Local haemodynamic changes preceding interictal spikes: A simultaneous electrocorticography (ECoG) and near-infrared spectroscopy (NIRS) analysis in rats

NeuroImage

Volumn 50, Issue 2, 2010, Pages 600-607

  Osharina, V ^a   Ponchel, E ^b   Aarabi, A ^a   Grebe, R ^a   Wallois, F ^a,b  

^a UNIVERSITÉ DE PICARDIE JULES VERNE   (France)

^b AMIENS UNIVERSITY HOSPITAL   (France)

Author keywords

Bicuculline methiodide; ECoG; Haemodynamic changes; Interictal spike; NIRS

Indexed keywords

BICUCULLINE METHIODIDE; OXYHEMOGLOBIN; BICUCULLINE; CONVULSANT AGENT; DRUG DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOENERGY; CONTROLLED STUDY; ELECTROCORTICOGRAPHY; FOCAL EPILEPSY; HEMODYNAMICS; MALE; NEAR INFRARED SPECTROSCOPY; NONHUMAN; OSCILLATION; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RAT; SENSORIMOTOR CORTEX; SIGNAL TRANSDUCTION; SPIKE; SPRAGUE DAWLEY RAT; ANIMAL; BRAIN; BRAIN CIRCULATION; BRAIN MAPPING; CHEMICALLY INDUCED DISORDER; CORTICAL SYNCHRONIZATION; ELECTROENCEPHALOGRAPHY; METHODOLOGY; PHYSIOLOGY; SEIZURE; VASCULARIZATION;

ANIMALS; BICUCULLINE; BRAIN; BRAIN MAPPING; CEREBROVASCULAR CIRCULATION; CONVULSANTS; CORTICAL SYNCHRONIZATION; ELECTROENCEPHALOGRAPHY; HEMODYNAMICS; MALE; RATS; RATS, SPRAGUE-DAWLEY; SEIZURES; SPECTROSCOPY, NEAR-INFRARED;

EID: 77952315818     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2010.01.009     Document Type: Article

References (57)

1. Aarabi, A., Kazemi, K., Grebe, R., Abrishami Moghaddam, H., Wallois, F., 2009. Detection of EEG transients in neonates and older children using a system based on dynamic time-warping template matching and spatial dipole clustering. NeuroImage 48 (1), 50-62.
2. Ances, B.M., 2004. Coupling of changes in cerebral blood ow with neural activity: what must initially dip must come back up. J. Cereb. Blood Flow. Metab. 24, 1-6.
3. Bashir, Z.I., Holmes, O., 1993. Phases in the development of a penicillin epileptiform focus in rat neocortex. Exp. Brain Res. 96, 319-327.
4. Bennett, M.R., Farnell, L., Gibson, W.G., 2008. Origin of blood volume change due to glutamatergic synaptic activity at astrocytes abutting on arteriolar smooth muscle cells. J. Theor. Biol. 250, 172-185.
5. Campbell, A., Homes, O., 1984. Bicuculline epileptogenesis in the rat. Brain Res. 323, 239-246.
6. Chamberlin, N.L., Traub, R.D., Dingledine, R., 1990. Role of EPSPs in initiation of spontaneous synchronized burst ring in rat hippocampal neurons bathed in high potassium. J. Neurophysiol. 64, 1000-1008.
7. Church, J., Baimbridge, K.G., 1991. Exposure to high-pH medium increases the incidence and extent of dye coupling between rat hippocampal CA1 pyramidal neurons in vitro. J. Neurosci. 11, 3289-3295.
8. Coles, J.A., Tsacopoulos, M., 1979. Potassium activity in photoreceptors, glial cells and extracellular space in the drone retina: changes during photostimulation. J. Physiol. 290 (2), 525-549 May.
9. Cosandier-Rimélé, D., Badier, J.M., Chauvel, P., Wendling, F., 2007. Modeling and interpretation of scalp-EEG and depth-EEG signals during interictal activity. Conf. Proc. IEEE Eng. Med. Biol. Soc. 4277-4280.
10. de Curtis, M., Avanzini, G., 2001. Interictal spikes in focal epileptogenesis. Progress in Neurobiology 63, 541-567.
11. de Curtis, M., Radici, C., Forti, M., 1999. Cellular mechanisms underlying spontaneous interictal spikes in a model of focal cortical epileptogenesis. Neuroscience 88, 107-117.
12. Filosa, J.A., Blanco, V.M., 2007. Neurovascular coupling in the mammalian brain. Exp. Physiol. 92 (4), 641-646.
13. Fisher, R.S., 1989. Animal models of the epilepsies. Brain Res. Rev. 14, 245-278.
14. Foucher, J.R., 2001. Synchrony, from cognition to seizure. Epileptic Disord. Spec. Issue 91-98.
15. Gotman, J., Bénar, C.G., Dubeau, F., 2004. Combining EEG and FMRI in epilepsy: methodological challenges and clinical results. J. Clin. Neurophysiol. 21 (4), 229-240.
16. Gotman, J., Kobayashi, E., Bagshaw, A.P., Bénar, C.G., Dubeau, F., 2006. Combining EEG and fMRI: a multimodal tool for epilepsy research. J. Magn. Reson. Imaging 23 (6), 906-920.
17. Gratton et al., 2001. The event-related optical signal (EROS) in visual cortex: replicability, consistency, localization, and resolution.
18. Hamandi, K., Salek-Haddadi, A., Fish, D.R., Lemieux, L., 2004. EEG/functional MRI in epilepsy: The Queen Square Experience. J. Clin. Neurophysiol. 21 (4), 241-248.
19. Hamel, E., 2004. Cholinergic modulation of the cortical microvascular bed. Prog. Brain Res. 145, 171-178.
20. Hamel, E., 2006. Perivascular nerves and the regulation of cerebrovascular tone. J. Appl. Physiol. 100 (3), 1059-1064.
21. Hawco, C.S., Bagshaw, A.P., Lu, Y., Dubeau, F., Gotman, J., 2007. BOLD changes occur prior to epileptic spikes seen on scalp EEG. Neuroimage 35 (4), 1450-1458.
22. Haydon, P.G., Carmignoto, G., 2006. Astrocyte control of synaptic transmission and neurovascular coupling. Physiol. Rev. 86, 1009-1031.
23. Hirase, H., Creso, J., Buzsaki, G., 2004. Capillary level imaging of local cerebral blood ow in bicuculline-induced epileptic foci. Neuroscience 128, 209-216.
24. Hoffman, W.H., Haberly, L.B., 1991. Bursting induced epileptiform EPSPs; in slices of piriform cortex are generated by deep cells. J. Neurosci. 11, 2021-2031.
25. Iadecola, C., Li, J., Ebner, T.J., Xu, X., 1995. Nitric oxide contributes to functional hyperemia in cerebellar cortex. Am. J. Physiol. Regul. Integr. Comp. Physiol. 268, R1153-R1162.
26. Jacobs, J., Kobayashi, E., Boor, R., Muhle, H., Stephan, W., Hawco, C., Dubeau, F., Jansen, O., Stephani, U., Gotman, J., Siniatchkin, M., 2007. Hemodynamic responses to interictal epileptiform discharges in children with symptomatic epilepsy. Epilepsia 48 (11), 2068-2078.
27. Jefferys, J.G.R., 1995. Nonsynaptic modulation of neuronal activity in the brain: electric currents and extracellular ions. Physiol. Rev. 75, 689-723.
28. Jefferys, J.G.R., Haas, H.L., 1982. Synchronized bursting of CA1 pyramidal cells in absence of synaptic transmission. Nature 300, 448-450.
29. Jobsis, F.F., 1977. Noninvasive, infrared monitoring of cerebral and myocardial oxygen sufciency and circulatory parameters. Science 198, 1264-1266.
30. Krakow, K., Woermann, F.G., Symms, M.R., Allen, M.J., Lemieux, L., Barker, G.J., Duncan, J.S., Fish, D.R., 1999. EEG-triggered functional MRI of interictal epileptiform activity in patients with partial seizures. Brain 122 (9), 1679-1688.
31. Kuschinsky, W., Wahl, M., Bosse, O., Thurau, K., 1972. Perivascular potassium and pH as determinants of local pial arterial diameter in cats. A microapplication study. Circ. Res. 31, 240-247.
32. Mäkiranta, M., Ruohonen, J., Suominen, K., Niinimäki, J., Sonkajärvi, E., Kiviniemi, V., Seppänen, T., Alahuhta, S., Jäntti, V., Tervonen, O., 2005. BOLD signal increase precedes EEG spike activity-a dynamic penicillin induced focal epilepsy in deep anesthesia. Neuroimage 27 (4), 715-724.
33. Malonek, D., Dirnagl, U., Lindauer, U., Yamada, K., Kanno, I., Grinvald, A., 1997. Vascular imprints of neuronal activity: relationships between the dynamics of cortical blood ow, oxygenation, and volume changes following sensory stimulation. Proc. Natl. Acad. Sci. U.S.A. 94, 14826-14831.
34. Merlet, I., 2001. Dipole modeling of interictal and ictal EEG and MEG paroxysms. Epileptic Disord. Spec. Issue 11-36.
35. Mulligan, S.J., MacVicar, B.A., 2004. Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature 431, 195-199.
36. Nguyen, T.S., Winn, H.R., Janigro, D., 2000. ATP-sensitive potassium channels may participate in the coupling of neuronal activity and cerebrovascular tone. Am. J. Physiol. Heart Circ. Physiol. 278, H878-H885.
37. Northington, F.J., Matherne, G.P., Berne, R.M., 1992. Competitive inhibition of nitric oxide synthase prevents the cortical hyperemia associated with peripheral nerve stimulation. Proc. Natl. Acad. Sci. U.S.A. 89, 6649-6652.
38. Patterson, M.S., Andersson-Engels, S., Wilson, B.C., Osei, E.K., 1995. Absorption spectroscopy in tissue-simulating materials: a theoretical and experimental study of photon paths. Applied Optics. 34, 22-30.
39. Perez-Velasquez, J.L., Valiante, T.A., Carlen, P.L., 1994. Modulation of gap junctional mechanisms during Ca-free induced field burst activity, a possible role for electrotonic coupling in epileptogenesis. J. Neurosci. 14, 4308-4317.
40. Rinne, T., Gratton, G., Fabiani, M., Cowan, N., Maclin, E., Stinard, A., Sinkkonen, J., Alho, K., Näätänen, R., 1999. Scalp-recorded optical signals make sound processing in the auditory cortex visible? Neuroimage 10 (5), 620-624.
41. Roche-Labarbe, N., Zaaimi, B., Nehlig, A., Berquin, P., Grebe, R. and Wallois, F., 2008. The haemodynamic response measured by NIRS to EEG spike and waves discharges in children. Epilepsia 49, 1871-1880.
42. Roche-Labarbe, N., Zaaimi, B., Nehlig, A., Grebe, R. and Wallois, F., in revision. The haemodynamic response measured by NIRS to EEG spike and waves discharges in a genetic model of absence epilepsy. The GAERS rat. Epilepsia.
43. Schousboe, A., 2003. Role of astrocytes in the maintenance and modulation of glutamatergic and GABAergic neurotransmission. Neurochem. Res. 28 (2), 347-352.
44. Schwartzkroin, P.A., Futamachi, K.J., Noebels, J.L., Prince, D.A., 1975. Transcallosal effects of a cortical epileptiform focus. Brain Res. 99, 59-68.
45. Seeck, M., Lazeyras, F., Michel, C.M., Blanke, O., Gericke, C.A., Ives, J., Delavelle, J., Golay, X., Haenggeli, C.A., de Tribolet, N., Landis, T., 1998. Non-invasive epileptic focus localization using EEG-triggered functional MRI and electromagnetic tomography. Electroenceph. Clin. Neurophysiol. 106, 508-512.
46. Soukupova, S., Mikolasova, R., Kubova, H., Mares, P., 1993. New model of cortical epileptic foci in freely moving developing rats. Epilepsy Res. 15, 27-33.
47. Steinbrink, J., Kohl, M., Obrig, H., Curio, G., Syré, F., Thomas, F., Wabnitz, H., Rinneberg, H., Villringer, A., 2000. Somatosensory evoked fast optical intensity changes detected non-invasively in the adult human head. Neurosci. Lett. 15 (291(2)), 105-108.
48. Steriade, M., Amzica, F., Neckelmann, D., Timofeev, I., 1998a. Spike-wave complexes and fast runs of cortically generated seizures. II: extra and intracellular patterns. J. Neurophysiol. 80, 1456-1479.
49. Steriade, M., Timofeev, I., Durmuller, N., Grenier, F., 1998b. Dynamic properties of corticothalamic neurons and local cortical interneurons generating fast rhythmic (30-40 Hz) spike bursts. J. Neurophysiol. 79, 483-490.
50. Suh, M., Bahar, S., Mehta, A.D., Schwartz, T.H., 2005. Temporal dependence in uncoupling of blood volume and oxygenation during interictal epileptiform events in rat neocortex. J. Neurosci. 25 (1), 68-77.
51. Szente, M.B., Boda, B., 1994. Cellular mechanisms of neocortical secondary epileptogenesis. Brain Res. 648, 203-214.
52. Taylor, C.P., Dudek, F.E., 1982. Synchronous neural afterdischarges in the rat hippocampal slices without active chemical synapses. Science 218, 810-812.
53. Tsacopoulos, M., 2002. Metabolic signaling between neurons and glial cells: a short review. J. Physiol. 96 (3-4), 283-288.
54. Warach, S., Ives, J.R., Schlaug, G., Patel, M.R., Darby, D.G., Thangaraj, V., Edelman, R.R., Schomer, D.L., 1996. EEG-triggered echo-planar functional MRI in epilepsy. Neurology 47, 89-93.
55. Valiante, T.A., Perez-Velasquez, J.L., Jahromi, S.S., Carlen, P.L., 1995. Coupling potentials in CA1 neurons during calcium-free-induced field bursts. J. Neurosci. 15, 6946-6958.
56. Vernieri, F., Tibuzzi, F., Pasqualetti, P., Rosato, N., Passarelli, F., Rossini, P.M., Silvestrini, M., 2004. Transcranial Doppler and near-infrared spectroscopy can evaluate the hemodynamic effect of carotid artery occlusion. Stroke 35 (1), 64-70.
57. Vulliemoz, S., Thornton, R., Rodionov, R., Carmichael, D.W., Guye, M., Lhatoo, S., McEvoy, A.W., Spinelli, L., Michel, C.M., Duncan, J.S., Lemieux, L., 2009. The spatio-temporal mapping of epileptic networks: combination of EEG-fMRI and EEG source imaging. NeuroImage 46 (3), 834-843.