Alpha-linolenic acid given as enteral or parenteral nutritional intervention against sensorimotor and cognitive deficits in a mouse model of ischemic stroke

Neuropharmacology

Volumn 108, Issue , 2016, Pages 60-72

  Bourourou, Miled ^a,b   Heurteaux, Catherine ^a,b   Blondeau, Nicolas ^a,b  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

^b INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

Disease modifiers; Neuroprotection; Nutraceutical; Nutrition; Polyunsaturated fatty acids; Stroke outcome and recovery

Indexed keywords

LINOLENIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CELL SURVIVAL; COGNITIVE DEFECT; CONTROLLED STUDY; DIET SUPPLEMENTATION; DRUG EFFECT; ENTERIC FEEDING; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA2 REGION; HIPPOCAMPAL CA3 REGION; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MORRIS WATER MAZE TEST; MORTALITY; MOTOR COORDINATION; MOUSE; NEUROPROTECTION; NONHUMAN; PARENTERAL NUTRITION; POLE TEST; PRIORITY JOURNAL; ROTAROD TEST; THERAPY EFFECT; ANIMAL; C57BL MOUSE; CEREBROVASCULAR ACCIDENT; DIET THERAPY; DISEASE MODEL; DRUG EFFECTS; PATHOLOGY; PHYSIOLOGY; PROCEDURES; PSYCHOMOTOR PERFORMANCE;

ALPHA-LINOLENIC ACID; ANIMALS; BRAIN ISCHEMIA; COGNITIVE DYSFUNCTION; DISEASE MODELS, ANIMAL; ENTERAL NUTRITION; MALE; MICE; MICE, INBRED C57BL; PARENTERAL NUTRITION; PSYCHOMOTOR PERFORMANCE; STROKE;

EID: 84969593692     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2016.04.040     Document Type: Article

References (86)

1. S.M. Allan, P.J. Tyrrell, and N.J. Rothwell Interleukin-1 and neuronal injury Nat. Rev. Immunol. 5 2005 629 640
2. R. Aquilani, M. Scocchi, P. Iadarola, S. Viglio, E. Pasini, S. Condello, F. Boschi, O. Pastoris, A.I. Bongiorno, and M. Verri Spontaneous neurocognitive retrieval of patients with sub-acute ischemic stroke is associated with dietary protein intake Nutr. Neurosci. 13 2010 129 134
3. M. Awada, A. Meynier, C.O. Soulage, L. Hadji, A. Geloen, M. Viau, L. Ribourg, B. Benoit, C. Debard, M. Guichardant, M. Lagarde, C. Genot, and M.C. Michalski n-3 PUFA added to high-fat diets affect differently adiposity and inflammation when carried by phospholipids or triacylglycerols in mice Nutr. Metab. (Lond) 10 2013 23
4. M. Balkaya, J.M. Krober, A. Rex, and M. Endres Assessing post-stroke behavior in mouse models of focal ischemia J. Cereb. Blood Flow. Metab. 33 2013 330 338
5. L. Belayev, L. Khoutorova, K.D. Atkins, T.N. Eady, S. Hong, Y. Lu, A. Obenaus, and N.G. Bazan Docosahexaenoic acid therapy of experimental ischemic stroke Transl. Stroke Res. 2 2011 33 41
6. N. Blondeau The nutraceutical potential of omega-3 alpha-linolenic acid in reducing the consequences of stroke Biochimie 120 2016 Jan 49 55 10.1016/j.biochi.2015.06.005
7. N. Blondeau, D. Debruyne, M. Piens, C. Nguemeni, J.C. Plumier, R.H. Lipsky, A.M. Marini, and C. Heurteaux Brain plasticity and anti-depressant effects are versatile potential of alpha-linolenic acid to promote stroke recovery J. Cereb. Blood Flow Metabolism 29 2009 S545
8. N. Blondeau, I. Lauritzen, C. Widmann, M. Lazdunski, and C. Heurteaux A potent protective role of lysophospholipids against global cerebral ischemia and glutamate excitotoxicity in neuronal cultures J. Cereb. Blood Flow. Metab. 22 2002 821 834
9. N. Blondeau, R.H. Lipsky, M. Bourourou, M.W. Duncan, P.B. Gorelick, and A.M. Marini Alpha-linolenic acid: an omega-3 fatty acid with neuroprotective properties-ready for use in the stroke clinic? Biomed. Res. Int. 2015 2015 519830
10. N. Blondeau, C. Nguemeni, D.N. Debruyne, M. Piens, X. Wu, H. Pan, X. Hu, C. Gandin, R.H. Lipsky, J.C. Plumier, A.M. Marini, and C. Heurteaux Subchronic alpha-linolenic acid treatment enhances brain plasticity and exerts an antidepressant effect: a versatile potential therapy for stroke Neuropsychopharmacology 34 2009 2548 2559
11. N. Blondeau, C. Nguemeni, D.N. Debruyne, M. Piens, X. Wu, H. Pan, X. Hu, C. Gandin, R.H. Lipsky, J.C. Plumier, A.M. Marini, and C. Heurteaux Subchronic alpha-linolenic acid treatment enhances brain plasticity and exerts an antidepressant effect: a versatile potential therapy for stroke Neuropsychopharmacology 34 2009 2548 2559
12. N. Blondeau, O. Petrault, S. Manta, V. Giordanengo, P. Gounon, R. Bordet, M. Lazdunski, and C. Heurteaux Polyunsaturated fatty acids are cerebral vasodilators via the TREK-1 potassium channel Circ. Res. 101 2007 176 184
13. N. Blondeau, and J.S. Tauskela A new future in brain preconditioning based on nutraceuticals: a focus on a-linolenic omega-3 fatty acid for stroke protection J.M. Gidday, M.A. Perez-Pinzon, J.H. Zhang, Innate Tolerance in the CNS 2013 Springer New York New York 133 163
14. N. Blondeau, C. Widmann, M. Lazdunski, and C. Heurteaux Activation of the nuclear factor-kappaB is a key event in brain tolerance J. Neurosci. 21 2001 4668 4677
15. N. Blondeau, C. Widmann, M. Lazdunski, and C. Heurteaux Polyunsaturated fatty acids induce ischemic and epileptic tolerance Neuroscience 109 2002 231 241
16. N. Blondeau, C. Widmann, M. Lazdunski, and C. Heurteaux Activation of the nuclear factor-kappaB is a key event in brain tolerance J. Krieglstein, S. Klumpp, Pharmacology of Cerebral Ischemia 2003 Medpharm Scientific Publishers Stuttgart
17. J.M. Bourre, O. Dumont, G. Pascal, and G. Durand Dietary alpha-linolenic acid at 1.3 g/kg maintains maximal docosahexaenoic acid concentration in brain, heart and liver of adult rats J. Nutr. 123 1993 1313 1319
18. N. Burgess, E.A. Maguire, and J. O'Keefe The human hippocampus and spatial and episodic memory Neuron 35 2002 625 641
19. C. Calautti, and J.C. Baron Functional neuroimaging studies of motor recovery after stroke in adults: a review Stroke 34 2003 1553 1566
20. M. Chopp, Y. Li, and Z.G. Zhang Mechanisms underlying improved recovery of neurological function after stroke in the rodent after treatment with neurorestorative cell-based therapies Stroke 40 2009 S143 S145
21. F.T. Collaboration Poor nutritional status on admission predicts poor outcomes after stroke: observational data from the FOOD trial Stroke 34 2003 1450 1456
22. G. Conductier, N. Blondeau, A. Guyon, J.L. Nahon, and C. Rovere The role of monocyte chemoattractant protein MCP1/CCL2 in neuroinflammatory diseases J. Neuroimmunol. 224 2010 93 100
23. A.V. Contreras, N. Torres, and A.R. Tovar PPAR-alpha as a key nutritional and environmental sensor for metabolic adaptation Adv. Nutr. 4 2013 439 452
24. S.C. Cramer Repairing the human brain after stroke. II. Restorative therapies Ann. Neurol. 63 2008 549 560
25. T.B. Cumming, R.S. Marshall, and R.M. Lazar Stroke, cognitive deficits, and rehabilitation: still an incomplete picture Int. J. Stroke 8 2013 38 45
26. M.S. Dennis, S.C. Lewis, C. Warlow, and F.T. Collaboration Routine oral nutritional supplementation for stroke patients in hospital (FOOD): a multicentre randomised controlled trial Lancet 365 2005 755 763
27. G. Di Pino, G. Pellegrino, G. Assenza, F. Capone, F. Ferreri, D. Formica, F. Ranieri, M. Tombini, U. Ziemann, J.C. Rothwell, and V. Di Lazzaro Modulation of brain plasticity in stroke: a novel model for neurorehabilitation Nat. Rev. Neurol. 10 2014 597 608
28. M. Dittmar, T. Spruss, G. Schuierer, and M. Horn External carotid artery territory ischemia impairs outcome in the endovascular filament model of middle cerebral artery occlusion in rats Stroke 34 2003 2252 2257
29. C. Drake, H. Boutin, M.S. Jones, A. Denes, B.W. McColl, J.R. Selvarajah, S. Hulme, R.F. Georgiou, R. Hinz, A. Gerhard, A. Vail, C. Prenant, P. Julyan, R. Maroy, G. Brown, A. Smigova, K. Herholz, M. Kassiou, D. Crossman, S. Francis, S.D. Proctor, J.C. Russell, S.J. Hopkins, P.J. Tyrrell, N.J. Rothwell, and S.M. Allan Brain inflammation is induced by co-morbidities and risk factors for stroke Brain Behav. Immun. 25 2011 1113 1122
30. M. El Amki, T. Clavier, N. Perzo, R. Bernard, P.O. Guichet, and H. Castel Hypothalamic, thalamic and hippocampal lesions in the mouse MCAO model: potential involvement of deep cerebral arteries? J. Neurosci. Methods 254 2015 80 85
31. E.V. Evarts, and S.P. Wise Basal ganglia outputs and motor control Ciba Found. Symp. 107 1984 83 102
32. B.M. Forman, J. Chen, and R.M. Evans Hypolipidemic drugs, polyunsaturated fatty acids, and eicosanoids are ligands for peroxisome proliferator-activated receptors alpha and delta Proc. Natl. Acad. Sci. U. S. A. 94 1997 4312 4317
33. P.W. Frankland, and B. Bontempi The organization of recent and remote memories Nat. Rev. Neurosci. 6 2005 119 130
34. T. Freret, P. Schumann-Bard, M. Boulouard, and V. Bouet On the importance of long-term functional assessment after stroke to improve translation from bench to bedside Exp. Transl. Stroke Med. 3 2011 6
35. W. Fujie, T. Kirino, N. Tomukai, T. Iwasawa, and A. Tamura Progressive shrinkage of the thalamus following middle cerebral artery occlusion in rats Stroke 21 1990 1485 1488
36. S.E. Gariballa, S.G. Parker, N. Taub, and C.M. Castleden Influence of nutritional status on clinical outcome after acute stroke Am. J. Clin. Nutr. 68 1998 275 281
37. A.S. Go, D. Mozaffarian, V.L. Roger, E.J. Benjamin, J.D. Berry, M.J. Blaha, S. Dai, E.S. Ford, C.S. Fox, S. Franco, H.J. Fullerton, C. Gillespie, S.M. Hailpern, J.A. Heit, V.J. Howard, M.D. Huffman, S.E. Judd, B.M. Kissela, S.J. Kittner, D.T. Lackland, J.H. Lichtman, L.D. Lisabeth, R.H. Mackey, D.J. Magid, G.M. Marcus, A. Marelli, D.B. Matchar, D.K. McGuire, E.R. Mohler 3rd, C.S. Moy, M.E. Mussolino, R.W. Neumar, G. Nichol, D.K. Pandey, N.P. Paynter, M.J. Reeves, P.D. Sorlie, J. Stein, A. Towfighi, T.N. Turan, S.S. Virani, N.D. Wong, D. Woo, and M.B. Turner Executive summary: heart disease and stroke statistics-2014 update: a report from the American Heart Association Circulation 129 2014 399 410
38. E.V. Golanov, and D.J. Reis Contribution of cerebral edema to the neuronal salvage elicited by stimulation of cerebellar fastigial nucleus after occlusion of the middle cerebral artery in rat J. Cereb. Blood Flow. Metab. 15 1995 172 174
39. E. Gouix, A. Buisson, A. Nieoullon, L. Kerkerian-Le Goff, J.S. Tauskela, N. Blondeau, and L. Had-Aissouni Oxygen glucose deprivation-induced astrocyte dysfunction provokes neuronal death through oxidative stress Pharmacol. Res. 87 2014 8 17
40. A. Gustavsson, M. Svensson, F. Jacobi, C. Allgulander, J. Alonso, E. Beghi, R. Dodel, M. Ekman, C. Faravelli, L. Fratiglioni, B. Gannon, D.H. Jones, P. Jennum, A. Jordanova, L. Jonsson, K. Karampampa, M. Knapp, G. Kobelt, T. Kurth, R. Lieb, M. Linde, C. Ljungcrantz, A. Maercker, B. Melin, M. Moscarelli, A. Musayev, F. Norwood, M. Preisig, M. Pugliatti, J. Rehm, L. Salvador-Carulla, B. Schlehofer, R. Simon, H.C. Steinhausen, L.J. Stovner, J.M. Vallat, P. Van den Bergh, J. van Os, P. Vos, W. Xu, H.U. Wittchen, B. Jonsson, J. Olesen, and C.D. Group Cost of disorders of the brain in Europe 2010 Eur. Neuropsychopharmacol. 21 2011 718 779
41. G.J. Hankey Nutrition and the risk of stroke Lancet Neurol. 11 2012 66 81
42. R. Hata, G. Mies, C. Wiessner, K. Fritze, D. Hesselbarth, G. Brinker, and K.A. Hossmann A reproducible model of middle cerebral artery occlusion in mice: hemodynamic, biochemical, and magnetic resonance imaging J. Cereb. Blood Flow. Metab. 18 1998 367 375
43. A.R. Heller, S. Fischer, T. Rossel, S. Geiger, G. Siegert, M. Ragaller, T. Zimmermann, and T. Koch Impact of n-3 fatty acid supplemented parenteral nutrition on haemostasis patterns after major abdominal surgery Br. J. Nutr. 87 Suppl. 1 2002 S95 S101
44. A.R. Heller, S. Rossler, R.J. Litz, S.N. Stehr, S.C. Heller, R. Koch, and T. Koch Omega-3 fatty acids improve the diagnosis-related clinical outcome Crit. Care Med. 34 2006 972 979
45. C. Heurteaux, C. Laigle, N. Blondeau, G. Jarretou, and M. Lazdunski Alpha-linolenic acid and riluzole treatment confer cerebral protection and improve survival after focal brain ischemia Neuroscience 137 2006 241 251
46. S. Ji, G. Kronenberg, M. Balkaya, K. Farber, K. Gertz, H. Kettenmann, and M. Endres Acute neuroprotection by pioglitazone after mild brain ischemia without effect on long-term outcome Exp. Neurol. 216 2009 321 328
47. B.B. Johansson Current trends in stroke rehabilitation. A review with focus on brain plasticity Acta Neurol. Scand. 123 2011 147 159
48. S.C. Johnston, S. Mendis, and C.D. Mathers Global variation in stroke burden and mortality: estimates from monitoring, surveillance, and modelling Lancet Neurol. 8 2009 345 354
49. A.C. Jonsson, I. Lindgren, B. Norrving, and A. Lindgren Weight loss after stroke: a population-based study from the Lund Stroke Register Stroke 39 2008 918 923
50. H.S. Jorgensen, H. Nakayama, H.O. Raaschou, and T.S. Olsen Recovery of walking function in stroke patients: the Copenhagen Stroke Study Arch. Phys. Med. Rehabil. 76 1995 27 32
51. K. Kataoka, T. Hayakawa, R. Kuroda, T. Yuguchi, and K. Yamada Cholinergic deafferentation after focal cerebral infarct in rats Stroke 22 1991 1291 1296
52. J. Katchanov, C. Harms, K. Gertz, L. Hauck, C. Waeber, L. Hirt, J. Priller, R. von Harsdorf, W. Bruck, H. Hortnagl, U. Dirnagl, P.G. Bhide, and M. Endres Mild cerebral ischemia induces loss of cyclin-dependent kinase inhibitors and activation of cell cycle machinery before delayed neuronal cell death J. Neurosci. 21 2001 5045 5053
53. J. Katchanov, C. Waeber, K. Gertz, A. Gietz, B. Winter, W. Bruck, U. Dirnagl, R.W. Veh, and M. Endres Selective neuronal vulnerability following mild focal brain ischemia in the mouse Brain Pathol. 13 2003 452 464
54. Kilic, E., ElAli, A., Kilic, U., Guo, Z., Ugur, M., Uslu, U., Bassetti, C. L., Schwab, M. E., Hermann, D. M., Role of Nogo-A in neuronal survival in the reperfused ischemic brain. J. Cereb. Blood Flow. Metab. 30, 969-984.
55. K. Kitajka, L.G. Puskas, A. Zvara, L. Hackler Jr., G. Barcelo-Coblijn, Y.K. Yeo, and T. Farkas The role of n-3 polyunsaturated fatty acids in brain: modulation of rat brain gene expression by dietary n-3 fatty acids Proc. Natl. Acad. Sci. U. S. A. 99 2002 2619 2624
56. J.A. Kleim, and T.A. Jones Principles of experience-dependent neural plasticity: implications for rehabilitation after brain damage J. Speech Lang. Hear Res. 51 2008 S225 S239
57. P.M. Kris-Etherton, W.S. Harris, and L.J. Appel Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease Circulation 106 2002 2747 2757
58. L. Lang-Lazdunski, N. Blondeau, G. Jarretou, M. Lazdunski, and C. Heurteaux Linolenic acid prevents neuronal cell death and paraplegia after transient spinal cord ischemia in rats J. Vasc. Surg. 38 2003 564 575
59. P. Langhorne, J. Bernhardt, and G. Kwakkel Stroke rehabilitation Lancet 377 2011 1693 1702
60. P. Langhorne, F. Coupar, and A. Pollock Motor recovery after stroke: a systematic review Lancet Neurol. 8 2009 741 754
61. I. Lauritzen, N. Blondeau, C. Heurteaux, C. Widmann, G. Romey, and M. Lazdunski Polyunsaturated fatty acids are potent neuroprotectors Embo J. 19 2000 1784 1793
62. O. Le Thuc, N. Blondeau, J.L. Nahon, and C. Rovère The complex contribution of chemokines to neuroinflammation: switching from beneficial to detrimental effects Ann. N. Y. Acad. Sci. 1351 2015 Sep 127 140 10.1111/nyas.12855
63. J.H. Lee, Y. Zheng, D. von Bornstadt, Y. Wei, A. Balcioglu, A. Daneshmand, N. Yalcin, E. Yu, F. Herisson, Y.B. Atalay, M.H. Kim, Y.J. Ahn, M. Balkaya, P. Sweetnam, O. Schueller, M.V. Poyurovsky, H.H. Kim, E.H. Lo, K.L. Furie, and C. Ayata Selective ROCK2 inhibition in focal cerebral ischemia Ann. Clin. Transl. Neurol. 1 2014 2 14
64. Z.C. Lin, J. Tao, Y.L. Gao, D.Z. Yin, A.Z. Chen, and L.D. Chen Analysis of central mechanism of cognitive training on cognitive impairment after stroke: resting-state functional magnetic resonance imaging study J. Int. Med. Res. 42 2014 659 668
65. N.B. Lincoln, M.J. Majid, and N. Weyman Cognitive rehabilitation for attention deficits following stroke Cochrane Database Syst. Rev. 4 2000 CD002842
66. D. Lloyd-Jones, R.J. Adams, T.M. Brown, M. Carnethon, S. Dai, G. De Simone, T.B. Ferguson, E. Ford, K. Furie, C. Gillespie, A. Go, K. Greenlund, N. Haase, S. Hailpern, P.M. Ho, V. Howard, B. Kissela, S. Kittner, D. Lackland, L. Lisabeth, A. Marelli, M.M. McDermott, J. Meigs, D. Mozaffarian, M. Mussolino, G. Nichol, V.L. Roger, W. Rosamond, R. Sacco, P. Sorlie, T. Thom, S. Wasserthiel-Smoller, N.D. Wong, and J. Wylie-Rosett Heart disease and stroke statistics-2010 update: a report from the American Heart Association Circulation 121 2010 e46 e215
67. K. Matsuura, H. Kabuto, H. Makino, and N. Ogawa Pole test is a useful method for evaluating the mouse movement disorder caused by striatal dopamine depletion J. Neurosci. Methods 73 1997 45 48
68. R.G. Morris, P. Garrud, J.N. Rawlins, and J. O'Keefe Place navigation impaired in rats with hippocampal lesions Nature 297 1982 681 683
69. T.H. Murphy, and D. Corbett Plasticity during stroke recovery: from synapse to behaviour Nat. Rev. Neurosci. 10 2009 861 872
70. R.D. Nair, and N.B. Lincoln Cognitive rehabilitation for memory deficits following stroke Cochrane Database Syst. Rev. 3 2007 Jul 18 CD002293
71. C. Nguemeni, B. Delplanque, C. Rovere, N. Simon-Rousseau, C. Gandin, G. Agnani, J.L. Nahon, C. Heurteaux, and N. Blondeau Dietary supplementation of alpha-linolenic acid in an enriched rapeseed oil diet protects from stroke Pharmacol. Res. 61 2010 226 233
72. C. Nguemeni, E. Gouix, M. Bourourou, C. Heurteaux, and N. Blondeau Alpha-linolenic acid: a promising nutraceutical for the prevention of stroke PharmaNutrition 1 2013 1 8
73. S. Pilz, A. Tomaschitz, C. Drechsler, A. Zittermann, J.M. Dekker, and W. Marz Vitamin D supplementation: a promising approach for the prevention and treatment of strokes Curr. Drug Targets 12 2011 88 96
74. H. Plamondon, and M.C. Roberge Dietary PUFA supplements reduce memory deficits but not CA1 ischemic injury in rats Physiol. Behav. 95 2008 492 500
75. C. Pudelkewicz, J. Seufert, and R.T. Holman Requirements of the female rat for linoleic and linolenic acids J. Nutr. 94 1968 138 146
76. H. Quintard, M. Borsotto, J. Veyssiere, C. Gandin, F. Labbal, C. Widmann, M. Lazdunski, and C. Heurteaux MLC901, a traditional Chinese medicine protects the brain against global ischemia Neuropharmacology 61 2011 622 631
77. A.K. Rehni, and T.G. Singh Involvement of CCR-2 chemokine receptor activation in ischemic preconditioning and postconditioning of brain in mice Cytokine 60 2012 83 89
78. N.D. Riediger, R.A. Othman, M. Suh, and M.H. Moghadasian A systemic review of the roles of n-3 fatty acids in health and disease J. Am. Diet. Assoc. 109 2009 668 679
79. D.C. Rogers, C.A. Campbell, J.L. Stretton, and K.B. Mackay Correlation between motor impairment and infarct volume after permanent and transient middle cerebral artery occlusion in the rat Stroke 28 1997 2060 2065 discussion 2066
80. N. Scherbakov, U. Dirnagl, and W. Doehner Body weight after stroke: lessons from the obesity paradox Stroke 42 2011 3646 3650
81. S. Stephens, R.A. Kenny, E. Rowan, L. Allan, R.N. Kalaria, M. Bradbury, and C.G. Ballard Neuropsychological characteristics of mild vascular cognitive impairment and dementia after stroke Int. J. Geriatr. Psychiatry 19 2004 1053 1057
82. K. Strong, C. Mathers, and R. Bonita Preventing stroke: saving lives around the world Lancet Neurol. 6 2007 182 187
83. V.R. Venna, D. Deplanque, C. Allet, K. Belarbi, M. Hamdane, and R. Bordet PUFA induce antidepressant-like effects in parallel to structural and molecular changes in the hippocampus Psychoneuroendocrinology 34 2009 199 211
84. Ward, P., Seri, Cavanna, A. E., Functional neuroanatomy and behavioural correlates of the basal ganglia: evidence from lesion studies. Behav. Neurol. 26, 219-223.
85. B. Winter, B. Bert, H. Fink, U. Dirnagl, and M. Endres Dysexecutive syndrome after mild cerebral ischemia? Mice learn normally but have deficits in strategy switching Stroke 35 2004 191 195
86. W. Zhang, X. Hu, W. Yang, Y. Gao, and J. Chen Omega-3 polyunsaturated fatty acid supplementation confers long-term neuroprotection against neonatal hypoxic-ischemic brain injury through anti-inflammatory actions Stroke 41 2010 2341 2347