Dietary intake of unsaturated fatty acids modulates physiological properties of entorhinal cortex neurons in mice

Journal of Neurochemistry

Volumn 122, Issue 2, 2012, Pages 427-443

  Arsenault, Dany ^a,b   Julien, Carl ^a,b   Chen, Chuck T ^c   Bazinet, Richard P ^c   Calon, Frédéric ^a,b  

^a UNIVERSITÉ LAVAL   (Canada)

^b LAVAL UNIVERSITY   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

action potential; alpha linoleic acid; electrophysiology; intrinsic properties; monounsaturated fatty acid; oleic acid

Indexed keywords

ARACHIDONIC ACID; CANOLA OIL; CORN OIL; DOCOSAHEXAENOIC ACID; FATTY ACID; MONOUNSATURATED FATTY ACID; OLEIC ACID; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLSERINE; SAFFLOWER OIL; SOYBEAN OIL; UNSATURATED FATTY ACID;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ARTICLE; DIETARY INTAKE; ENTORHINAL CORTEX; FAT INTAKE; FATTY ACID ANALYSIS; GRAY MATTER; HIPPOCAMPUS; LIPID ANALYSIS; MOUSE; NONHUMAN; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; WHITE MATTER;

ACTION POTENTIALS; ANIMALS; BRAIN CHEMISTRY; DATA INTERPRETATION, STATISTICAL; DIET; ENTORHINAL CORTEX; EXCITATORY POSTSYNAPTIC POTENTIALS; FATTY ACIDS, MONOUNSATURATED; FATTY ACIDS, UNSATURATED; FLAME IONIZATION; LIPIDS; MICE; MICE, INBRED C57BL; NERVE NET; NEURONS; PATCH-CLAMP TECHNIQUES; PHOSPHOLIPIDS; PREFRONTAL CORTEX; SOYBEAN OIL;

ANIMALIA; BRASSICA NAPUS VAR. NAPUS; CARTHAMUS TINCTORIUS; GLYCINE MAX; MUS; ZEA MAYS;

EID: 84863325743     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07772.x     Document Type: Article

References (103)

1. Ahmad A., Murthy M., Greiner R. S., Moriguchi T., and, Salem N. Jr, (2002) A decrease in cell size accompanies a loss of docosahexaenoate in the rat hippocampus. Nutr. Neurosci. 5, 103-113. (Pubitemid 34303213)
2. Alemany R., Navarro M. A., Vogler O., Perona J. S., Osada J., and, Ruiz-Gutierrez V., (2010) Olive oils modulate fatty acid content and signaling protein expression in apolipoprotein E knockout mice brain. Lipids 45, 53-61.
3. Ali A. B., Bannister A. P., and, Thomson A. M., (2007) Robust correlations between action potential duration and the properties of synaptic connections in layer 4 interneurones in neocortical slices from juvenile rats and adult rat and cat. J. Physiol. 580, 149-169. (Pubitemid 46470650)
4. Amtul Z., Westaway D., Cechetto D. F., and, Rozmahel R. F,. (2012) Oleic Acid Ameliorates Amyloidosis in Cellular and Mouse Models of Alzheimer's Disease. Brain Pathol. 21, 321-329.
5. Arsenault D., and, Zhang Z. W., (2006) Developmental remodelling of the lemniscal synapse in the ventral basal thalamus of the mouse. J. Physiol. 573, 121-132. (Pubitemid 43670862)
6. Arsenault D., Julien C., and, Calon F,. (2011a) Chronic dietary intake of alpha-linolenic acid does not replicate the effects of DHA on passive properties of entorhinal cortex neurons. Br. J. Nutr. 107, 1099-1111.
7. Arsenault D., Julien C., Tremblay C., and, Calon F,. (2011b) DHA improves cognition and prevents dysfunction of entorhinal cortex neurons in 3xTg-AD mice. PLoS ONE 6, e17397.
8. Baccus S. A., Sahley C. L., and, Muller K. J., (2001) Multiple sites of action potential initiation increase neuronal firing rate. J. Neurophysiol. 86, 1226-1236. (Pubitemid 32847770)
9. Barberger-Gateau P., Letenneur L., Deschamps V., Peres K., Dartigues J. F., and, Renaud S., (2002) Fish, meat, and risk of dementia: cohort study. BMJ 325, 932-933. (Pubitemid 35265208)
10. Barcelo-Coblijn G., Golovko M. Y., Weinhofer I., Berger J., and, Murphy E. J., (2007) Brain neutral lipids mass is increased in alpha-synuclein gene-ablated mice. J. Neurochem. 101, 132-141. (Pubitemid 46426471)
11. Bean B. P., (2007) The action potential in mammalian central neurons. Nat. Rev. Neurosci. 8, 451-465. (Pubitemid 46789230)
12. Beck H., and, Yaari Y., (2008) Plasticity of intrinsic neuronal properties in CNS disorders. Nat. Rev. Neurosci. 9, 357-369. (Pubitemid 351556043)
13. Blond J. P., Ratieuville P., and, Bezard J., (1986) Dietary fatty acids and delta 5 desaturation by rat liver microsomes. Reprod. Nutr. Dev. 26, 77-84.
14. Bourre J. M., Pascal G., Durand G., Masson M., Dumont O., and, Piciotti M., (1984) Alterations in the fatty acid composition of rat brain cells (neurons, astrocytes, and oligodendrocytes) and of subcellular fractions (myelin and synaptosomes) induced by a diet devoid of n-3 fatty acids. J. Neurochem. 43, 342-348. (Pubitemid 14093559)
15. Bourre J. M., Francois M., Youyou A., Dumont O., Piciotti M., Pascal G., and, Durand G., (1989) The effects of dietary alpha-linolenic acid on the composition of nerve membranes, enzymatic activity, amplitude of electrophysiological parameters, resistance to poisons and performance of learning tasks in rats. J. Nutr. 119, 1880-1892. (Pubitemid 20063881)
16. Bourre J. M., Dumont O., and, Durand G., (1993) Brain phospholipids as dietary source of (n-3) polyunsaturated fatty acids for nervous tissue in the rat. J. Neurochem. 60, 2018-2028. (Pubitemid 23148773)
17. Bourre J. M., Dumont O. L., Clement M. E., and, Durand G. A., (1997) Endogenous synthesis cannot compensate for absence of dietary oleic acid in rats. J. Nutr. 127, 488-493. (Pubitemid 27120005)
18. Bousquet M., Saint-Pierre M., Julien C., Salem N. Jr, Cicchetti F., and, Calon F., (2008) Beneficial effects of dietary omega-3 polyunsaturated fatty acid on toxin-induced neuronal degeneration in an animal model of Parkinson's disease. FASEB J. 22, 1213-1225. (Pubitemid 351519975)
19. Brenna J. T., and, Diau G. Y., (2007) The influence of dietary docosahexaenoic acid and arachidonic acid on central nervous system polyunsaturated fatty acid composition. Prostaglandins Leukot. Essent. Fatty Acids 77, 247-250. (Pubitemid 350198855)
20. Brenna J. T., Salem N. Jr, Sinclair A. J., and, Cunnane S. C., (2009) alpha-Linolenic acid supplementation and conversion to n-3 long-chain polyunsaturated fatty acids in humans. Prostaglandins Leukot. Essent. Fatty Acids 80, 85-91.
21. Calon F., Lim G. P., Yang F., et al. (2004) Docosahexaenoic acid protects from dendritic pathology in an Alzheimer's disease mouse model. Neuron 43, 633-645. (Pubitemid 39179724)
22. Carrie I., Smirnova M., Clement M., De J. D., Frances H., and, Bourre J. M., (2002) Docosahexaenoic acid-rich phospholipid supplementation: effect on behavior, learning ability, and retinal function in control and n-3 polyunsaturated fatty acid deficient old mice. Nutr Neurosci 5, 43-52. (Pubitemid 34228993)
23. Cartling B., (1997) Control of computational dynamics of coupled integrate-and-fire neurons. Biol. Cybern. 76, 383-395. (Pubitemid 127665198)
24. Castagnet P. I., Golovko M. Y., Barcelo-Coblijn G. C., Nussbaum R. L., and, Murphy E. J., (2005) Fatty acid incorporation is decreased in astrocytes cultured from alpha-synuclein gene-ablated mice. J. Neurochem. 94, 839-849. (Pubitemid 41098515)
25. Cermenati G., Abbiati F., Cermenati S., et al. (2011) Diabetes-induced myelin abnormalities are associated with an altered lipid pattern: protective effects of LXR activation. J. Lipid Res. 53, 300-310.
26. Clarke A. L., Petrou S., Walsh J. V. Jr, and, Singer J. J., (2002) Modulation of BK(Ca) channel activity by fatty acids: structural requirements and mechanism of action. Am. J. Physiol. Cell Physiol. 283, C1441-1453. (Pubitemid 35178436)
27. Cole G. M., Ma Q. L., and, Frautschy S. A., (2009) Omega-3 fatty acids and dementia. Prostaglandins Leukot. Essent. Fatty Acids 81, 213-221.
28. Coscina D. V., Yehuda S., Dixon L. M., Kish S. J., and, Leprohon-Greenwood C. E., (1986) Learning is improved by a soybean oil diet in rats. Life Sci. 38, 1789-1794. (Pubitemid 16053291)
29. Crawford M. A., Bazinet R. P., and, Sinclair A. J., (2009) Fat intake and CNS functioning: ageing and disease. Ann. Nutr. Metab. 55, 202-228.
30. Denson D. D., Wang X., Worrell R. T., and, Eaton D. C., (2000) Effects of fatty acids on BK channels in GH(3) cells. Am. J. Physiol. Cell Physiol. 279, C1211-C1219.
31. Devore E. E., Grodstein F., van Rooij F. J., Hofman A., Rosner B., Stampfer M. J., Witteman J. C., and, Breteler M. M., (2009) Dietary intake of fish and omega-3 fatty acids in relation to long-term dementia risk. Am. J. Clin. Nutr. 90, 170-176.
32. Diau G. Y., Hsieh A. T., Sarkadi-Nagy E. A., Wijendran V., Nathanielsz P. W., and, Brenna J. T., (2005) The influence of long chain polyunsaturate supplementation on docosahexaenoic acid and arachidonic acid in baboon neonate central nervous system. BMC Med. 3, 11.
33. Disterhoft J. F., and, Oh M. M., (2006) Learning, aging and intrinsic neuronal plasticity. Trends Neurosci. 29, 587-599. (Pubitemid 44416462)
34. Disterhoft J. F., and, Oh M. M., (2007) Alterations in intrinsic neuronal excitability during normal aging. Aging Cell 6, 327-336. (Pubitemid 46785138)
35. Disterhoft J. F., Golden D. T., Read H. L., Coulter D. A., and, Alkon D. L., (1988) AHP reductions in rabbit hippocampal neurons during conditioning correlate with acquisition of the learned response. Brain Res. 462, 118-125.
36. Dolorfo C. L., and, Amaral D. G., (1998) Entorhinal cortex of the rat: organization of intrinsic connections. J. Comp. Neurol. 398, 49-82. (Pubitemid 28373876)
37. Dolphin A. C., (2009) Calcium channel diversity: multiple roles of calcium channel subunits. Curr. Opin. Neurobiol. 19, 237-244.
38. Feart C., Samieri C., Rondeau V., Amieva H., Portet F., Dartigues J. F., Scarmeas N., and, Barberger-Gateau P., (2009) Adherence to a Mediterranean diet, cognitive decline, and risk of dementia. JAMA 302, 638-648.
39. Fedorova I., and, Salem N. Jr, (2006) Omega-3 fatty acids and rodent behavior. Prostaglandins Leukot. Essent. Fatty Acids 75, 271-289. (Pubitemid 44444990)
40. Fedorova I., Hussein N., Baumann M. H., Di Martino C., and, Salem N. Jr, (2009) An n-3 fatty acid deficiency impairs rat spatial learning in the Barnes maze. Behav. Neurosci. 123, 196-205.
41. Folch J., Lees M., and, Sloane Stanley G. H., (1957) A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226, 497-509.
42. Foot M., Cruz T. F., and, Clandinin M. T., (1982) Influence of dietary fat on the lipid composition of rat brain synaptosomal and microsomal membranes. Biochem. J. 208, 631-640. (Pubitemid 13119407)
43. Fotuhi M., Zandi P. P., Hayden K. M., et al. (2008) Better cognitive performance in elderly taking antioxidant vitamins E and C supplements in combination with nonsteroidal anti-inflammatory drugs: the Cache County Study. Alzheimers Dement 4, 223-227. (Pubitemid 351682262)
44. Garg M. L., Wierzbicki A. A., Thomson A. B., and, Clandinin M. T., (1988) Dietary cholesterol and/or n-3 fatty acid modulate delta 9-desaturase activity in rat liver microsomes. Biochim. Biophys. Acta 962, 330-336.
45. Gentet L. J., Stuart G. J., and, Clements J. D., (2000) Direct measurement of specific membrane capacitance in neurons. Biophys. J. 79, 314-320. (Pubitemid 30436747)
46. Ghatta S., Nimmagadda D., Xu X., and, O'Rourke S. T., (2006) Large-conductance, calcium-activated potassium channels: structural and functional implications. Pharmacol. Ther. 110, 103-116. (Pubitemid 43248728)
47. Golowasch J., Thomas G., Taylor A. L., Patel A., Pineda A., Khalil C., and, Nadim F., (2009) Membrane capacitance measurements revisited: dependence of capacitance value on measurement method in nonisopotential neurons. J. Neurophysiol. 102, 2161-2175.
48. Gong J., Shi F., Shao L., and, Zheng X., (2004) Effects of soybean phospholipids on learning and memory ability and contents of lipids in mice's brain. Wei Sheng Yan Jiu 33, 324-327.
49. van Haeften T., Baks-te-Bulte L., Goede P. H., Wouterlood F. G., and, Witter M. P., (2003) Morphological and numerical analysis of synaptic interactions between neurons in deep and superficial layers of the entorhinal cortex of the rat. Hippocampus 13, 943-952. (Pubitemid 38100743)
50. Haist F., Bowden Gore J., and, Mao H., (2001) Consolidation of human memory over decades revealed by functional magnetic resonance imaging. Nat. Neurosci. 4, 1139-1145. (Pubitemid 34116560)
51. Hattori H., and, Kanfer J. N., (1984) Synaptosomal phospholipase D: potential role in providing choline for acetylcholine synthesis. Biochem. Biophys. Res. Commun. 124, 945-949. (Pubitemid 15219715)
52. Hattori H., Kanfer J. N., and, Massarelli R., (1987) Stimulation of phospholipase D activity and indication of acetylcholine synthesis by oleate in rat brain synaptosomal preparations. Neurochem. Res. 12, 687-692. (Pubitemid 17106837)
53. Heude B., Ducimetiere P., and, Berr C., (2003) Cognitive decline and fatty acid composition of erythrocyte membranes - The EVA Study. Am. J. Clin. Nutr. 77, 803-808.
54. van der Heyden M. J., Hilgevoord A. A., Bour L. J., and, Ongerboer de Visser B. W., (1994) Modeling motoneuron firing properties: dependency on size and calcium dynamics. Biol. Cybern. 72, 133-139.
55. Hou Z. Y., Lin C. I., Vassalle M., Chiang B. N., and, Cheng K. K., (1989) Role of acetylcholine in induction of repetitive activity in human atrial fibers. Am. J. Physiol. 256, H74-84.
56. Hsieh A. T., and, Brenna J. T., (2009) Dietary docosahexaenoic acid but not arachidonic acid influences central nervous system fatty acid status in baboon neonates. Prostaglandins Leukot. Essent. Fatty Acids 81, 105-110.
57. 2 + -activated K+ channels in glutamatergic hippocampal terminals and their role in spike repolarization and regulation of transmitter release. J. Neurosci. 21, 9585-9597. (Pubitemid 34184046)
58. Huang T. L., Zandi P. P., Tucker K. L., Fitzpatrick A. L., Kuller L. H., Fried L. P., Burke G. L., and, Carlson M. C,. (2005) Benefits of fatty fish on dementia risk are stronger for those without APOE epsilon4. Neurology 65, 1409-1414. (Pubitemid 41552771)
59. Ito H., Hosoya Y., Inanobe A., Tomoike H., and, Endoh M., (1995) Acetylcholine and adenosine activate the G protein-gated muscarinic K+ channel in ferret ventricular myocytes. Naunyn Schmiedebergs Arch. Pharmacol. 351, 610-617.
60. Izquierdo I., and, Medina J. H., (1997) Memory formation: the sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol. Learn. Mem. 68, 285-316. (Pubitemid 27506324)
61. Jo Y. H., Su Y., Gutierrez-Juarez R., and, Chua S. Jr, (2009) Oleic acid directly regulates POMC neuron excitability in the hypothalamus. J. Neurophysiol. 101, 2305-2316.
62. Julien C., Berthiaume L., Hadj-Tahar A., Rajput A. H., Bedard P. J., Di Paolo T., Julien P., and, Calon F., (2006) Postmortem brain fatty acid profile of levodopa-treated Parkinson disease patients and parkinsonian monkeys. Neurochem. Int. 48, 404-414. (Pubitemid 43327280)
63. Kong W. J., Guo C. K., Zhang X. W., Chen X., Zhang S., Li G. Q., Li Z. W., and, Van Cauwenberge P., (2007) The coupling of acetylcholine-induced BK channel and calcium channel in guinea pig saccular type II vestibular hair cells. Brain Res. 1129, 110-115. (Pubitemid 46048768)
64. Kroger E., Verreault R., Carmichael P. H., Lindsay J., Julien P., Dewailly E., Ayotte P., and, Laurin D., (2009) Omega-3 fatty acids and risk of dementia: the Canadian Study of Health and Aging. Am. J. Clin. Nutr. 90, 184-192.
65. Lancaster B., and, Nicoll R. A., (1987) Properties of two calcium-activated hyperpolarizations in rat hippocampal neurones. J. Physiol. 389, 187-203. (Pubitemid 17115795)
66. Lipton P. A., and, Eichenbaum H., (2008) Complementary roles of hippocampus and medial entorhinal cortex in episodic memory. Neural Plast 2008, 258467.
67. Liu T. F., and, Chen X. J., (1993) Effects of pinacidil and acetylcholine on early afterdepolarization of atrial fibers in mouse heart. Methods Find. Exp. Clin. Pharmacol. 15, 71-75.
68. Madison D. V., and, Nicoll R. A., (1984) Control of the repetitive discharge of rat CA 1 pyramidal neurones in vitro. J. Physiol. 354, 319-331. (Pubitemid 14066369)
69. Masood A., Stark K. D., and, Salem N. Jr, (2005) A simplified and efficient method for the analysis of fatty acid methyl esters suitable for large clinical studies. J. Lipid Res. 46, 2299-2305. (Pubitemid 41377483)
70. Matthews E. A., Weible A. P., Shah S., and, Disterhoft J. F., (2008) The BK-mediated fAHP is modulated by learning a hippocampus-dependent task. Proc. Natl Acad. Sci. USA 105, 15154-15159.
71. Mauvoisin D., and, Mounier C., (2012) Hormonal and nutritional regulation of SCD1 gene expression. Biochimie 93, 78-86.
72. Moriguchi T., Greiner R. S., and, Salem N. Jr, (2000) Behavioral deficits associated with dietary induction of decreased brain docosahexaenoic acid concentration. J. Neurochem. 75, 2563-2573.
73. Morris M. C., Evans D. A., Bienias J. L., Tangney C. C., Bennett D. A., Wilson R. S., Aggarwal N., and, Schneider J., (2003) Consumption of fish and n-3 fatty acids and risk of incident Alzheimer disease. Arch. Neurol. 60, 940-946. (Pubitemid 36858352)
74. Nakajima Y., Nakajima S., Leonard R. J., and, Yamaguchi K., (1986) Acetylcholine raises excitability by inhibiting the fast transient potassium current in cultured hippocampal neurons. Proc. Natl Acad. Sci. USA 83, 3022-3026. (Pubitemid 16041793)
75. Oh M. M., McKay B. M., Power J. M., and, Disterhoft J. F., (2009) Learning-related postburst afterhyperpolarization reduction in CA1 pyramidal neurons is mediated by protein kinase A. Proc. Natl Acad. Sci. USA 106, 1620-1625.
76. Panza F., Solfrizzi V., Colacicco A. M., D'Introno A., Capurso C., Torres F., Del Parigi A., Capurso S., and, Capurso A., (2004) Mediterranean diet and cognitive decline. Public Health Nutr. 7, 959-963. (Pubitemid 39389283)
77. Panza F., Frisardi V., Seripa D., Imbimbo B. P., Pilotto A., and, Solfrizzi V,. (2010) Dietary Unsaturated Fatty Acids and Risk of Mild Cognitive Impairment. J. Alzheimers Dis. 21, 867-870.
78. Plourde M., and, Cunnane S. C., (2007) Extremely limited synthesis of long chain polyunsaturates in adults: implications for their dietary essentiality and use as supplements. Appl. Physiol. Nutr. Metab. 32, 619-634.
79. Polo-Hernandez E., De Castro F., Garcia-Garcia A. G., Tabernero A., and, Medina J. M., (2011) Oleic acid synthesized in the periventricular zone promotes axonogenesis in the striatum during brain development. J. Neurochem. 114, 1756-1766.
80. Qian J., and, Saggau P., (1999) Modulation of transmitter release by action potential duration at the hippocampal CA3-CA1 synapse. J. Neurophysiol. 81, 288-298. (Pubitemid 29264176)
81. Raffaelli G., Saviane C., Mohajerani M. H., Pedarzani P., and, Cherubini E., (2004) BK potassium channels control transmitter release at CA3-CA3 synapses in the rat hippocampus. J. Physiol. 557, 147-157. (Pubitemid 38771643)
82. Rioux F. M., and, Innis S. M., (1992) Oleic acid (18: 1) in plasma, liver and brain myelin lipid of piglets fed from birth with formulas differing in 18: 1 content. J. Nutr. 122, 1521-1528.
83. Rodriguez-Rodriguez R. A., Tabernero A., Velasco A., Lavado E. M., and, Medina J. M., (2004) The neurotrophic effect of oleic acid includes dendritic differentiation and the expression of the neuronal basic helix-loop-helix transcription factor NeuroD2. J. Neurochem. 88, 1041-1051. (Pubitemid 38280672)
84. Saar D., and, Barkai E., (2003) Long-term modifications in intrinsic neuronal properties and rule learning in rats. Eur. J. Neurosci. 17, 2727-2734. (Pubitemid 36819297)
85. Sah P., and, Faber E. S., (2002) Channels underlying neuronal calcium-activated potassium currents. Prog. Neurobiol. 66, 345-353. (Pubitemid 34518289)
86. Scarmeas N., Stern Y., Mayeux R., and, Luchsinger J. A., (2006) Mediterranean diet, Alzheimer disease, and vascular mediation. Arch. Neurol. 63, 1709-1717. (Pubitemid 44925078)
87. Scarmeas N., Stern Y., Mayeux R., Manly J. J., Schupf N., and, Luchsinger J. A., (2009) Mediterranean diet and mild cognitive impairment. Arch. Neurol. 66, 216-225.
88. Schaefer E. J., Bongard V., Beiser A. S., et al. (2006) Plasma phosphatidylcholine docosahexaenoic acid content and risk of dementia and Alzheimer disease: the Framingham Heart Study. Arch. Neurol. 63, 1545-1550. (Pubitemid 44748796)
89. Sewards T. V., and, Sewards M. A., (2003) Input and output stations of the entorhinal cortex: superficial vs. deep layers or lateral vs. medial divisions? Brain Res. Brain Res. Rev. 42, 243-251. (Pubitemid 36645240)
90. Solfrizzi V., Panza F., Torres F., Mastroianni F., Del Parigi A., Venezia A., and, Capurso A., (1999) High monounsaturated fatty acids intake protects against age-related cognitive decline. Neurology 52, 1563-1569. (Pubitemid 29220628)
91. Solfrizzi V., Capurso C., D'Introno A., Colacicco A. M., Chirico M., Capurso A., and, Panza F,. (2007) Whole-diet approach, Mediterranean diet, and Alzheimer disease. Arch. Neurol. 64, 606; author reply 607.
92. Solfrizzi V., Frisardi V., Capurso C., D'Introno A., Colacicco A. M., Vendemiale G., Capurso A., and, Panza F., (2010) Dietary fatty acids in dementia and predementia syndromes: epidemiological evidence and possible underlying mechanisms. Ageing Res. Rev. 9, 184-199.
93. Stauffer E., (2005) A review of the analysis of vegetable oil residues from fire debris samples: spontaneous ignition, vegetable oils, and the forensic approach. J. Forensic Sci. 50, 1091-1100. (Pubitemid 41279157)
94. Steffenach H. A., Witter M., Moser M. B., and, Moser E. I., (2005) Spatial memory in the rat requires the dorsolateral band of the entorhinal cortex. Neuron 45, 301-313. (Pubitemid 40128123)
95. Stillwell W., Shaikh S. R., Zerouga M., Siddiqui R., and, Wassall S. R., (2005) Docosahexaenoic acid affects cell signaling by altering lipid rafts. Reprod. Nutr. Dev. 45, 559-579. (Pubitemid 41511882)
96. Velasco A., Tabernero A., and, Medina J. M., (2003) Role of oleic acid as a neurotrophic factor is supported in vivo by the expression of GAP-43 subsequent to the activation of SREBP-1 and the up-regulation of stearoyl-CoA desaturase during postnatal development of the brain. Brain Res. 977, 103-111. (Pubitemid 36638699)
97. Wainwright P. E., Huang Y. S., DeMichele S. J., Xing H., Liu J. W., Chuang L. T., and, Biederman J., (2003) Effects of high-gamma-linolenic acid canola oil compared with borage oil on reproduction, growth, and brain and behavioral development in mice. Lipids 38, 171-178. (Pubitemid 36457726)
98. Witter M. P., Van Hoesen G. W., and, Amaral D. G., (1989) Topographical organization of the entorhinal projection to the dentate gyrus of the monkey. J. Neurosci. 9, 216-228. (Pubitemid 19057188)
99. Wurtman R. J., Cansev M., and, Ulus I. H., (2009) Synapse formation is enhanced by oral administration of uridine and DHA, the circulating precursors of brain phosphatides. J. Nutr. Health Aging 13, 189-197.
100. Yurko-Mauro K., McCarthy D., Rom D., Nelson E. B., Ryan A. S., Blackwell A., Salem N. Jr, and, Stedman M., (2011) Beneficial effects of docosahexaenoic acid on cognition in age-related cognitive decline. Alzheimers Dement 6, 456-464.
101. Zhang Z. W., (2004) Maturation of layer V pyramidal neurons in the rat prefrontal cortex: intrinsic properties and synaptic function. J. Neurophysiol. 91, 1171-1182.
102. Zhang Z. W., and, Arsenault D., (2005) Gain modulation by serotonin in pyramidal neurones of the rat prefrontal cortex. J. Physiol. 566, 379-394. (Pubitemid 41030547)
103. Zhou F. M., and, Hablitz J. J,. (1996) Layer I neurons of rat neocortex. I. Action potential and repetitive firing properties. J. Neurophysiol. 76, 651-667. (Pubitemid 26284561)