Ictal but not interictal epileptic discharges activate astrocyte endfeet and elicit cerebral arteriole responses

Frontiers in Cellular Neuroscience

Volumn , Issue JUNE, 2011, Pages

  Gómez Gonzalo, Marta ^a,b   Losi, Gabriele ^a,b   Brondi, Marco ^a,c   Uva, Laura ^d   Sato, Sebastian Sulis ^a,c   de Curtis, Marco ^d   Ratto, Gian Michele ^a   Carmignoto, Giorgio ^a,b  

^a CNR   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

^c SCUOLA NORMALE SUPERIORE   (Italy)

^d DEPARTMENT OF NEUROSURGERY   (Italy)

Author keywords

Calcium; Epilepsy; Neurovascular coupling

Indexed keywords

CALCIUM ION;

ANIMAL CELL; ANIMAL TISSUE; ARTERIOLE; ARTICLE; ASTROCYTE; BOLD SIGNAL; BRAIN BLOOD FLOW; BRAIN SLICE; CALCIUM ABSORPTION; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL ACTIVATION; EPILEPTIC DISCHARGE; EVOKED RESPONSE; GLIA CELL; GUINEA PIG; IN VITRO STUDY; NEUROIMAGING; NEUROPIL; NONHUMAN; PATCH CLAMP; RAT; SIGNAL NOISE RATIO; VASODILATATION; VASOMOTOR REFLEX; WHOLE CELL;

EID: 84862592259     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2011.00008     Document Type: Article

References (47)

1. Akopov, S., Sercombe, R., and Seylaz, J. (1996). Cerebrovascular reacti- vity: role of endothelium/platelet/ leukocyte interactions. Cerebrovasc. Brain Metab. Rev. 8, 11-94.
2. Archer, J. S., Abbott, D. F., Waites, A. B., and Jackson, G. D. (2003). fMRI deactivation of the poste- rior cingulate during generalized spike and wave. Neuroimage 20, 1915-1922.
3. Avoli, M., Barbarosie, M., Lucke, A., Nagao, T., Lopantsev, V., and Kohling, R. (1996). Synchronous GABA-mediated potentials and epileptiform discharges in the rat limbic system in vitro. J. Neurosci. 16,3912-3924.
4. Avoli, M., D'antuono, M., Louvel, J., Kohling, R., Biagini, G., Pumain, R., D'arcangelo, G., and Tancredi, V. (2002). Network and pharmacolog- ical mechanisms leading to epilepti- form synchronization in the limbic system in vitro. Prog. Neurobiol. 68, 167-207.
5. Bagshaw, A. P., Aghakhani, Y., Benar, C. G., Kobayashi, E., Hawco, C., Dubeau, F., Pike, G. B., and Gotman, J. (2004). EEG-fMRI of focal epilep- tic spikes: analysis with multiple haemodynamic functions and comparison with gadolinium-enhanced MR angiograms. Hum. Brain Mapp. 22,179-192.
6. Boison, D. (2005). Adenosine and epilepsy: from therapeutic rationale to new therapeutic strategies. Neuroscientist 11, 25-36.
7. Carmignoto, G., and Gomez-Gonzalo, M. (2010). The contribution of astrocyte signalling to neurovascular coupling. Brain Res. Rev. 63, 138-148.
8. Cauli, B., Tong, X.-K., Rancillac, A., Serluca, N., Lambolez, B., Rossier, J., and Hamel, E. (2004). Cortical GABA interneurons in neurovascular coupling: relays for subcortical vasoactive pathways. J. Neurosci. 24, 8940-8949.
9. D'antuono, M., Kohling, R., Ricalzone, S., Gotman, J., Biagini, G., and Avoli, M. (2010). Antiepileptic drugs abol- ish ictal but not interictal epilepti- form discharges in vitro. Epilepsia 51,423-431.
10. De Curtis, M., and Avanzini, G. (2001). Interictal spikes in focal epileptoge-nesis. Prog. Neurobiol. 63, 541-567.
11. De Curtis, M., Biella, G., Buccellati, C., and Folco, G. (1998). Simul- taneous investigation of the neuronal and vascular compartments in the guinea pig brain isolated in vitro. Brain Res. Brain Res. Protoc. 3,221-228.
12. De Curtis, M., Pare, D., and Llinas, R. R. (1991). The electrophysiology of the olfactory-hippocampal circuit in the isolated and perfused adult mam-malian brain in vitro. Hippocampus 1,341-354.
13. Fellin, T., Pascual, O., Gobbo, S., Pozzan, T., Haydon, P. G., and Carmignoto, G. (2004). Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynap-tic NMDA receptors. Neuron 43, 729-743.
14. Fergus, A., Jin, Y., Thai, Q. A., Kas-Sell, N. F., and Lee, K. S. (1995). Vasodilatory actions of calcitonin gene-relatedpeptideandnitricoxide in parenchymal microvessels of the rat hippocampus. Brain Res. 694, 78-84.
15. Fergus, A., and Lee, K.S.(1997).Regulation of cerebral microvessels by glu- tamatergic mechanisms. Brain Res. 754,35-45.
16. Filosa, J. A., Bonev, A. D., Straub, S. V., Meredith, A. L., Wilkerson, M. K., Aldrich, R. W., and Nelson, M. T. (2006). Local potassium signaling couples neuronal activity to vasodi- lation in the brain. Nat. Neurosci. 9, 1397-1403.
17. Girouard, H., and Iadecola, C. (2006). Neurovascular coupling in the nor- mal brain and in hypertension, stroke, and Alzheimer disease. J. Appl. Physiol. 100, 328-335.
18. Gomez-Gonzalo, M., Losi, G., Chiavegato, A., Zonta, M., Cammarota, M., Brondi, M., Vetri, F., Uva, L., Pozzan, T., De Curtis, M., Ratto, G. M., and Carmignoto, G. (2010). An excitatory loop with astrocytes contributes to drive neurons to seizure threshold. PLoS Biol. 8, e1000352. doi: 10.1371/journal.pbio.1000352
19. Gordon, G. R., Choi, H. B., Rungta, R. L., Ellis-Davies, G. C., and Macvicar, B. A. (2008). Brain metabolism dic-tates the polarity of astrocyte con- trol over arterioles. Nature 456, 745-749.
20. Gotman, J., Kobayashi, E., Bagshaw, A. P., Benar, C. G., and Dubeau, F. (2006). Combining EEG and fMRI:a multimodal tool for epilepsy research. Magn. Reson. Imaging 23, 906-920.
21. Harkin, C. P., Hudetz, A. G., Schmeling, W. T., Kampine, J. P., and Farber, N. E. (1997a). Halothane-induced dilatation of intraparenchymal arterioles in rat brain slices: a comparison to sodium nitro-prusside. Anesthesiology 86, 885-894.
22. Harkin, C. P., Schmeling, W. T., Kampine, J. P., and Farber, N. E. (1997b). The effects of hyper- and hypocarbia on intraparenchymal arterioles in rat brain slices. Neuroreport 8, 1841-1844.
23. Haydon, P. G., and Carmignoto, G. (2006). Astrocyte control of synaptic transmission and neurovas- cular coupling. Physiol. Rev. 86, 1009-1031.
24. Horiuchi, T., Dietrich, H. H., Hongo, K., Goto, T., and Dacey, R. G. Jr. (2002). Role of endothelial nitric oxide and smooth muscle potassium channels in cerebral arteriolar dilation in response to acidosis. Stroke 33,844-849.
25. Iadecola, C. (2004). Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat. Rev. Neu- rosci. 5, 347-360.
26. Iadecola, C., and Nedergaard, M. (2007). Glial regulation of the cerebral microvasculature. Nat. Neurosci. 10, 1369-1376.
27. Jefferys, J. G. R. (2003). Models and mechanisms of experimental epilep-sies. Epilepsia 44(Suppl. 12), 44-50.
28. Knot, H. J., Zimmermann, P. A., and Nelson, M. T. (1996). Extracel- lular K(+)-induced hyperpolariza- tions and dilatations of rat coronary and cerebral arteries involve inward rectifier K(+) channels. J. Physiol. 492,419-430.
29. Kobayashi, E., Bagshaw, A. P., Grova, C., Dubeau, F., and Gotman, J. (2006). Negative BOLD responses to epileptic spikes. Hum. Brain Mapp. 27, 488-497.
30. Kuhl, D. E., Engel, J. Jr., Phelps, M. E., and Selin, C. (1980). Epileptic patterns of local cerebral metab- olism and perfusion in humans determined by emission computed tomography of 18FDG and 13NH3. Ann. Neurol. 8, 348-360.
31. Librizzi, L., Folco, G., and De Curtis, M. (2000). Nitric oxide synthase inhibitors unmask acetylcholine- mediated constriction of cerebral vessels in the in vitro isolated guinea-pig brain. Neuroscience 101, 283-287.
32. Lindauer, U., Vogt, J., Schuh-Hofer, S., Dreier, J. P., and Dirnagl, U. (2003). Cerebrovascular vasodi- lation to extraluminal acidosis occurs via combined activation of ATP-sensitive and Ca2+-activated potassium channels. J. Cereb. Blood Flow Metab. 23, 1227-1238.
33. Losi, G., Cammarota, M., Chiavegato, A., Gomez-Gonzalo, M., and Carmignoto, G. (2010). A new experimental model of focal seizures intheentorhinalcortex. Epilepsia 51, 1493-1502.
34. Lovick, T. A., Brown, L. A., and Key, B. J. (1999). Neurovascu- lar relationships in hippocampal slices: physiological and anatomical studies of mechanisms underlying flow-metabolism coupling in intra- parenchymal microvessels. Neuroscience 92, 47-60.
35. Metea, M. R., and Newman, E. A. (2006). Glial cells dilate and con- strict blood vessels: a mechanism of neurovascular coupling. J. Neurosci. 26,2862-2870.
36. Mulligan, S. J., and Macvicar, B. A. (2004). Calcium transients in astro- cyte endfeet cause cerebrovascular constrictions. Nature 431, 195-199.
37. Nimmerjahn, A., Kirchhoff, F., Kerr, J. N., and Helmchen, F. (2004). Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo. Nat. Methods 1, 31-37.
38. Pasti, L., Volterra, A., Pozzan, T., and Carmignoto, G. (1997). Intracellu- lar calcium oscillations in astrocytes: a highly plastic, bidirectional form of communication between neurons and astrocytes in situ. J. Neurosci. 17, 7817-7830.
39. Sagher, O., Zhang, X. Q., Szeto, W., Thai, Q. A., Jin, Y., Kassell, N. F., and Lee, K. S. (1993). Live com- puterized videomicroscopy of cere- bral microvessels in brain slices. J. Cereb. Blood Flow Metab. 13, 676-682.
40. Straub, S. V., Bonev, A. D., Wilkerson, M. K., and Nelson, M. T. (2006). Dynamic inositol trisphosphate-mediated calcium signals within astrocytic endfeet underlie vasodilation of cerebral arterioles. J. Gen. Physiol. 128, 659-669.
41. Takano, T., Tian, G.-F., Peng, W., Lou, N., Libionka, W., Han, X., and Nedergaard, M. (2006). Astrocyte- mediated control of cerebral blood flow. Nat. Neurosci. 9, 260-267.
42. Traub, R. D., and Wong, R. K. (1982). Cellular mechanism of neuronal synchronization in epilepsy. Science 216,745-747.
43. Van Paesschen, W., Dupont, P., Sunaert, S., Goffin, K., and Van Laere, K. (2007). The use of SPECT and PET in routine clinical practice in epilepsy. Curr. Opin. Neurol. 20, 194-202.
44. Yamamoto, T., and Kato, T.(2002).Para- doxical correlation between signal in functional magnetic resonance imaging and deoxygenated haemo- globin content in capillaries: a new theoretical explanation. Phys. Med. Biol. 47, 1121-1141.
45. Zhao, M., Ma, H., Suh, M., and Schwartz, T. H. (2009). Spatiotem- poral dynamics of perfusion and oximetry during ictal discharges in the rat neocortex. J. Neurosci. 29, 2814-2823.
46. Zimmermann, A., Domoki, F., and Bari, F. (2008). Seizure-induced alter- ations in cerebrovascular function in the neonate. Dev. Neurosci. 30, 293-305.
47. Zonta, M., Angulo, M. C., Gobbo, S., Rosengarten, B., Hossmann, K.- A., Pozzan, T., and Carmignoto, G. (2003). Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat. Neurosci. 6, 43-50.