Preictal and ictal neurovascular and metabolic coupling surrounding a seizure focus

Journal of Neuroscience

Volumn 31, Issue 37, 2011, Pages 13292-13300

  Zhao, Mingrui ^a   Nguyen, John ^b   Ma, Hongtao ^a   Nishimura, Nozomi ^b   Schaffer, Chris B ^b   Schwartz, Theodore H ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b School of Operations Research and Industrial Engineering   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOPYRIDINE; FLAVOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOFLUORESCENCE FLAVOPROTEIN IMAGING; AUTOFLUORESCENCE IMAGING; BLOOD OXYGENATION; BLOOD VESSEL DIAMETER; BRAIN BLOOD VOLUME; BRAIN MAPPING; BRAIN METABOLISM; BRAIN OXYGEN CONSUMPTION; CELL SWELLING; CONTROLLED STUDY; EPILEPTIC FOCUS; EPILEPTOGENESIS; IMAGING; LIGHT SCATTERING; MALE; NONHUMAN; OPTICAL IMAGING; PRIORITY JOURNAL; RAT; SEIZURE; TWO PHOTON IMAGING; VASOCONSTRICTION;

4-AMINOPYRIDINE; ANIMALS; BLOOD VOLUME; CEREBRAL CORTEX; CEREBROVASCULAR CIRCULATION; DISEASE MODELS, ANIMAL; ELECTROENCEPHALOGRAPHY; MALE; OXIDATION-REDUCTION; RATS; RATS, SPRAGUE-DAWLEY; SEIZURES; VASOCONSTRICTION;

EID: 80052943080     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2597-11.2011     Document Type: Article

References (54)

1. Bragin A, Mody I, Wilson CL, Engel J Jr (2002) Local generation of fast ripples in epileptic brain. J Neurosci 22:2012-2021.
2. Bruehl C, Witte OW (1995) Cellular activity underlying altered brain metabolism during focal epileptic activity. Ann Neurol 38:414-420.
3. Chance B, Schoener B, Oshino R, Itshak F, Nakase Y (1979) Oxidation-reduction ratio studies of mitochondria in freeze-trapped samples. NADH and flavoprotein fluorescence signals. J Biol Chem 254:4764- 4771.
4. Derdikman D, Hildesheim R, Ahissar E, Arieli A, Grinvald A (2003) Imaging spatiotemporal dynamics of surround inhibition in the barrels so-matosensory cortex. J Neurosci 23:3100-3105.
5. Devor A, Tian P, Nishimura N, Teng IC, Hillman EM, Narayanan SN, Ulbert I, Boas DA, Kleinfeld D, Dale AM (2007) Suppressed neuronal activity and concurrent arteriolar vasoconstriction may explain negative blood oxygenation level-dependent signal. J Neurosci 27:4452-4459.
6. Diehl B, Knecht S, Deppe M, Young C, Stodieck SR (1998) Cerebral hemo-dynamic response to generalized spike-wave discharges. Epilepsia 39: 1284-1289.
7. Engel J Jr, Kuhl DE, Phelps ME (1982) Patterns of human local cerebral glucose metabolism during epileptic seizures. Science 218:64-66.
8. Filosa JA, Bonev AD, Straub SV, Meredith AL, Wilkerson MK, Aldrich RW, Nelson MT (2006) Local potassium signaling couples neuronal activity to vasodilation in the brain. Nat Neurosci 9:1397-1403.
9. Folbergrova ́ J, Ingvar M, Siesjo BK (1981) Metabolic changes in cerebral cortex, hippocampus, and cerebellum during sustained bicuculline-induced seizures. J Neurochem 37:1228-1238.
10. Franck G, Sadzot B.Regional cerebral blood flow and metabolic rates in human focal epilepsy and status epilepticus. Adv Neurol 44:935-948.
11. Gibbs FA (1933) Cerebral blood flow preceding and accompanying experimental convulsions Arch Neurol Psychiat Chicago 30:1003-1010.
12. Gjedde A (2006) Blood-Brain Transfer and Metabolism of Oxygen. In: Blood-brain barriers: from ontogeny to artificial interfaces (Dermietzel R, Spray DC, Nedergaard M, eds), pp 2 v. (xxxii, 741 p.). Weinheim: Wiley-VCH.
13. Hamel E (2006) Perivascular nerves and the regulation of cerebrovascular tone. J Appl Physiol 100:1059-1064.
14. Hawco CS, Bagshaw AP, Lu Y, Dubeau F, Gotman J (2007) BOLD changes occur prior to epileptic spikes seen on scalp EEG. Neuroimage 35:1450-1458.
15. Hirase H, Creso J, Buzsaki G (2004a) Capillary level imaging of local cerebral blood flow in bicuculline-induced epileptic foci. Neuroscience 128:209-216.
16. Hirase H, Qian L, Bartho ́ P, Buzsaki G (2004b) Calcium dynamics of cortical astrocytic networks in vivo. PLoS Biol 2:E96.
17. Hoshi Y, Tamura M (1992) Cerebral oxygenation state in chemically-induced seizures in the rat-study by near infrared spectrophotometry. Adv Exp Med Biol 316:137-142.
18. Husson TR, Mallik AK, Zhang JX, Issa NP (2007) Functional imaging of primary visual cortex using flavoprotein autofluorescence. J Neurosci 27:8665-8675.
19. Iadecola C, Nedergaard M (2007) Glial regulation of the cerebral microvas-culature. Nat Neurosci 10:1369-1376.
20. Iadecola C.(1997) Local and propagated vascular responses evoked by focal synaptic activity in cerebellar cortex. J Neuro-physiol 78:651-659.
21. Ingvar M (1986) Cerebral blood flow and metabolic rate during seizures. Relationship to epileptic brain damage. Ann N Y Acad Sci 462:194-206.
22. Kasischke KA, Vishwasrao HD, Fisher PJ, Zipfel WR, Webb WW (2004) Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis. Science 305:99-103.
23. Kobayashi E, Hawco CS, Grova C, Dubeau F, Gotman J (2006) Widespread and intense BOLD changes during brief focal electrographic seizures. Neurology 66:1049-1055.
24. Kreisman NR, Magee JC, Brizzee BL (1991) Relative hypoperfusion in rat cerebral cortex during recurrent seizures. J Cereb Blood Flow Metab 11:77-87.
25. Litt B, Esteller R, Echauz J, D'Alessandro M, Shor R, Henry T, Pennell P, Epstein C, Bakay R, Dichter M, Vachtsevanos G (2001) Epileptic seizures may begin hours in advance of clinical onset: a report of five patients. Neuron 30:51-64.
26. Llano DA, Theyel BB, Mallik AK, Sherman SM, Issa NP (2009) Rapid and sensitive mapping of long-range connections in vitro using flavoprotein autofluorescence imaging combined with laser photostimulation. J Neu-rophysiol 101:3325-3340.
27. Makiranta M, Ruohonen J, Suominen K, Niinimaki J, Sonkajarvi E, Kiviniemi V, Seppanen T, Alahuhta S, Jantti V, Tervonen O (2005) BOLD signal increase preceeds EEG spike activity-a dynamic penicillin induced focal epilepsy in deep anesthesia. Neuroimage 27:715-724.
28. Masamoto K, Omura T, Takizawa N, Kobayashi H, Katura T, Maki A, Kawa-guchi H, Tanishita K (2003) Biphasic changes in tissue partial pressure of oxygen closely related tolocalized neural activityin guinea pig auditory cortex. J Cereb Blood Flow Metab 23:1075-1084.
29. Moore CI, Cao R (2008) The hemo-neural hypothesis: on the role of blood flow in information processing. J Neurophysiol 99:2035-2047.
30. Motamedi GK, Salazar P, Smith EL, Lesser RP, Webber WR, Ortinski PI, Vicini S, Rogawski MA (2006) Termination of epileptiform activity by cooling in rat hippocampal slice epilepsy models. Epilepsy Res 70:200- 210.
31. Nguyen QT, Tsai PS, Kleinfeld D (2006) MPScope: a versatile software suite for multiphoton microscopy. J Neurosci Methods 156:351-359.
32. Offenhauser N, Thomsen K, Caesar K, Lauritzen M (2005) Activity-induced tissue oxygenation changes in rat cerebellar cortex: interplay of postsyn-aptic activation and blood flow. J Physiol 565:279-294.
33. Peppiatt CM, Howarth C, Mobbs P, Attwell D (2006) Bidirectional control of CNS capillary diameter by pericytes. Nature 443:700-704.
34. Prince DA, Wilder BJ (1967) Control mechanisms in cortical epileptogenic foci. "Surround" inhibition. Arch Neurol 16:194-202.
35. Raichle ME, Mintun MA (2006) Brain work and brain imaging. Annu Rev Neurosci 29:449-476.
36. Reinert KC, Gao W, Chen G, Ebner TJ (2007) Flavoprotein autofluorescence imaging in the cerebellar cortex in vivo. J Neurosci Res 85:3221-3232.
37. Rensing N, Ouyang Y, Yang XF, Yamada KA, Rothman SM, Wong M (2005) In vivo imaging of dendritic spines during electrographic seizures. Ann Neurol 58:888-898.
38. Roche-Labarbe N, Zaaimi B, Berquin P, Nehlig A, Grebe R, Wallois F (2008) NIRS-measured oxy- and deoxyhemoglobin changes associated with EEG spike-and-wave discharges in children. Epilepsia 49:1871-1880.
39. Salzberg BM, Obaid AL, Gainer H (1985) Large and rapid changes in light scattering accompany secretion by nerve terminals in the mammalian neurohypophysis. J Gen Physiol 86:395-411.
40. Schwartz TH, Bonhoeffer T (2001) In vivo optical mapping of epileptic foci and surround inhibition in ferret cerebral cortex. Nat Med 7:1063-1067.
41. Shibuki K, Hishida R, Murakami H, Kudoh M, Kawaguchi T, Watanabe M, Watanabe S, Kouuchi T, Tanaka R (2003) Dynamic imaging of somatosensory cortical activity in the rat visualized by flavoprotein autofluores-cence. J Physiol 549:919-927.
42. Shmuel A, Augath M, Oeltermann A, Logothetis NK (2006) Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1. NatNeurosci 9:569-577.
43. Sirotin YB, Das A (2009) Anticipatory haemodynamic signals in sensory cortex not predicted by local neuronal activity. Nature 457:475-479.
44. Sirotin YB, Das A (2010) Spatial Relationship between Flavoprotein Fluorescence and the Hemodynamic Response in the Primary Visual Cortex of Alert Macaque Monkeys. Front Neuroenergetics 2:6.
45. Skarphedinsson JO, Hårding H, Thoren P (1988) Repeated measurements of cerebral blood flow in rats. Comparison between hydrogen clearance method and laser Doppler Flowmetry. Acta Physiol Scand 134:133-142.
46. Takao T, Murakami H, Fukuda M, Kawaguchi T, Kakita A, Takahashi H, Kudoh M, Tanaka R, Shibuki K (2006) Transcranial imaging of audiogenic epileptic foci in the cortex of DBA/2J mice. Neuroreport 17: 267-271.
47. Thomsen K, Piilgaard H, Gjedde A, Bonvento G, Lauritzen M (2009) Principal cell spiking, postsynaptic excitation, and oxygen consumption in the rat cerebellar cortex. J Neurophysiol 102:1503-1512.
48. Trevelyan AJ, Sussillo D, Yuste R (2007) Feedforward inhibition contributes to the control of epileptiform propagation speed. J Neurosci 27:3383-3387.
49. Truccolo W, Donoghue JA, Hochberg LR, Eskandar EN, Madsen JR, Anderson WS, Brown EN, Halgren E, Cash SS (2011) Single-neuron dynamics in human focal epilepsy. Nat Neurosci 14:635-641.
50. Wang X, Lou N, Xu Q, Tian GF, Peng WG, Han X, Kang J, Takano T, Nedergaard M (2006) Astrocytic Ca2+ signaling evoked by sensory stimulation in vivo. NatNeurosci 9:816-823.
51. Xu L, Rensing N, Yang XF, Zhang HX, Thio LL, Rothman SM, Weisenfeld AE, Wong M, Yamada KA (2008) Leptin inhibits 4-aminopyridine- and pentylenetetrazole-induced seizures and AMPAR-mediated synaptic transmission in rodents. J Clin Invest 118:272-280.
52. Zhao M, Suh M, Ma H, Perry C, Geneslaw A, Schwartz TH (2007) Focal increases in perfusion and decreases in hemoglobin oxygenation precede seizure onset in spontaneous human epilepsy. Epilepsia 48:2059-2067.
53. Zhao M, Ma H, Suh M, Schwartz TH (2009) Spatiotemporal dynamics of perfusion and oximetry during ictal discharges in the rat neocortex. J Neurosci 29:2814-2823.
54. Zhu XH, Zhang Y, Tian RX, Lei H, Zhang N, Zhang X, Merkle H, Ugurbil K, Chen W (2002) Development of (17)ONMR approach for fast imaging of cerebral metabolic rate of oxygen in rat brain at high field. Proc Natl Acad Sci U S A 99:13194-13199.