N-methyl-D-aspartate induces cortical hyperemia through cortical spreading depression-dependent and -independent mechanisms in rats

Microcirculation

Volumn 16, Issue 7, 2009, Pages 929-639

  Lenti, Laura ^a,b   Domoki, Ferenc ^a,b   Gáspár, Tamás ^a   Snipes, James A ^a   Bari, Ferenc ^b   Busija, David W ^a  

^a WAKE FOREST UNIVERSITY HEALTH SCIENCES   (United States)

^b UNIVERSITY OF SZEGED   (Hungary)

Author keywords

AMPA; cerebral blood flow; glutamate; kainate; laser Doppler flowmetry; piglet

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID; N METHYLASPARTIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIAL CARBON DIOXIDE TENSION; ARTERIAL OXYGEN TENSION; ARTERIAL PRESSURE; ARTICLE; BRAIN BLOOD FLOW; CEREBROVASCULAR DISEASE; CONTROLLED STUDY; CORTICAL HYPEREMIA; END TIDAL CARBON DIOXIDE TENSION; EXPERIMENTAL PIG; HYPEREMIA; LASER DOPPLER FLOWMETRY; MALE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; RECTUM TEMPERATURE; SPREADING CORTICAL DEPRESSION; ANIMAL; BLOOD FLOW; BRAIN CIRCULATION; BRAIN CORTEX; CHEMICALLY INDUCED DISORDER; DOSE RESPONSE; PHYSIOLOGY; VASCULARIZATION; WISTAR RAT;

MUS; RATTUS; RATTUS NORVEGICUS;

ANIMALS; CEREBRAL CORTEX; CEREBROVASCULAR CIRCULATION; CORTICAL SPREADING DEPRESSION; DOSE-RESPONSE RELATIONSHIP, DRUG; HYPEREMIA; N-METHYLASPARTATE; RATS; RATS, WISTAR; REGIONAL BLOOD FLOW;

EID: 79952108636     PISSN: 10739688     EISSN: 15498719     Source Type: Journal    
DOI: 10.1080/10739680903131510     Document Type: Article

References (45)

1. Addae.JI. Evans SM, Ali N, Stone TW (2000). NMDA-induced changes in a cortical network in vivo are prevented by AMPA. Brain Res 869: 211-215.
2. Ayata C, Moskowitz MA. (2006). Cortical spreading depression confounds concentration-dependent pial arteriolar dilation during N-methyl-D-aspartate superfusion. Am J Physiol Heart Circ Physiol 290:H1837-H1841.
3. Bari F, Errico RA, Louis TM, Busija DW. (1996). Differential effects of short-term hypoxia and hypercapnia on N-methyl-D-aspartate-induced cerebral vasodilatation in piglets. Stroke 27:1634-1639; discussion, 1639-1640.
4. +channels and nitric oxide on pial arterioles in piglets. J Cereb Blood Flow Metab 16:1158-1164.
5. Bari F, Louis TM, Busija DW (1997). Kainate-induced cerebrovascular dilation is resistant to ischemia in piglets. Stroke 28:1272-1276; discussion, 1277.
6. Bari F, Nagy K, Guidetti P, Schwarcz R, Busija DW, Domoki F. (2006). Kynurenic acid attenuates NMDA-induced pial arteriolar dilation in newborn pigs. Brain Res 1069:39-46.
7. Busija DW, Bari F, Domoki F, Horiguchi T, Shimizu K. (2008). Mechanisms involved in the cerebrovascular dilator effects of cortical spreading depression. Prog Neurobiol 86:379-395.
8. Busija DW, Bari F, Domoki F, Louis T. (2007). Mechanisms involved in the cerebrovascular dilator effects of N-methyl-D-aspartate in cerebral cortex. Brain Res Rev 56:89-100.
9. Busija DW, Heistad DD, Marcus ML. (1981). Continuous measurement of cerebral blood flow in anesthetized cats and dogs. Am J Physiol 241:H228-H234.
10. Busija DW, Leffler CW. (1989). Dilator effects of amino-acid neurotransmitters on piglet pial arterioles. Am J Physiol 257:H1200-H1203.
11. Busija DW, Marcus ML, Heistad DD. (1982). Pial artery diameter and blood-flow velocity during sympathetic stimulation in cats. J Cereb Blood Flow Metab 2:363-367.
12. Busija DW, Wei M. (1993). Altered cerebrovascular responsiveness to N-methyl-D-aspartate after asphyxia in piglets. Am J Physiol 265:H389-H394.
13. Clements.D, Lester RA, Tong G, Jahr CE, Westbrook GL. (1992). The time course of glutamate in the synaptic cleft. Science 258:1498-1501.
14. Domoki F, Perciaccante JV, Shimizu K, Puskar M, Busija DW, Bari F. (2002). N-methyl-D-aspartate-induced vasodilation is mediated by endothelium-independent nitric oxide release in piglets. Am J Physiol Heart Circ Physiol 282:H1404-H1409.
15. Domoki F, Veltkamp R, Bari F, Louis TM, Busija DW. (1999). Cerebrovascular reactivity remains intact after cortical depolarization in newborn piglets. Pediatr Res 45:834-837.
16. Faraci FM, Breese KR. (1993). Nitric oxide mediates vasodilatation in response to activation of N-methyl-D-aspartate receptors in brain. Circ Res 72:476-480.
17. Faraci FM, Breese KR. (1994). Dilatation of cerebral arterioles in response to N-methyl-D-aspartate: role of CGRP and acetylcholine. Brain Res 640: 93-97.
18. Faraci FM, Brian.E,.r. (1995) 7-nitroindazole inhibits brain nitric oxide synthase and cerebral vasodilatation in response to N-methyl-D-aspartate. Stroke 26:2172-2175; discussion, 2176.
19. Faraci FM, Heistad DD. (1994). Responses of cerebral arterioles to N-methyl-D-aspartate and activation of ATP-sensitive potassium channels in old rats. Brain Res 654:349-351.
20. Farkas E, Pratt R, Sengpiel F, Obrenovitch TP. (2008). Direct, live imaging of cortical spreading depression and anoxic depolarisation using a fluorescent, voltage-sensitive dye. J Cereb Blood Flow Metab 28:251-262.
21. Fergus A, Lee KS. (1997). Regulation of cerebral microvessels by glutamatergic mechanisms. Brain Res 754:35-45.
22. Gill R, Andine P, Hillered L, Persson L, Hagberg H. (1992). The effect of MK-801 on cortical spreading depression in the penumbral zone following focal ischaemia in the rat. J Cereb Blood Flow Metab 12:371-379.
23. Girouard H, Wang G, Gallo EF, Anrather J, Zhou P, Pickel VM, et al. (2009). NMDA-receptor activation increases free radical production through nitric oxide and NOX2. J Neurosci 29:2545-2552.
24. Hardebo JE, Wieloch T, Kahrstrom J. (1989). Excitatory amino acids and cerebrovascular tone. Acta Physiol Scand 136:483-485.
25. Iliff JJ, D'Ambrosio R, Ngai AC, Winn HR. (2003). Adenosine receptors mediate glutamate-evoked arteriolar dilation in the rat cerebral cortex. Am J Physiol Heart Circ Physiol 284:H1631-H1637.
26. Kitahara Y, Taga K, Abe H, Shimoji K. (2001). The effects of anesthetics on cortical spreading depression elicitation and c-fos expression in rats. J Neurosurg Anesthesiol 13:26-32.
27. Koehler RC, Roman RJ, Harder DR. (2009). Astrocytes and the regulation of cerebral blood flow. Trends Neurosci 32:160-169.
28. Kudo C, Nozari A, Moskowitz MA, Ayata C. (2008). The impact of anesthetics and hyperoxia on cortical spreading depression. Exp Neurol 212:201-206.
29. Lauritzen M, Hansen AJ. (1992). The effect of glutamate receptor blockade on anoxic depolarization and cortical spreading depression. J Cereb Blood Flow Metab 12:223-229.
30. Leffler CW, Parfenova H, Fedinec AL, Basuroy S, Tcheranova D. (2006). Contributions of astrocytes and CO to pial arteriolar dilation to glutamate in newborn pigs. Am J Physiol Heart Circ Physiol 291:H2897-H2904.
31. Marrannes R, Willems R, De Prins E, Wauquier A. (1988). Evidence for a role of the N-methyl-D-aspartate (NMDA) receptor in cortical spreading depression in the rat. Brain Res 457:226-240.
32. Meng W, Tobin JR, Busija DW. (1995). Glutamate-induced cerebral vasodilation is mediated by nitric oxide through N-methyl-D-aspartate receptors. Stroke 26:857-862; discussion, 863.
33. Obrenovitch TP, Zilkha E, Urenjak J. (1996). Evidence against high extracellular glutamate promoting the elicitation of spreading depression by potassium. J Cereb Blood Flow Metab 16:923-931.
34. Pellerin L, Magistretti PJ. (1994). Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci U S A 91:10625-10629.
35. Pelligrino DA, Gay RL, 3rd, Baughman VL, Wang Q. (1996). NO synthase inhibition modulates NMDA-induced changes in cerebral blood flow and EEG activity. Am J Physiol 271:H990-H995.
36. Philip S, Armstead WM. (2004). NMDA dilates pial arteries by KATP and Kca channel activation. Brain Res Bull 63:127-131.
37. Richter F, Bauer R, Lehmenkuhler A, Schaible HG. (2008). Spreading depression in the brainstem of the adult rat: electrophysiological parameters and influences on regional brainstem blood flow. J Cereb Blood Flow Metab 28:984-994.
38. Richter F, Lehmenkuhler A, Fechner R, Manveljan L, Haschke W. (1998). Postnatal conditioning for spreading cortical depression in the rat brain. Brain Res Dev Brain Res 106:217-221.
39. Schade JP. (1959). Maturational aspects of EEG and of spreading depression in rabbit. J Neurophysiol 22:245-257.
40. Shibata M, Leffler CW, Busija DW. (1991). Prostanoids attenuate pial arteriolar dilation induced by cortical spreading depression in rabbits. Am J Physiol 261:R828-R834.
41. Simandle SA, Kerr BA, Lacza Z, Eckman DM, Busija DW, Bari F. (2005). Piglet pial arteries respond to N-methyl-D-aspartate in vivo but not in vitro. Micro-vasc Res 70:76-83.
42. Takahashi T. (2005). Postsynaptic receptor mechanisms underlying developmental speeding of synaptic transmission. Neurosci Res 53:229-240.
43. Van Harreveld A, Stamm JS, Christensen E. (1956). Spreading depression in rabbit, cat, and monkey. Am J Physiol 184:312-320.
44. Yang ST, Chang HH. (1998). Nitric oxide of neuronal origin mediates NMDA-induced cerebral hyperemia in rats. Neuroreport 9:415-418.
45. Zonta M, Angulo MC, Gobbo S, Rosengarten B, Hossmann KA, Pozzan T, et al. (2003). Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat Neurosci 6:43-50.