Galarreta M., and Hestrin S. Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex. Nat. Neurosci. 1 (1998) 587-594
15. Goadsby P.J., Lipton R.B., and Ferrari M.D. Migraine current understanding and treatment. N. Engl. J. Med. 346 (2002) 257-270
16. Grafstein B. Mechanism of spreading cortical depression. J. Neurophysiol. 19 (1956) 154-171
17. Haan J., Terwindt G.M., van den Maagdenberg A.M., Stam A.H., and Ferrari M.D. A review of the genetic relation between migraine and epilepsy. Cephalalgia 28 (2008) 105-113
18. Hadjikhani N., Sanchez del Rio M., Wu O., Schwartz D., Bakker D., Fischl B., Kwong K.K., Cutrer F.M., Rosen B.R., Tootell R.B.H., et al. Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proc. Natl. Acad. Sci. USA 98 (2001) 4687-4692
19. Haglund M.M., and Schwartzkroin P.A. Role of Na-K pump potassium regulation and IPSPs in seizures and spreading depression in immature rabbit hippocampal slices. J. Neurophysiol. 63 (1990) 225-239
20. 1A calcium channel subunit linked to familial hemiplegic migraine. J. Neurosci. 19 (1999) 1610-1619
21. Herreras O. Electrical prodromals of spreading depression void Grafstein's potassium hypothesis. J. Neurophysiol. 94 (2005) 3656-3657
22. Jensen M.S., and Yaari Y. Role of intrinsic burst firing, potassium accumulation, and electrical coupling in the elevated potassium model of hippocampal epilepsy. J. Neurophysiol. 77 (1997) 1224-1233
23. Kager H., Wadman W.J., and Somjen G.G. Conditions for the triggering of spreading depression studied with computer simulations. J. Neurophysiol. 88 (2002) 2700-2712
24. Kaja S., van de Ven R.C., Broos L.A., Veldman H., van Dijk J.G., Verschuuren J.J., Frants R.R., Ferrari M.D., van den Maagdenberg A.M., and Plomp J.J. Gene dosage-dependent transmitter release changes at neuromuscular synapses of CACNA1A R192Q knockin mice are non-progressive and do not lead to morphological changes or muscle weakness. Neuroscience 135 (2005) 81-95
25. Kapfer C., Glickfeld L.L., Atallah B.V., and Scanziani M. Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex. Nat. Neurosci. 10 (2007) 743-753
26. Kunkler P.E., Hulse R.E., Schmitt M.W., Nicholson C., and Kraig R.P. Optical current source density analysis in hippocampal organotypic culture shows that spreading depression occurs with uniquely reversing currents. J. Neurosci. 25 (2005) 3952-3961
27. Lauritzen M. Pathophysiology of the migraine aura. The spreading depression theory. Brain 117 (1994) 199-210
28. Marrannes R., Willems R., De Prins E., and Wauquier A. Evidence for a role of the N-methyl-D-aspartate (NMDA) receptor in cortical spreading depression in the rat. Brain Res. 457 (1988) 226-240
29. Marty A., and Llano I. Excitatory effects of GABA in established brain networks. Trends Neurosci. 28 (2005) 284-289
30. McCarren M., and Alger B.E. Use-dependent depression of IPSPs in rat hippocampal pyramidal cells in vitro. J. Neurophysiol. 53 (1985) 557-571
31. 2+ sensor proteins mediates short-term synaptic plasticity. Neuron 57 (2008) 210-216
32. Monier C., Chavane F., Baudot P., Graham L.J., and Fregnac Y. Orientation and direction selectivity of synaptic inputs in visual cortical neurons: a diversity of combinations produces spike tuning. Neuron 37 (2003) 663-680
33. Neher E. Correction for liquid junction potentials in patch clamp experiments. Methods Enzymol. 207 (1992) 123-131
34. 2+ channel gene CACNL1A4. Cell 87 (1996) 543-552
35. Pietrobon D. Function and dysfunction of synaptic calcium channels: insights from mouse models. Curr. Opin. Neurobiol. 15 (2005) 257-265
36. Pietrobon D. Migraine: new molecular mechanisms. Neuroscientist 11 (2005) 373-386
37. Pietrobon D. Familial hemiplegic migraine. Neurotherapeutics 4 (2007) 274-284
38. Pietrobon D., and Striessnig J. Neurobiology of migraine. Nat. Rev. Neurosci. 4 (2003) 386-398
39. Pinto D.J., Patrick S.L., Huang W.C., and Connors B.W. Initiation, propagation, and termination of epileptiform activity in rodent neocortex in vitro involve distinct mechanisms. J. Neurosci. 25 (2005) 8131-8140
40. Poolos N.P., and Kocsis J.D. Elevated extracellular potassium concentration enhances synaptic activation of N-methyl-D-aspartate receptors in hippocampus. Brain Res. 508 (1990) 7-12
41. 2+ channels mediate transmitter release with a similar cooperativity at rat hippocampal autapses. J. Neurosci. 18 (1998) 2849-2855
42. Reyes A., Lujan R., Rozov A., Burnashev N., Somogyi P., and Sakmann B. Target-cell-specific facilitation and depression in neocortical circuits. Nat. Neurosci. 1 (1998) 279-285
43. 2+ buffers in facilitating and depressing nerve terminals of pyramidal cells in layer 2/3 of the rat neocortex indicates a target cell-specific difference in presynaptic calcium dynamics. J. Physiol. 531 (2001) 807-826
44. Schneggenburger R., and Neher E. Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406 (2000) 889-893
45. Shu Y., Hasenstaub A., and McCormick D.A. Turning on and off recurrent balanced cortical activity. Nature 423 (2003) 288-293
46. Silberberg G., and Markram H. Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 53 (2007) 735-746
47. 2+ currents in rat CA1 hippocampal pyramidal neurons. Neuroscience 116 (2003) 629-638
48. Somjen G.G. Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol. Rev. 81 (2001) 1065-1096
49. Takada N., Yanagawa Y., and Komatsu Y. Activity-dependent maturation of excitatory synaptic connections in solitary neuron cultures of mouse neocortex. Eur. J. Neurosci. 21 (2005) 422-430
50. Thomsen L.L., Eriksen M.K., Roemer S.F., Andersen I., Olesen J., and Russell M.B. A population-based study of familial hemiplegic migraine suggests revised diagnostic criteria. Brain 125 (2002) 1379-1391
51. Thomsen L.L., Olesen J., and Russell M.B. Increased risk of migraine with typical aura in probands with familial hemiplegic migraine and their relatives. Eur. J. Neurol. 10 (2003) 421-427
52. Thomson A.M., Deuchars J., and West D.C. Large, deep layer pyramid-pyramid single axon EPSPs in slices of rat motor cortex display paired pulse and frequency-dependent depression, mediated presynaptically and self-facilitation, mediated postsynaptically. J. Neurophysiol. 70 (1993) 2354-2369
53. 1E subunits form the pore of three cerebellar R-type calcium channels with different pharmacological and permeation properties. J. Neurosci. 1 (2000) 171-178
54. V2.1 current density in neurons. Proc. Natl. Acad. Sci. USA 99 (2002) 13284-13289
55. V2.1 calcium channels produced by mutation S218L causing familial hemiplegic migraine and delayed cerebral edema and coma after minor head trauma. J. Biol. Chem. 280 (2005) 17678-17686
56. Traynelis S.F., and Dingledine R. Potassium-induced spontaneous electrographic seizures in the rat hippocampal slice. J. Neurophysiol. 59 (1988) 259-276
57. Turrigiano G.G., and Nelson S.B. Homeostatic plasticity in the developing nervous system. Nat. Rev. Neurosci. 5 (2004) 97-107
58. van den Maagdenberg A.M., Pietrobon D., Pizzorusso T., Kaja S., Broos L.A., Cesetti T., van de Ven R.C., Tottene A., van der Kaa J., Plomp J.J., et al. A Cacna1a knockin migraine mouse model with increased susceptibility to cortical spreading depression. Neuron 41 (2004) 701-710
59. Vilagi I., Klapka N., and Luhmann H.J. Optical recording of spreading depression in rat neocortical slices. Brain Res. 898 (2001) 288-296
60. Wadman W.J., Juta A.J., Kamphuis W., and Somjen G.G. Current source density of sustained potential shifts associated with electrographic seizures and with spreading depression in rat hippocampus. Brain Res. 570 (1992) 85-91
61. Welch K.M. Brain hyperexcitability: the basis for antiepileptic drugs in migraine prevention. Headache 45 Suppl 1 (2005) S25-S32
62. Westenbroek R.E., Sakurai T., Elliott E.M., Hell J.W., Starr T.V., Snutch T.P., and Catterall W.A. Immunochemical identification and subcellular distribution of the alpha1A subunits of brain calcium channels. J. Neurosci. 15 (1995) 6403-6418
63. Zaitsev A.V., Povysheva N.V., Lewis D.A., and Krimer L.S. P/Q-type, but not N-type, calcium channels mediate GABA release from fast-spiking interneurons to pyramidal cells. J. Neurophysiol. 97 (2007) 3567-3573