Hippocampal functional hyperemia mediated by NMDA receptor/NO signaling in rats during mild exercise

Journal of Applied Physiology

Volumn 112, Issue 1, 2012, Pages 197-203

  Nishijima, Takeshi ^a,b   Okamoto, Masahiro ^a   Matsui, Takashi ^a   Kita, Ichiro ^b   Soya, Hideaki ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b TOKYO METROPOLITAN UNIVERSITY   (Japan)

Author keywords

Cerebral blood flow; Hippocampus; Laser Doppler flowmetry; Microdialysis; Running

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NITRIC OXIDE;

ANIMAL; ANIMAL EXPERIMENT; ARTICLE; BRAIN CIRCULATION; HIPPOCAMPUS; HYPEREMIA; MALE; METHODOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RAT; SIGNAL TRANSDUCTION; WISTAR RAT;

ANIMALS; CEREBROVASCULAR CIRCULATION; HIPPOCAMPUS; HYPEREMIA; MALE; NITRIC OXIDE; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION;

EID: 84855387558     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00763.2011     Document Type: Article

References (51)

1. Akgoren N, Fabricius M, Lauritzen M. Importance of nitric oxide for local increases of blood flow in rat cerebellar cortex during electrical stimulation. Proc Natl Acad Sci U S A 91: 5903-5907, 1994. (Pubitemid 24188250)
2. Anderson CM, Nedergaard M. Astrocyte-mediated control of cerebral microcirculation. Trends Neurosci 26: 340-344; author reply 344-345, 2003. (Pubitemid 36794547)
3. Bhardwaj A, Northington FJ, Ichord RN, Hanley DF, Traystman RJ, Koehler RC. Characterization of ionotropic glutamate receptor-mediated nitric oxide production in vivo in rats. Stroke 28: 850-856; discussion 856-857, 1997.
4. Borgos J. Laser Doppler monitoring of cerebral blood flow. Neurol Res 18: 251-255, 1996. (Pubitemid 26323667)
5. Carro E, Nunez A, Busiguina S, Torres-Aleman I. Circulating insulinlike growth factor I mediates effects of exercise on the brain. J Neurosci 20: 2926-2933, 2000. (Pubitemid 30220318)
6. Chi OZ, Liu X, Weiss HR. Effects of inhibition of neuronal nitric oxide synthase on NMDA-induced changes in cerebral blood flow and oxygen consumption. Exp Brain Res 148: 256-260, 2003. (Pubitemid 36057013)
7. Choi SH, Li Y, Parada LF, Sisodia SS. Regulation of hippocampal progenitor cell survival, proliferation and dendritic development by BDNF. Mol Neurodegener 4: 52, 2009.
8. Cotman CW, Berchtold NC. Exercise: A behavioral intervention to enhance brain health and plasticity. Trends Neurosci 25: 295-301, 2002. (Pubitemid 34667010)
9. Cotman CW, Berchtold NC, Christie LA. Exercise builds brain health: Key roles of growth factor cascades and inflammation. Trends Neurosci 30: 464-472, 2007. (Pubitemid 47374831)
10. de Novellis V, Marabese I, Uliano R, Palazzo E, Scafuro A, sca Rossi F, Maione S. Type I and II metabotropic glutamate receptors modulate periaqueductal grey glycine release: Interaction between mGlu2/3 and A1 adenosine receptors. Neuropharmacology 43: 1061-1069, 2002. (Pubitemid 36009358)
11. Delp MD, Armstrong RB, Godfrey DA, Laughlin MH, Ross CD, Wilkerson MK. Exercise increases blood flow to locomotor, vestibular, cardiorespiratory and visual regions of the brain in miniature swine. J Physiol 533: 849-859, 2001. (Pubitemid 32600538)
12. Dishman RK, Berthoud HR, Booth FW, Cotman CW, Edgerton VR, Fleshner MR, Gandevia SC, Gomez-Pinilla F, Greenwood BN, Hillman CH, Kramer AF, Levin BE, Moran TH, Russo-Neustadt AA, Salamone JD, Van Hoomissen JD, Wade CE, York DA, Zigmond MJ. Neurobiology of exercise. Obesity (Silver Spring) 14: 345-356, 2006. (Pubitemid 46219751)
13. Faraci FM, Breese KR. Nitric oxide mediates vasodilatation in response to activation of N-methyl-D-Aspartate receptors in brain. Circ Res 72: 476-480, 1993. (Pubitemid 23024535)
14. Fergus A, Lee KS. Regulation of cerebral microvessels by glutamatergic mechanisms. Brain Res 754: 35-45, 1997. (Pubitemid 27170249)
15. Florence G, Seylaz J. Rapid autoregulation of cerebral blood flow: A laser-Doppler flowmetry study. J Cereb Blood Flow Metab 12: 674-680, 1992.
16. Girouard H, Iadecola C. Neurovascular coupling in the normal brain and in hypertension, stroke, and Alzheimer disease. J Appl Physiol 100: 328-335, 2006. (Pubitemid 43671125)
17. Gross PM, Marcus ML, Heistad DD. Regional distribution of cerebral blood flow during exercise in dogs. J Appl Physiol 48: 213-217, 1980. (Pubitemid 10139161)
18. Gu W, Jiang W, Wester P. Real-time cortical cerebral blood flow follow-up in conscious, freely moving rats by laser Doppler flowmetry. Methods 30: 172-177, 2003. (Pubitemid 36506564)
19. Haberl RL, Heizer ML, Ellis EF. Laser-Doppler assessment of brain microcirculation: Effect of local alterations. Am J Physiol Heart Circ Physiol 256: H1255-H1260, 1989.
20. Jorgensen LG, Perko G, Payne G, Secher NH. Effect of limb anesthesia on middle cerebral response to handgrip. Am J Physiol Heart Circ Physiol 264: H553-H559, 1993. (Pubitemid 23081132)
21. Kaiser MG, During MJ. Combining laser Doppler flowmetry with microdialysis: A novel approach to investigate the coupling of regional cerebral blood flow to neuronal activity. J Neurosci Methods 60: 165-173, 1995.
22. Kitamura T, Mishina M, Sugiyama H. Enhancement of neurogenesis by running wheel exercises is suppressed in mice lacking NMDA receptor epsilon 1 subunit. Neurosci Res 47: 55-63, 2003. (Pubitemid 36993875)
23. Kojda G, Hambrecht R. Molecular mechanisms of vascular adaptations to exercise. Physical activity as an effective antioxidant therapy? Cardiovasc Res 67: 187-197, 2005. (Pubitemid 40943611)
24. Lange-Asschenfeldt C, Kojda G. Alzheimer's disease, cerebrovascular dysfunction and the benefits of exercise: From vessels to neurons. Exp Gerontol 43: 499-504, 2008.
25. Linkis P, Jorgensen LG, Olesen HL, Madsen PL, Lassen NA, Secher NH. Dynamic exercise enhances regional cerebral artery mean flow velocity. J Appl Physiol 78: 12-16, 1995.
26. Lopez-Lopez C, LeRoith D, Torres-Aleman I. Insulin-like growth factor I is required for vessel remodeling in the adult brain. Proc Natl Acad Sci U S A 101: 9833-9838, 2004. (Pubitemid 38869322)
27. Lujan R, Nusser Z, Roberts JD, Shigemoto R, Somogyi P. Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus. Eur J Neurosci 8: 1488-1500, 1996.
28. Maejima T, Hashimoto K, Yoshida T, Aiba A, Kano M. Presynaptic inhibition caused by retrograde signal from metabotropic glutamate to cannabinoid receptors. Neuron 31: 463-475, 2001. (Pubitemid 32778564)
29. Manzoni O, Bockaert J. Metabotropic glutamate receptors inhibiting excitatory synapses in the CA1 area of rat hippocampus. Eur J Neurosci 7: 2518-2523, 1995.
30. Masuki S, Nose H. Increased cerebral activity suppresses baroreflex control of heart rate in freely moving mice. J Physiol 587: 5783-5794, 2009.
31. Meng W, Tobin JR, Busija DW. Glutamate-induced cerebral vasodilation is mediated by nitric oxide through N-methyl-D-Aspartate receptors. Stroke 26: 857-862; discussion 863, 1995.
32. Nakajima K, Uchida S, Suzuki A, Hotta H, Aikawa Y. The effect of walking on regional blood flow and acetylcholine in the hippocampus in conscious rats. Auton Neurosci 103: 83-92, 2003. (Pubitemid 36057156)
33. Naylor AS, Persson AI, Eriksson PS, Jonsdottir IH, Thorlin T. Extended voluntary running inhibits exercise-induced adult hippocampal progenitor proliferation in the spontaneously hypertensive rat. J Neurophysiol 93: 2406-2414, 2005. (Pubitemid 40570827)
34. Nishijima T, Piriz J, Duflot S, Fernandez AM, Gaitan G, Gomez- Pinedo U, Verdugo JM, Leroy F, Soya H, Nunez A, Torres-Aleman I. Neuronal activity drives localized blood-brain-barrier transport of serum insulin-like growth factor-I into the CNS. Neuron 67: 834-846, 2010.
35. Nishijima T, Soya H. Evidence of functional hyperemia in the rat hippocampus during mild treadmill running. Neurosci Res 54: 186-191, 2006. (Pubitemid 43276076)
36. Nishijima T, Soya H. Hemodynamics under hippocampal functional hyperemia in anesthetized rat: A greater contribution of red blood cell velocity compared to its concentration. Jpn J Physiol 55: 303-307, 2005.
37. Ogoh S, Ainslie PN. Cerebral blood flow during exercise: Mechanisms of regulation. J Appl Physiol 107: 1370-1380, 2009.
38. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. San Diego, CA: Academic, 1998.
39. Pelligrino DA, Gay RL 3rd, Baughman VL, Wang Q. NO synthase inhibition modulates NMDA-induced changes in cerebral blood flow and EEG activity. Am J Physiol Heart Circ Physiol 271: H990-H995, 1996.
40. Querido JS, Sheel AW. Regulation of cerebral blood flow during exercise. Sports Med 37: 765-782, 2007. (Pubitemid 47347391)
41. Schmidt-Kastner R, Freund TF. Selective vulnerability of the hippocampus in brain ischemia. Neuroscience 40: 599-636, 1991.
42. Secher NH, Seifert T, Van Lieshout JJ. Cerebral blood flow and metabolism during exercise: Implications for fatigue. J Appl Physiol 104: 306-314, 2008.
43. Sokoloff L. Relationships among local functional activity, energy metabolism, and blood flow in the central nervous system. Fed Proc 40: 2311-2316, 1981. (Pubitemid 11036104)
44. Soya H, Mukai A, Deocaris CC, Ohiwa N, Chang H, Nishijima T, Fujikawa T, Togashi K, Saito T. Threshold-like pattern of neuronal activation in the hypothalamus during treadmill running: Establishment of a minimum running stress (MRS) rat model. Neurosci Res 58: 341-348, 2007. (Pubitemid 47198907)
45. Soya H, Nakamura T, Deocaris CC, Kimpara A, Iimura M, Fujikawa T, Chang H, McEwen BS, Nishijima T. BDNF induction with mild exercise in the rat hippocampus. Biochem Biophys Res Commun 358: 961-967, 2007. (Pubitemid 46828982)
46. Springer JE, Gwag BJ, Sessler FM. Neurotrophic factor mRNA expression in dentate gyrus is increased following in vivo stimulation of the angular bundle. Brain Res Mol Brain Res 23: 135-143, 1994. (Pubitemid 24090990)
47. van Praag H, Christie BR, Sejnowski TJ, Gage FH. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci U S A 96: 13427-13431, 1999.
48. van Praag H, Shubert T, Zhao C, Gage FH. Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 25: 8680-8685, 2005. (Pubitemid 41362045)
49. Wilson RI, Nicoll RA. Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410: 588-592, 2001. (Pubitemid 32267203)
50. Yang G, Iadecola C. Activation of cerebellar climbing fibers increases cerebellar blood flow: Role of glutamate receptors, nitric oxide, and cGMP. Stroke 29: 499-508, 1998. (Pubitemid 28086698)
51. Zonta M, Angulo MC, Gobbo S, Rosengarten B, Hossmann KA, Pozzan T, Carmignoto G. Neuron-to-Astrocyte signaling is central to the dynamic control of brain microcirculation. Nat Neurosci 6: 43-50, 2003. (Pubitemid 36026331)