Effects of diet on brain plasticity in animal and human studies: mind the gap

Tytus Murphy, Gisele Pereira Dias, Sandrine Thuret, Tytus Murphy, Gisele Pereira Dias, Sandrine Thuret

Abstract

Dietary interventions have emerged as effective environmental inducers of brain plasticity. Among these dietary interventions, we here highlight the impact of caloric restriction (CR: a consistent reduction of total daily food intake), intermittent fasting (IF, every-other-day feeding), and diet supplementation with polyphenols and polyunsaturated fatty acids (PUFAs) on markers of brain plasticity in animal studies. Moreover, we also discuss epidemiological and intervention studies reporting the effects of CR, IF and dietary polyphenols and PUFAs on learning, memory, and mood. In particular, we evaluate the gap in mechanistic understanding between recent findings from animal studies and those human studies reporting that these dietary factors can benefit cognition, mood, and anxiety, aging, and Alzheimer's disease-with focus on the enhancement of structural and functional plasticity markers in the hippocampus, such as increased expression of neurotrophic factors, synaptic function and adult neurogenesis. Lastly, we discuss some of the obstacles to harnessing the promising effects of diet on brain plasticity in animal studies into effective recommendations and interventions to promote healthy brain function in humans. Together, these data reinforce the important translational concept that diet, a modifiable lifestyle factor, holds the ability to modulate brain health and function.

Figures

Figure 1
Figure 1
Different dietary interventions in animal and human studies are believed to modulate various aspects of brain plasticity and in turn influence behaviour. Animal studies provide the vast majority of our current mechanistic understanding of the potential mechanisms by which dietary interventions impact brain plasticity. Further mechanistic studies aiming to fill the gap in our understanding of how diet can modulate plasticity and promote mental health in human populations are clearly needed. Moreover, additional intervention studies are also required to demonstrate efficacy, enabling the safe translation of such dietary interventions into clinical practice or incorporated into our daily lifestyles to enhance brain health/function and well-being. In red, effects induced by CR; in purple, effects induced by IF; in green, effects induced by supplementation with polyphenols; in orange, effects induced by PUFAs. AD: Alzheimer's disease; AHN: adult hippocampal neurogenesis; BDNF: brain-derived neurotrophic factor; CBF: cerebral blood flow; CBV: cerebral blood volume; CORT: corticosterone; CR: calorie restriction; CREB: cAMP responsive-element binding; 5-HT: 5-hydroxytryptamine; IF: intermittent fasting; GR: glucocorticoid receptor; LTP: long-term potentiation; MAO-A: monoamine oxidase A; NMDAR: N-methyl-D-aspartate receptor; NE: noradrenaline; NPY-1: neuropeptide Y type 1 receptor; PUFAs: polyunsaturated fatty acids.

References

    1. Squire LR. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychological Review. 1992;99(2):195–231.
    1. Squire LR. The hippocampus and spatial memory. Trends in Neurosciences. 1993;16(2):56–57.
    1. Burgess N, Maguire EA, O’Keefe J. The human hippocampus and spatial and episodic memory. Neuron. 2002;35(4):625–641.
    1. Sweatt JD. Hippocampal function in cognition. Psychopharmacology. 2004;174(1):99–110.
    1. Suthana N, Ekstrom A, Moshirvaziri S, Knowlton B, Bookheimer S. Dissociations within human hippocampal subregions during encoding and retrieval of spatial information. Hippocampus. 2011;21(7):694–701.
    1. Jun H, Mohammed Qasim Hussaini S, Rigby MJ, Jang MH. Functional role of adult hippocampal neurogenesis as a therapeutic strategy for mental disorders. Neural Plasticity. 2012;2012854285
    1. Tsien JZ, Li M, Osan R, et al. On initial Brain Activity Mapping of episodic and semantic memory code in the hippocampus. Neurobiology of Learning and Memory. 2013;105:200–210.
    1. Cooke SF, Bliss TV. Plasticity in the human central nervous system. Brain. 2006;129, part 7:1659–1673.
    1. Maren S, Baudry M. Properties and mechanisms of long-term synaptic plasticity in the mammalian brain: relationships to learning and memory. Neurobiology of Learning and Memory. 1995;63(1):1–18.
    1. Urban NN, Henze DA, Lewis DA, Barrionuevo G. Properties of LTP induction in the CA3 region of the primate hippocampus. Learning Memory. 1996;3(2-3):86–95.
    1. Bonaguidi MA, Song J, Ming GL, Song H. A unifying hypothesis on mammalian neural stem cell properties in the adult hippocampus. Current Opinion in Neurobiology. 2012;22(5):754–761.
    1. Mu Y, Lee SW, Gage FH. Signaling in adult neurogenesis. Current Opinion in Neurobiology. 2010;20(4):416–423.
    1. Deng W, Aimone JB, Gage FH. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nature Reviews Neuroscience. 2010;11(5):339–350.
    1. Snyder JS, Soumier A, Brewer M, Pickel J, Cameron HA. Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature. 2011;476(7361):458–462.
    1. Eisch AJ, Petrik D. Depression and hippocampal neurogenesis: a road to remission? Science. 2012;338(6103):72–75.
    1. Mendez-David I, Hen R, Gardier AM, David DJ. Adult hippocampal neurogenesis: an actor in the antidepressant-like action. Annales Pharmaceutiques Françaises. 2013;71(3):143–149.
    1. Revest J-M, Dupret D, Koehl M, et al. Adult hippocampal neurogenesis is involved in anxiety-related behaviors. Molecular Psychiatry. 2009;14(10):959–967.
    1. Palmer TD, Willhoite AR, Gage FH. Vascular niche for adult hippocampal neurogenesis. Journal of Comparative Neurology. 2000;425(4):479–494.
    1. Villeda SA, Luo J, Mosher KI, et al. The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature. 2011;477(7362):90–94.
    1. Mustroph ML, Chen S, Desai SC, Cay EB, DeYoung EK, Rhodes JS. Aerobic exercise is the critical variable in an enriched environment that increases hippocampal neurogenesis and water maze learning in male C57BL/6J mice. Neuroscience. 2012;219:62–71.
    1. Bechara RG, Kelly AM. Exercise improves object recognition memory and induces BDNF expression and cell proliferation in cognitively enriched rats. Behavioural Brain Research. 2013;245:96–100.
    1. Ambrogini P, Lattanzi D, Ciuffoli S, Betti M, Fanelli M, Cuppini R. Physical exercise and environment exploration affect synaptogenesis in adult-generated neurons in the rat dentate gyrus: possible role of BDNF. Brain Research. 2013;1534:1–12.
    1. Beauquis J, Roig P, de Nicola AF, Saravia F. Short-term environmental enrichment enhances adult neurogenesis, vascular network and dendritic complexity in the hippocampus of type 1 diabetic mice. PLoS ONE. 2010;5(11)e13993
    1. Huang YF, Yang CH, Huang CC, Hsu KS. Vascular endothelial growth factor-dependent spinogenesis underlies antidepressant-like effects of enriched environment. The Journal of Biological Chemistry. 2012;287(49):40938–40955.
    1. Glasper ER, Schoenfeld TJ, Gould E. Adult neurogenesis: optimizing hippocampal function to suit the environment. Behavioural Brain Research. 2012;227(2):380–383.
    1. Kempermann G. New neurons for ‘survival of the fittest’. Nature Reviews Neuroscience. 2012;13(10):727–736.
    1. Lucassen PJ, Pruessner J, Sousa N, et al. Neuropathology of stress. Acta Neuropathologica. 2014;127(1):109–135.
    1. McEwen BS, Magarinos AM. Stress and hippocampal plasticity: implications for the pathophysiology of affective disorders. Human Psychopharmacology. 2001;16(1):S7–S19.
    1. Whiteman AS, Young DE, He X, et al. Interaction between serum BDNF and aerobic fitness predicts recognition memory in healthy young adults. Behavioural Brain Research. 2014;259:302–312.
    1. van der Borght K, Kóbor-Nyakas DÉ, Klauke K, et al. Physical exercise leads to rapid adaptations in hippocampal vasculature: temporal dynamics and relationship to cell proliferation and neurogenesis. Hippocampus. 2009;19(10):928–936.
    1. Stangl D, Thuret S. Impact of diet on adult hippocampal neurogenesis. Genes & Nutrition. 2009;4(4):271–282.
    1. Zainuddin MS, Thuret S. Nutrition, adult hippocampal neurogenesis and mental health. British Medical Bulletin. 2012;103(1):89–114.
    1. Ribaric S. Diet and aging. Oxidative Medicine and Cellular Longevity. 2012;2012:20 pages.741468
    1. McCay CM, Crowell MF, Maynard LA. The effect of retarded growth upon the length of life span and upon the ultimate body size. 1935. Nutrition. 1989;5(3):155–172.
    1. Martin B, Mattson MP, Maudsley S. Caloric restriction and intermittent fasting: two potential diets for successful brain aging. Ageing Research Reviews. 2006;5(3):332–353.
    1. Colman RJ, Anderson RM, Johnson SC, et al. Caloric restriction delays disease onset and mortality in rhesus monkeys. Science. 2009;325(5937):201–204.
    1. Fontana L, Partridge L, Longo VD. Extending healthy life span—from yeast to humans. Science. 2010;328(5976):321–326.
    1. Mattson MP. Energy intake and exercise as determinants of brain health and vulnerability to injury and disease. Cell Metabolism. 2012;16(6):706–722.
    1. Redman LM, Ravussin E. Caloric restriction in humans: impact on physiological, psychological, and behavioral outcomes. Antioxidants & Redox Signaling. 2011;14(2):275–287.
    1. Weiss EP, Fontana L. Caloric restriction: powerful protection for the aging heart and vasculature. American Journal of Physiology Heart and Circulatory Physiology. 2011;301(4):H1205–H1219.
    1. Shetty PK, Galeffi F, Turner DA. Age-induced alterations in hippocampal function and metabolism. Aging and Disease. 2011;2(3):196–218.
    1. Park S-K, Prolla TA. Lessons learned from gene expression profile studies of aging and caloric restriction. Ageing Research Reviews. 2005;4(1):55–65.
    1. Stranahan AM, Mattson MP. Bidirectional metabolic regulation of neurocognitive function. Neurobiology of Learning and Memory. 2011;96(4):507–516.
    1. Adams MM, Shi L, Linville MC, et al. Caloric restriction and age affect synaptic proteins in hippocampal CA3 and spatial learning ability. Experimental Neurology. 2008;211(1):141–149.
    1. Rothman SM, Griffioen KJ, Wan R, Mattson MP. Brain-derived neurotrophic factor as a regulator of systemic and brain energy metabolism and cardiovascular health. Annals of the New York Academy of Sciences. 2012;1264:49–63.
    1. Fusco S, Ripoli C, Podda MV, et al. A role for neuronal cAMP responsive-element binding (CREB)-1 in brain responses to calorie restriction. Proceedings of the National Academy of Sciences of the United States of America. 2012;109(2):621–626.
    1. Kuhla A, Lange S, Holzmann C, et al. Lifelong caloric restriction increases working memory in mice. PLoS ONE. 2013;8(7)e68778
    1. Steinman MQ, Crean KK, Trainor BC. Photoperiod interacts with food restriction in performance in the Barnes maze in female California mice. European Journal of Neuroscience. 2011;33(2):361–370.
    1. Yilmaz N, Vural H, Yilmaz M, et al. Calorie restriction modulates hippocampal NMDA receptors in diet-induced obese rats. Journal of Receptors and Signal Transduction. 2011;31(3):214–219.
    1. Mattson MP, Wan R. Beneficial effects of intermittent fasting and caloric restriction on the cardiovascular and cerebrovascular systems. The Journal of Nutritional Biochemistry. 2005;16(3):129–137.
    1. Kishi T, Sunagawa K. Exercise training plus calorie restriction causes synergistic protection against cognitive decline via up-regulation of BDNF in hippocampus of stroke-prone hypertensive rats. Proceedings of the Annual International Conference of the IEEE Engineering in Medicine and Biology Society IEEE Engineering in Medicine and Biology Society Conference; 2012; pp. 6764–6767.
    1. Newton IG, Forbes ME, Legault C, Johnson JE, Brunso-Bechtold JK, Riddle DR. Caloric restriction does not reverse aging-related changes in hippocampal BDNF. Neurobiology of Aging. 2005;26(5):683–688.
    1. Association AP. Diagnostic and Statistical Manual of Mental Disorders. 5th edition. Arlington, Va, USA: American Psychiatric; 2013.
    1. Mateus-Pinheiro A, Pinto L, Bessa JM, et al. Sustained remission from depressive-like behavior depends on hippocampal neurogenesis. Translational Psychiatry. 2013;3, article e210
    1. de Carvalho MR, Dias GP, Cosci F, et al. Current findings of fMRI in panic disorder: contributions for the fear neurocircuitry and CBT effects. Expert Review of Neurotherapeutics. 2010;10(2):291–303.
    1. Dias GP, de Carvalho MR, Silveira ACD, et al. Current methodological designs of fMRI studies of panic disorder: can data be compared? Psychology and Neuroscience. 2011;4(3):391–407.
    1. Dias GP, Cavegn N, Nix A, et al. The role of dietary polyphenols on adult hippocampal neurogenesis: molecular mechanisms and behavioural effects on depression and anxiety. Oxidative Medicine and Cellular Longevity. 2012;2012:18 pages.541971
    1. Riddle MC, McKenna MC, Yoon YJ, et al. Caloric restriction enhances fear extinction learning in mice. Neuropsychopharmacology. 2013;38(6):930–937.
    1. Vanelzakker MB, Kathryn Dahlgren M, Caroline Davis F, Dubois S, Shin LM. From Pavlov to PTSD: the extinction of conditioned fear in rodents, humans, and anxiety disorders. Neurobiology of Learning and Memory. 2013
    1. Kaplan GB, Moore KA. The use of cognitive enhancers in animal models of fear extinction. Pharmacology Biochemistry and Behavior. 2011;99(2):217–228.
    1. Jahng JW, Kim JG, Kim HJ, Kim B-T, Kang D-W, Lee J-H. Chronic food restriction in young rats results in depression- and anxiety-like behaviors with decreased expression of serotonin reuptake transporter. Brain Research. 2007;1150(1):100–107.
    1. Lutter M, Sakata I, Osborne-Lawrence S, et al. The orexigenic hormone ghrelin defends against depressive symptoms of chronic stress. Nature Neuroscience. 2008;11(7):752–753.
    1. Lutter M, Krishnan V, Russo SJ, Jung S, McClung CA, Nestler EJ. Orexin signaling mediates the antidepressant-like effect of calorie restriction. The Journal of Neuroscience. 2008;28(12):3071–3075.
    1. Pankevich DE, Teegarden SL, Hedin AD, Jensen CL, Bale TL. Caloric restriction experience reprograms stress and orexigenic pathways and promotes binge eating. Journal of Neuroscience. 2010;30(48):16399–16407.
    1. Burke SN, Barnes CA. Neural plasticity in the ageing brain. Nature Reviews Neuroscience. 2006;7(1):30–40.
    1. Artegiani B, Calegari F. Age-related cognitive decline: can neural stem cells help us? Aging. 2012;4(3):176–186.
    1. Lynch AM, Loane DJ, Minogue AM, et al. Eicosapentaenoic acid confers neuroprotection in the amyloid-beta challenged aged hippocampus. Neurobiology of Aging. 2007;28(6):845–855.
    1. Texel SJ, Mattson MP. Impaired adaptive cellular responses to oxidative stress and the pathogenesis of Alzheimer’s disease. Antioxidants & Redox Signaling. 2011;14(8):1519–1534.
    1. Pitsikas N, Algeri S. Deterioration of spatial and nonspatial reference and working memory in aged rats: protective effect of life-long calorie restriction. Neurobiology of Aging. 1992;13(3):369–373.
    1. Komatsu T, Chiba T, Yamaza H, et al. Manipulation of caloric content but not diet composition, attenuates the deficit in learning and memory of senescence-accelerated mouse strain P8. Experimental Gerontology. 2008;43(4):339–346.
    1. Means LW, Higgins JL, Fernandez TJ. Mid-life onset of dietary restriction extends life and prolongs cognitive functioning. Physiology & Behavior. 1993;54(3):503–508.
    1. Goto S, Takahashi R, Radak Z, Sharma R. Beneficial biochemical outcomes of late-onset dietary restriction in rodents. Annals of the New York Academy of Sciences. 2007;1100:431–441.
    1. Kaur M, Sharma S, Kaur G. Age-related impairments in neuronal plasticity markers and astrocytic GFAP and their reversal by late-onset short term dietary restriction. Biogerontology. 2008;9(6):441–454.
    1. Sharma S, Singh R, Kaur M, Kaur G. Late-onset dietary restriction compensates for age-related increase in oxidative stress and alterations of HSP 70 and synapsin1 protein levels in male Wistar rats. Biogerontology. 2010;11(2):197–209.
    1. Eckles-Smith K, Clayton D, Bickford P, Browning MD. Caloric restriction prevents age-related deficits in LTP and in NMDA receptor expression. Molecular Brain Research. 2000;78(1-2):154–162.
    1. Mladenovic Djordjevic A, Perovic M, Tesic V, et al. Long-term dietary restriction modulates the level of presynaptic proteins in the cortex and hippocampus of the aging rat. Neurochemistry International. 2010;56(2):250–255.
    1. Lee J, Duan W, Long JM, Ingram DK, Mattson MP. Dietary restriction increases the number of newly generated neural cells, and BDNF expression, in the dentate gyrus of rats. Journal of Molecular Neuroscience. 2000;15(2):99–108.
    1. Bondolfi L, Ermini F, Long JM, Ingram DK, Jucker M. Impact of age and caloric restriction on neurogenesis in the dentate gyrus of C57BL/6 mice. Neurobiology of Aging. 2004;25(3):333–340.
    1. Gillette-Guyonnet S, Vellas B. Caloric restriction and brain function. Current Opinion in Clinical Nutrition and Metabolic Care. 2008;11(6):686–692.
    1. Keen-Rhinehart E, Ondek K, Schneider JE. Neuroendocrine regulation of appetitive ingestive behavior. Frontiers in Neuroscience. 2013;7, article 213
    1. Rangani RJ, Upadhya MA, Nakhate KT, Kokare DM, Subhedar NK. Nicotine evoked improvement in learning and memory is mediated through NPY Y1 receptors in rat model of Alzheimer’s disease. Peptides. 2012;33(2):317–328.
    1. Howell OW, Doyle K, Goodman JH, et al. Neuropeptide Y stimulates neuronal precursor proliferation in the post-natal and adult dentate gyrus. Journal of Neurochemistry. 2005;93(3):560–570.
    1. Veyrat-Durebex C, Quirion R, Ferland G, Dumont Y, Gaudreau P. Aging and long-term caloric restriction regulate neuropeptide Y receptor subtype densities in the rat brain. Neuropeptides. 2013;47(3):163–169.
    1. Martin CK, Heilbronn LK, de Jonge L, et al. Effect of calorie restriction on resting metabolic rate and spontaneous physical activity. Obesity. 2007;15(12):2964–2973.
    1. Smith PJ, Blumenthal JA, Babyak MA, et al. Effects of the dietary approaches to stop hypertension diet, exercise, and caloric restriction on neurocognition in overweight adults with high blood pressure. Hypertension. 2010;55(6):1331–1338.
    1. Anekonda TS. Resveratrol—a boon for treating Alzheimer’s disease? Brain Research Reviews. 2006;52(2):316–326.
    1. Voss MW, Erickson KI, Prakash RS, et al. Neurobiological markers of exercise-related brain plasticity in older adults. Brain, Behavior, and Immunity. 2013;28:90–99.
    1. Erickson KI, Prakash RS, Voss MW, et al. Brain-derived neurotrophic factor is associated with age-related decline in hippocampal volume. The Journal of Neuroscience. 2010;30(15):5368–5375.
    1. Scarisbrick IA, Jones EG, Isackson PJ. Coexpression of mRNAs for NGF, BDNF, and NT-3 in the cardiovascular system of the pre- and postnatal rat. The Journal of Neuroscience. 1993;13(3):875–893.
    1. Gielen A, Khademi M, Muhallab S, Olsson T, Piehl F. Increased brain-derived neurotrophic factor expression in white blood cells of relapsing-remitting multiple sclerosis patients. Scandinavian Journal of Immunology. 2003;57(5):493–497.
    1. Holtzman DM, Morris JC, Goate AM. Alzheimer’s disease: the challenge of the second century. Science Translational Medicine. 2011;3(77, article 77sr1)
    1. Krstic D, Knuesel I. Deciphering the mechanism underlying late-onset Alzheimer disease. Nature Reviews Neurology. 2013;9(1):25–34.
    1. Lazarov O, Lee M, Peterson DA, Sisodia SS. Evidence that synaptically released β-amyloid accumulates as extracellular deposits in the hippocampus of transgenic mice. Journal of Neuroscience. 2002;22(22):9785–9793.
    1. Phillips HS, Hains JM, Armanini M, Laramee GR, Johnson SA, Winslow JW. BDNF mRNA is decreased in the hippocampus of individuals with Alzheimer’s disease. Neuron. 1991;7(5):695–702.
    1. Tapia-Arancibia L, Aliaga E, Silhol M, Arancibia S. New insights into brain BDNF function in normal aging and Alzheimer disease. Brain Research Reviews. 2008;59(1):201–220.
    1. Lazarov O, Mattson MP, Peterson DA, Pimplikar SW, van Praag H. When neurogenesis encounters aging and disease. Trends in Neurosciences. 2010;33(12):569–579.
    1. Gillette-Guyonnet S, Secher M, Vellas B. Nutrition and neurodegeneration: epidemiological evidence and challenges for future research. British Journal of Clinical Pharmacology. 2013;75(3):738–755.
    1. Pasinetti GM, Eberstein JA. Metabolic syndrome and the role of dietary lifestyles in Alzheimer’s disease. Journal of Neurochemistry. 2008;106(4):1503–1514.
    1. Maruszak A, Pilarski A, Murphy T, Branch N, Thuret S. Hippocampal neurogenesis in Alzheimer's disease: is there a role for dietary modulation? Journal of Alzheimer's Disease. 2014;38(1):11–38.
    1. Wu P, Shen Q, Dong S, Xu Z, Tsien JZ, Hu Y. Calorie restriction ameliorates neurodegenerative phenotypes in forebrain-specific presenilin-1 and presenilin-2 double knockout mice. Neurobiology of Aging. 2008;29(10):1502–1511.
    1. Luchsinger JA, Tang MX, Shea S, Mayeux R. Caloric intake and the risk of Alzheimer disease. Archives of Neurology. 2002;59(8):1258–1263.
    1. Gustafson D, Rothenberg E, Blennow K, Steen B, Skoog I. An 18-year follow-up of overweight and risk of Alzheimer disease. Archives of Internal Medicine. 2003;163(13):1524–1528.
    1. Geda YE, Ragossnig M, Roberts LA, et al. Caloric intake, aging, and mild cognitive impairment: a population-based study. Journal of Alzheimer's disease. 2013;34(2):501–507.
    1. Mattson MP, Duan W, Guo Z. Meal size and frequency affect neuronal plasticity and vulnerability to disease: cellular and molecular mechanisms. Journal of Neurochemistry. 2003;84(3):417–431.
    1. Harrison K. 5:2 Your Life - Get Happy, Get Healthy, Get Slim. CreateSpace Independent Publishing Platform; 2013.
    1. Bruce-Keller AJ, Umberger G, McFall R, Mattson MP. Food restriction reduces brain damage and improves behavioral outcome following excitotoxic and metabolic insults. Annals of Neurology. 1999;45(1):8–15.
    1. Qiu G, Spangler EL, Wan R, et al. Neuroprotection provided by dietary restriction in rats is further enhanced by reducing glucocortocoids. Neurobiology of Aging. 2012;33(10):2398–2410.
    1. Lee J, Seroogy KB, Mattson MP. Dietary restriction enhances neurotrophin expression and neurogenesis in the hippocampus of adult mice. Journal of Neurochemistry. 2002;80(3):539–547.
    1. Fontán-Lozano Á, Sáez-Cassanelli JL, Inda MC, et al. Caloric restriction increases learning consolidation and facilitates synaptic plasticity through mechanisms dependent on NR2B subunits of the NMDA receptor. Journal of Neuroscience. 2007;27(38):10185–10195.
    1. Anson RM, Guo Z, de Cabo R, et al. Intermittent fasting dissociates beneficial effects of dietary restriction on glucose metabolism and neuronal resistance to injury from calorie intake. Proceedings of the National Academy of Sciences of the United States of America. 2003;100(10):6216–6220.
    1. Li B, Zhao J, Lv J, et al. Additive antidepressant-like effects of fasting with imipramine via modulation of 5-HT2 receptors in the mice. Progress in Neuro-Psychopharmacology & Biological Psychiatry. 2014;48:199–206.
    1. Singh R, Lakhanpal D, Kumar S, et al. Late-onset intermittent fasting dietary restriction as a potential intervention to retard age-associated brain function impairments in male rats. Age. 2012;34(4):917–933.
    1. Mansuy IM. Calcineurin in memory and bidirectional plasticity. Biochemical and Biophysical Research Communications. 2003;311(4):1195–1208.
    1. Soderling TR. Calcium/calmodulin-dependent protein kinase II: role in learning and memory. Molecular and Cellular Biochemistry. 1993;127-128:93–101.
    1. Giese KP, Fedorov NB, Filipkowski RK, Silva AJ. Autophosphorylation at Thr286 of the α calcium-calmodulin kinase II in LTP and learning. Science. 1998;279(5352):870–873.
    1. Rutten BPF, van der Kolk NM, Schafer S, et al. Age-related loss of synaptophysin immunoreactive presynaptic boutons within the hippocampus of APP751SL, PS1M146L, and APP751 SL/PS1M146L transgenic mice. American Journal of Pathology. 2005;167(1):161–173.
    1. Vallejo EA. Hunger diet on alternate days in the nutrition of the aged. La Prensa Médica Argentina. 1957;44(2):119–120.
    1. Stunkard A. Nutrition, Aging and Obesity, in Nutrition, Longevity, and Aging. New York, NY, USA: Academic Press; 1976.
    1. Heilbronn LK, Smith SR, Martin CK, Anton SD, Ravussin E. Alternate-day fasting in nonobese subjects: effects on body weight, body composition, and energy metabolism. American Journal of Clinical Nutrition. 2005;81(1):69–73.
    1. Hussin NM, Shahar S, Teng NI, Ngah WZ, Das SK. Efficacy of fasting and calorie restriction (FCR) on mood and depression among ageing men. The Journal of Nutrition, Health & Aging. 2013;17(8):674–680.
    1. Teng NIMF, Shahar S, Manaf ZA, Das SK, Taha CSC, Ngah WZW. Efficacy of fasting calorie restriction on quality of life among aging men. Physiology and Behavior. 2011;104(5):1059–1064.
    1. Halagappa VKM, Guo Z, Pearson M, et al. Intermittent fasting and caloric restriction ameliorate age-related behavioral deficits in the triple-transgenic mouse model of Alzheimer’s disease. Neurobiology of Disease. 2007;26(1):212–220.
    1. Driscoll I, Troncoso J. Asymptomatic Alzheimer’s disease: a prodrome or a state of resilience? Current Alzheimer Research. 2011;8(4):330–335.
    1. Gomez-Pinilla F, Tyagi E. Diet and cognition: interplay between cell metabolism and neuronal plasticity. Current Opinion in Clinical Nutrition and Metabolic Care. 2013;16(6):726–733.
    1. Spencer JP. The impact of fruit flavonoids on memory and cognition. British Journal of Nutrition. 2010;104(supplement 3):S40–S47.
    1. Gupta SC, Patchva S, Koh W, Aggarwal BB. Discovery of curcumin, a component of golden spice, and its miraculous biological activities. Clinical and Experimental Pharmacology and Physiology. 2012;39(3):283–299.
    1. Gomez-Pinilla F, Nguyen TT. Natural mood foods: the actions of polyphenols against psychiatric and cognitive disorders. Nutritional Neuroscience. 2012;15(3):127–133.
    1. Rendeiro C, Vauzour D, Kean RJ, et al. Blueberry supplementation induces spatial memory improvements and region-specific regulation of hippocampal BDNF mRNA expression in young rats. Psychopharmacology. 2012;223(3):319–330.
    1. Rendeiro C, Vauzour D, Rattray M, et al. Dietary levels of pure flavonoids improve spatial memory performance and increase hippocampal brain-derived neurotrophic factor. PLoS ONE. 2013;8(5)e63535
    1. Zhao YN, Li WF, Li F, et al. Resveratrol improves learning and memory in normally aged mice through microRNA-CREB pathway. Biochemical and Biophysical Research Communications. 2013;435(4):597–602.
    1. Saharan S, Jhaveri DJ, Bartlett PF. SIRT1 regulates the neurogenic potential of neural precursors in the adult subventricular zone and hippocampus. Journal of Neuroscience Research. 2013;91(5):642–659.
    1. Harada N, Zhao J, Kurihara H, Nakagata N, Okajima K. Resveratrol improves cognitive function in mice by increasing production of insulin-like growth factor-I in the hippocampus. The Journal of Nutritional Biochemistry. 2011;22(12):1150–1159.
    1. Narimatsu N, Harada N, Kurihara H, Nakagata N, Sobue K, Okajima K. Donepezil improves cognitive function in mice by increasing the production of insulin-like growth factor-I in the hippocampus. Journal of Pharmacology and Experimental Therapeutics. 2009;330(1):2–12.
    1. Dal-Pan A, Pifferi F, Marchal J, Picq J-L, Aujard F. Cognitive performances are selectively enhanced during chronic caloric restriction or resveratrol supplementation in a primate. PLoS ONE. 2011;6(1)e16581
    1. Park HR, Kong KH, Yu BP, Mattson MP, Lee J. Resveratrol inhibits the proliferation of neural progenitor cells and hippocampal neurogenesis. The Journal of Biological Chemistry. 2012;287(51):42588–42600.
    1. Willner P, Towell A, Sampson D, Sophokleous S, Muscat R. Reduction of sucrose preference by chronic unpredictable mild stress, and its restoration by a tricyclic antidepressant. Psychopharmacology. 1987;93(3):358–364.
    1. Liu D, Zhang Q, Gu J, et al. Resveratrol prevents impaired cognition induced by chronic unpredictable mild stress in rats. Progress in Neuro-Psychopharmacology & Biological Psychiatry. 2014;49:21–29.
    1. Wang Z, Gu J, Wang X, et al. Antidepressant-like activity of resveratrol treatment in the forced swim test and tail suspension test in mice: the HPA axis, BDNF expression and phosphorylation of ERK. Pharmacology Biochemistry and Behavior. 2013;112:104–110.
    1. Madhyastha S, Sahu SS, Rao G. Resveratrol for prenatal-stress-induced oxidative damage in growing brain and its consequences on survival of neurons. The Journal of Basic and Clinical Physiology and Pharmacology. 2013
    1. Madhyastha S, Sekhar S, Rao G. Resveratrol improves postnatal hippocampal neurogenesis and brain derived neurotrophic factor in prenatally stressed rats. International Journal of Developmental Neuroscience. 2013;31(7):580–585.
    1. Pilar-Cuellar F, Vidal R, Diaz A, et al. Neural plasticity and proliferation in the generation of antidepressant effects: hippocampal implication. Neural Plasticity. 2013;2013:21 pages.537265
    1. Xu Y, Wang Z, You W, et al. Antidepressant-like effect of trans-resveratrol: involvement of serotonin and noradrenaline system. European Neuropsychopharmacology. 2010;20(6):405–413.
    1. Liu Y, Jia G, Gou L, et al. Antidepressant-like effects of tea polyphenols on mouse model of chronic unpredictable mild stress. Pharmacology Biochemistry and Behavior. 2013;104:27–32.
    1. Yu Y, Wang R, Chen C, et al. Antidepressant-like effect of trans-resveratrol in chronic stress model: behavioral and neurochemical evidences. Journal of Psychiatric Research. 2013;47(3):315–322.
    1. Casadesus G, Shukitt-Hale B, Stellwagen HM, et al. Modulation of hippocampal plasticity and cognitive behavior by short-term blueberry supplementation in aged rats. Nutritional Neuroscience. 2004;7(5-6):309–316.
    1. Conboy L, Foley AG, O’Boyle NM, et al. Curcumin-induced degradation of PKCδ is associated with enhanced dentate NCAM PSA expression and spatial learning in adult and aged Wistar rats. Biochemical Pharmacology. 2009;77(7):1254–1265.
    1. Dong S, Zeng Q, Mitchell ES, et al. Curcumin enhances neurogenesis and cognition in aged rats: implications for transcriptional interactions related to growth and synaptic plasticity. PLoS ONE. 2012;7(2)e31211
    1. Kuwabara T, Hsieh J, Muotri A, et al. Wnt-mediated activation of NeuroD1 and retro-elements during adult neurogenesis. Nature Neuroscience. 2009;12(9):1097–1105.
    1. Mons N, Segu L, Nogues X, Buhot MC. Effects of age and spatial learning on adenylyl cyclase mRNA expression in the mouse hippocampus. Neurobiology of Aging. 2004;25(8):1095–1106.
    1. Bhullar KS, Rupasinghe HP. Polyphenols: multipotent therapeutic agents in neurodegenerative diseases. Oxidative Medicine and Cellular Longevity. 2013;2013:18 pages.891748
    1. Ng TP, Chiam PC, Lee T, Chua HC, Lim L, Kua EH. Curry consumption and cognitive function in the elderly. American Journal of Epidemiology. 2006;164(9):898–906.
    1. Letenneur L, Proust-Lima C, Le Gouge A, Dartigues JF, Barberger-Gateau P. Flavonoid intake and cognitive decline over a 10-year period. American Journal of Epidemiology. 2007;165(12):1364–1371.
    1. Kesse-Guyot E, Fezeu L, Andreeva VA, et al. Total and specific polyphenol intakes in midlife are associated with cognitive function measured 13 years later. Journal of Nutrition. 2012;142(1):76–83.
    1. Mandel SA, Avramovich-Tirosh Y, Reznichenko L, et al. Multifunctional activities of green tea catechins in neuroprotection: modulation of cell survival genes, iron-dependent oxidative stress and PKC signaling pathway. NeuroSignals. 2005;14(1-2):46–60.
    1. Choi DY, Lee YJ, Hong JT, Lee HJ. Antioxidant properties of natural polyphenols and their therapeutic potentials for Alzheimer’s disease. Brain Research Bulletin. 2012;87(2-3):144–153.
    1. Gaudreault SB, Dea D, Poirier J. Increased caveolin-1 expression in Alzheimer’s disease brain. Neurobiol Aging. 2004;25(6):753–759.
    1. Moosmang S, Haider N, Klugbauer N, et al. Role of hippocampal Cav1.2 Ca2+ channels in NMDA receptor-independent synaptic plasticity and spatial memory. The Journal of Neuroscience. 2005;25(43):9883–9892.
    1. Veng LM, Mesches MH, Browning MD. Age-related working memory impairment is correlated with increases in the L-type calcium channel protein α 1D (Cav1.3) in area CA1 of the hippocampus and both are ameliorated by chronic nimodipine treatment. Molecular Brain Research. 2003;110(2):193–202.
    1. Wang J, Ferruzzi MG, Ho L, et al. Brain-targeted proanthocyanidin metabolites for Alzheimer’s disease treatment. The Journal of Neuroscience. 2012;32(15):5144–5150.
    1. Ho L, Ferruzzi MG, Janle EM, et al. Identification of brain-targeted bioactive dietary quercetin-3-O-glucuronide as a novel intervention for Alzheimer’s disease. The FASEB Journal. 2013;27(2):769–781.
    1. Hoppe JB, Coradini K, Frozza RL, et al. Free and nanoencapsulated curcumin suppress beta-amyloid-induced cognitive impairments in rats: involvement of BDNF and Akt/GSK-3beta signaling pathway. Neurobiol Learning Memory. 2013;106:134–144.
    1. Kuriyama S, Hozawa A, Ohmori K, et al. Green tea consumption and cognitive function: a cross-sectional study from the Tsurugaya Project 1. The American Journal of Clinical Nutrition. 2006;83(2):355–361.
    1. Lindsay J, Laurin D, Verreault R, et al. Risk factors for Alzheimer’s disease: a prospective analysis from the Canadian Study of Health and Aging. American Journal of Epidemiology. 2002;156(5):445–453.
    1. Luchsinger JA, Tang MX, Siddiqui M, Shea S, Mayeux R. Alcohol intake and risk of dementia. Journal of the American Geriatrics Society. 2004;52(4):540–546.
    1. Andrieu S, Ousset P-J, Coley N, Ouzid M, Mathiex-Fortunet H, Vellas B. GuidAge study: a 5-year double blind, randomised trial of EGb 761 for the prevention of Alzheimer’s disease in elderly subjects with memory complaints. I. Rationale, design and baseline data. Current Alzheimer Research. 2008;5(4):406–415.
    1. Vellas B, Coley N, Ousset PJ, et al. Long-term use of standardised Ginkgo biloba extract for the prevention of Alzheimer’s disease (GuidAge): a randomised placebo-controlled trial. The Lancet Neurology. 2012;11(10):851–859.
    1. Dangour AD, Allen E, Richards M, Whitehouse P, Uauy R. Design considerations in long-term intervention studies for the prevention of cognitive decline or dementia. Nutrition Reviews. 2010;68(supplement 1):S16–S21.
    1. Cederholm T, Salem N, Jr., Palmblad J. omega-3 fatty acids in the prevention of cognitive decline in humans. Advances in Nutrition. 2013;4(6):672–676.
    1. Davidson MH. Omega-3 fatty acids: new insights into the pharmacology and biology of docosahexaenoic acid, docosapentaenoic acid, and eicosapentaenoic acid. Current Opinion in Lipidology. 2013;24(6):467–474.
    1. Meyer BJ, Mann NJ, Lewis JL, Milligan GC, Sinclair AJ, Howe PRC. Dietary intakes and food sources of omega-6 and omega-3 polyunsaturated fatty acids. Lipids. 2003;38(4):391–398.
    1. Su HM. Mechanisms of n-3 fatty acid-mediated development and maintenance of learning memory performance. The Journal of Nutritional Biochemistry. 2010;21(5):364–373.
    1. Farkas T, Kitajka K, Fodor E, et al. Docosahexaenoic acid-containing phospholipid molecular species in brains of vertebrates. Proceedings of the National Academy of Sciences of the United States of America. 2000;97(12):6362–6366.
    1. Kitajka K, Puskas LG, Zvara A, et al. The role of n-3 polyunsaturated fatty acids in brain: modulation of rat brain gene expression by dietary n-3 fatty acids. Proceedings of the National Academy of Sciences of the United States of America. 2002;99(5):2619–2624.
    1. Barcelo-Coblijn G, Hogyes E, Kitajka K, et al. Modification by docosahexaenoic acid of age-induced alterations in gene expression and molecular composition of rat brain phospholipids. Proceedings of the National Academy of Sciences of the United States of America. 2003;100(20):11321–11326.
    1. Jansen D, Zerbi V, Arnoldussen IA, et al. Effects of specific multi-nutrient enriched diets on cerebral metabolism, cognition and neuropathology in abetaPPswe-PS1dE9 mice. PLoS ONE. 2013;8(9)e75393
    1. Kawashima A, Harada T, Kami H, Yano T, Imada K, Mizuguchi K. Effects of eicosapentaenoic acid on synaptic plasticity, fatty acid profile and phosphoinositide 3-kinase signaling in rat hippocampus and differentiated PC12 cells. Journal of Nutritional Biochemistry. 2010;21(4):268–277.
    1. Niculescu MD, Lupu DS, Craciunescu CN. Maternal α-linolenic acid availability during gestation and lactation alters the postnatal hippocampal development in the mouse offspring. International Journal of Developmental Neuroscience. 2011;29(8):795–802.
    1. Kawakita E, Hashimoto M, Shido O. Docosahexaenoic acid promotes neurogenesis in vitro and in vivo . Neuroscience. 2006;139(3):991–997.
    1. Venna VR, Deplanque D, Allet C, Belarbi K, Hamdane M, Bordet R. PUFA induce antidepressant-like effects in parallel to structural and molecular changes in the hippocampus. Psychoneuroendocrinology. 2009;34(2):199–211.
    1. He C, Qu X, Cui L, Wang J, Kang JX. Improved spatial learning performance of fat-1 mice is associated with enhanced neurogenesis and neuritogenesis by docosahexaenoic acid. Proceedings of the National Academy of Sciences of the United States of America. 2009;106(27):11370–11375.
    1. Crupi R, Cambiaghi M, Deckelbaum R, et al. n − 3 fatty acids prevent impairment of neurogenesis and synaptic plasticity in B-cell activating factor (BAFF) transgenic mice. Preventive Medicine. 2012;54(supplement):S103–S108.
    1. Lei X, Zhang W, Liu T, et al. Perinatal supplementation with omega-3 polyunsaturated fatty acids improves sevoflurane-induced neurodegeneration and memory impairment in neonatal rats. PLoS ONE. 2013;8(8)e70645
    1. Jiang H, Wang Z, Wang Y, et al. Antidepressant-like effects of curcumin in chronic mild stress of rats: involvement of its anti-inflammatory action. Progress in Neuro-Psychopharmacology & Biological Psychiatry. 2013;47:33–39.
    1. Bhatia HS, Agrawal R, Sharma S, Huo Y-X, Ying Z, Gomez-Pinilla F. Omega-3 fatty acid deficiency during brain maturation reduces neuronal and behavioral plasticity in adulthood. PLoS ONE. 2011;6(12)e28451
    1. Vines A, Delattre AM, Lima MMS, et al. The role of 5-HT1A receptors in fish oil-mediated increased BDNF expression in the rat hippocampus and cortex: a possible antidepressant mechanism. Neuropharmacology. 2012;62(1):184–191.
    1. Hennebelle M, Balasse L, Latour A, et al. Influence of omega-3 fatty acid status on the way rats adapt to chronic restraint stress. PLoS ONE. 2012;7(7)e42142
    1. Sharma S, Zhuang Y, Gomez-Pinilla F. High-fat diet transition reduces brain DHA levels associated with altered brain plasticity and behaviour. Scientific Reports. 2012;2, article 431
    1. Tyagi E, Agrawal R, Zhuang Y, Abad C, Waschek JA, Gomez-Pinilla F. Vulnerability imposed by diet and brain trauma for anxiety-like phenotype: implications for post-traumatic stress disorders. PLoS ONE. 2013;8(3)e57945
    1. Matsuoka Y. Clearance of fear memory from the hippocampus through neurogenesis by omega-3 fatty acids: a novel preventive strategy for posttraumatic stress disorder? BioPsychoSocial Medicine. 2011;5, article 3
    1. Sublette ME, Ellis SP, Geant AL, Mann JJ. Meta-analysis of the effects of eicosapentaenoic acid (EPA) in clinical trials in depression. Journal of Clinical Psychiatry. 2011;72(12):1577–1584.
    1. Lin PY, Mischoulon D, Freeman MP, et al. Are omega-3 fatty acids antidepressants or just mood-improving agents? The effect depends upon diagnosis, supplement preparation, and severity of depression. Molecular Psychiatry. 2012;17(12):1161–1163.
    1. Martins JG, Bentsen H, Puri BK. Eicosapentaenoic acid appears to be the key omega-3 fatty acid component associated with efficacy in major depressive disorder: a critique of Bloch and Hannestad and updated meta-analysis. Molecular Psychiatry. 2012;17:1144–1167.
    1. Tanskanen A, Hibbeln JR, Hintikka J, et al. Fish consumption, depression, and suicidality in a general population. Archives of General Psychiatry. 2001;58(5):512–513.
    1. Silvers KM, Scott KM. Fish consumption and self-reported physical and mental health status. Public Health Nutrition. 2002;5(3):427–431.
    1. Hibbeln JR. Seafood consumption, the DHA content of mothers’ milk and prevalence rates of postpartum depression: a cross-national, ecological analysis. Journal of Affective Disorders. 2002;69(1–3):15–29.
    1. Adams PB, Lawson S, Sanigorski A, Sinclair AJ. Arachidonic acid to eicosapentaenoic acid ratio in blood correlates positively with clinical symptoms of depression. Lipids. 1996;31(supplement):S157–S161.
    1. Peet M, Murphy B, Shay J, Horrobin D. Depletion of omega-3 fatty acid levels in red blood cell membranes of depressive patients. Biological Psychiatry. 1998;43(5):315–319.
    1. Jazayeri S, Tehrani-Doost M, Keshavarz SA, et al. Comparison of therapeutic effects of omega-3 fatty acid eicosapentaenoic acid and fluoxetine, separately and in combination, in major depressive disorder. Australian and New Zealand Journal of Psychiatry. 2008;42(3):192–198.
    1. Frangou S, Lewis M, McCrone P. Efficacy of ethyl-eicosapentaenoic acid in bipolar depression: randomised double-blind placebo-controlled study. British Journal of Psychiatry. 2006;188:46–50.
    1. Haberka M, Mizia-Stec K, Mizia M, et al. Effects of n-3 polyunsaturated fatty acids on depressive symptoms, anxiety and emotional state in patients with acute myocardial infarction. Pharmacological Reports. 2013;65(1):59–68.
    1. Giltay EJ, Geleijnse JM, Kromhout D. Effects of n-3 fatty acids on depressive symptoms and dispositional optimism after myocardial infarction. The American Journal of Clinical Nutrition. 2011;94(6):1442–1450.
    1. Kiecolt-Glaser JK, Belury MA, Andridge R, Malarkey WB, Glaser R. Omega-3 supplementation lowers inflammation and anxiety in medical students: a randomized controlled trial. Brain, Behavior, and Immunity. 2011;25(8):1725–1734.
    1. Kelly L, Grehan B, Chiesa AD, et al. The polyunsaturated fatty acids, EPA and DPA exert a protective effect in the hippocampus of the aged rat. Neurobiology of Aging. 2011;32(12):2318.e1–2318.e15.
    1. Labrousse VF, Nadjar A, Joffre C, et al. Short-term long chain omega3 diet protects from neuroinflammatory processes and memory impairment in aged mice. PLoS ONE. 2012;7(5)e36861
    1. Hussain G, Schmitt F, Loeffler JP, de Aguilar JL. Fatting the brain: a brief of recent research. Frontiers in Cellular Neuroscience. 2013;7, article 144
    1. Sydenham E, Dangour AD, Lim WS. Omega 3 fatty acid for the prevention of cognitive decline and dementia. The Cochrane Database of Systematic Reviews. 2012;6CD005379
    1. Luchtman DW, Song C. Cognitive enhancement by omega-3 fatty acids from child-hood to old age: findings from animal and clinical studies. Neuropharmacology. 2013;64:550–565.
    1. van Gelder BM, Tijhuis M, Kalmijn S, Kromhout D. Fish consumption, n-3 fatty acids, and subsequent 5-y cognitive decline in elderly men: the Zutphen Elderly Study. American Journal of Clinical Nutrition. 2007;85(4):1142–1147.
    1. Nilsson A, Radeborg K, Salo I, Bjorck I. Effects of supplementation with n-3 polyunsaturated fatty acids on cognitive performance and cardiometabolic risk markers in healthy 51 to 72 years old subjects: a randomized controlled cross-over study. Nutrition Journal. 2012;11, article 99
    1. Titova OE, Sjogren P, Brooks SJ, et al. Dietary intake of eicosapentaenoic and docosahexaenoic acids is linked to gray matter volume and cognitive function in elderly. Age. 2013;35(4):1495–1505.
    1. van de Rest O, Spiro A, III, Krall-Kaye E, Geleijnse JM, de Groot LCPGM, Tucker KL. Intakes of (n − 3) fatty acids and fatty fish are not associated with cognitive performance and 6-year cognitive change in men participating in the Veterans Affairs Normative Aging Study. Journal of Nutrition. 2009;139(12):2329–2336.
    1. Adams MM, Donohue HS, Linville MC, Iversen EA, Newton IG, Brunso-Bechtold JK. Age-related synapse loss in hippocampal CA3 is not reversed by caloric restriction. Neuroscience. 2010;171(2):373–382.
    1. Jansen D, Zerbi V, Janssen CI, et al. Impact of a multi-nutrient diet on cognition, brain metabolism, hemodynamics, and plasticity in apoE4 carrier and apoE knockout mice. Brain Structure & Function. In press.
    1. Amtul Z, Uhrig M, Rozmahel RF, Beyreuther K. Structural insight into the differential effects of omega-3 and omega-6 fatty acids on the production of Aβ peptides and amyloid plaques. Journal of Biological Chemistry. 2011;286(8):6100–6107.
    1. Liu CC, Kanekiyo T, Xu H, Bu G. Apolipoprotein E and Alzheimer disease: risk, mechanisms and therapy. Nature Reviews Neurology. 2013;9(2):106–118.
    1. Davignon J. Apolipoprotein E and atherosclerosis: beyond lipid effect. Arteriosclerosis, Thrombosis, and Vascular Biology. 2005;25(2):267–269.
    1. Mahley RW. Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science. 1988;240(4852):622–630.
    1. Pfrieger FW. Cholesterol homeostasis and function in neurons of the central nervous system. Cellular and Molecular Life Sciences. 2003;60(6):1158–1171.
    1. Kariv-Inbal Z, Yacobson S, Berkecz R, et al. The isoform-specific pathological effects of ApoE4 in vivo are prevented by a fish oil (DHA) diet and are modified by cholesterol. Journal of Alzheimer’s Disease. 2012;28(3):667–683.
    1. von Arnim CAF, Gola U, Biesalski HK. More than the sum of its parts? Nutrition in Alzheimer’s disease. Nutrition. 2010;26(7-8):694–700.
    1. Seignourel PJ, Kunik ME, Snow L, Wilson N, Stanley M. Anxiety in dementia: a critical review. Clinical Psychology Review. 2008;28(7):1071–1082.
    1. Arsenault D, Julien C, Tremblay C, Calon F. DHA improves cognition and prevents dysfunction of entorhinal cortex neurons in 3xTg-AD mice. PLoS ONE. 2011;6(2)e17397
    1. Bonnet E, Touyarot K, Alfos S, Pallet V, Higueret P, Abrous DN. Retinoic acid restores adult hippocampal neurogenesis and reverses spatial memory deficit in vitamin A deprived rats. PLoS ONE. 2008;3(10)e3487
    1. Fotuhi M, Mohassel P, Yaffe K. Fish consumption, long-chain omega-3 fatty acids and risk of cognitive decline or Alzheimer disease: a complex association. Nature Clinical Practice Neurology. 2009;5(3):140–152.
    1. Morris MC, Evans DA, Bienias JL, et al. Consumption of fish and n-3 fatty acids and risk of incident Alzheimer disease. Archives of Neurology. 2003;60(7):940–946.
    1. Phillips MA, Childs CE, Calder PC, Rogers PJ. Lower omega-3 fatty acid intake and status are associated with poorer cognitive function in older age: a comparison of individuals with and without cognitive impairment and Alzheimer’s disease. Nutritional Neuroscience. In press.
    1. Chiu CC, Su KP, Cheng TC, et al. The effects of omega-3 fatty acids monotherapy in Alzheimer’s disease and mild cognitive impairment: a preliminary randomized double-blind placebo-controlled study. Progress in Neuro-Psychopharmacology & Biological Psychiatry. 2008;32(6):1538–1544.
    1. Dangour AD, Andreeva VA, Sydenham E, Uauy R. Omega 3 fatty acids and cognitive health in older people. British Journal of Nutrition. 2012;107(supplement 2):S152–S158.
    1. Sperling RA, Karlawish J, Johnson KA. Preclinical Alzheimer disease-the challenges ahead. Nature Reviews Neurology. 2013;9(1):54–58.
    1. Scheltens P, Kamphuis PJGH, Verhey FRJ, et al. Efficacy of a medical food in mild Alzheimer’s disease: a randomized, controlled trial. Alzheimer’s and Dementia. 2010;6(1):1.e1–10.e1.
    1. Scheltens P, Twisk JW, Blesa R, et al. Efficacy of Souvenaid in mild Alzheimer's disease: results from a randomized, controlled trial. Journal of Alzheimer’s Disease. 2012;31(1):225–236.
    1. Gomez-Pinilla F. Brain foods: the effects of nutrients on brain function. Nature Reviews Neuroscience. 2008;9(7):568–578.
    1. Gomez-Pinilla F. The combined effects of exercise and foods in preventing neurological and cognitive disorders. Preventive Medicine. 2011;52(supplement 1):S75–S80.
    1. Witte AV, Fobker M, Gellner R, Knecht S, Floel A. Caloric restriction improves memory in elderly humans. Proceedings of the National Academy of Sciences of the United States of America. 2009;106(4):1255–1260.
    1. Voss MW, Vivar C, Kramer AF, van Praag H. Bridging animal and human models of exercise-induced brain plasticity. Trends in Cognitive Sciences. 2013;17(10):525–544.
    1. Chytrova G, Ying Z, Gomez-Pinilla F. Exercise contributes to the effects of DHA dietary supplementation by acting on membrane-related synaptic systems. Brain Research. 2010;1341:32–40.
    1. Wu A, Ying Z, Gomez-Pinilla F. Docosahexaenoic acid dietary supplementation enhances the effects of exercise on synaptic plasticity and cognition. Neuroscience. 2008;155(3):751–759.
    1. Wu A, Ying Z, Gomez-Pinilla F. Exercise facilitates the action of dietary DHA on functional recovery after brain trauma. Neuroscience. 2013;248:655–663.
    1. van Praag H, Lucero MJ, Yeo GW, et al. Plant-derived flavanol (-)epicatechin enhances angiogenesis and retention of spatial memory in mice. Journal of Neuroscience. 2007;27(22):5869–5878.
    1. Molteni R, Wu A, Vaynman S, Ying Z, Barnard RJ, Gómez-Pinilla F. Exercise reverses the harmful effects of consumption of a high-fat diet on synaptic and behavioral plasticity associated to the action of brain-derived neurotrophic factor. Neuroscience. 2004;123(2):429–440.
    1. Trepanowski JF, Canale RE, Marshall KE, Kabir MM, Bloomer RJ. Impact of caloric and dietary restriction regimens on markers of health and longevity in humans and animals: a summary of available findings. Nutrition Journal. 2011;10(1, article 107)
    1. Seo AY, Hofer T, Sung B, Judge S, Chung HY, Leeuwenburgh C. Hepatic oxidative stress during aging: effects of 8% long-term calorie restriction and lifelong exercise. Antioxidants and Redox Signaling. 2006;8(3-4):529–538.
    1. Deruisseau KC, Kavazis AN, Judge S, et al. Moderate caloric restriction increases diaphragmatic antioxidant enzyme mRNA, but not when combined with lifelong exercise. Antioxidants and Redox Signaling. 2006;8(3-4):539–547.
    1. Holloszy JO. Mortality rate and longevity of food-restricted exercising male rats: a reevaluation. Journal of Applied Physiology. 1997;82(2):399–403.
    1. Agrawal R, Gomez-Pinilla F. Metabolic syndrome’ in the brain: deficiency in omega-3 fatty acid exacerbates dysfunctions in insulin receptor signalling and cognition. The Journal of Physiology. 2012;590, part 10:2485–2499.
    1. Ho NF, Hooker JM, Sahay A, Holt DJ, Roffman JL. In vivo imaging of adult human hippocampal neurogenesis: progress, pitfalls and promise. Molecular Psychiatry. 2013;18(4):404–416.
    1. Nagahama Y, Nabatame H, Okina T, et al. Cerebral correlates of the progression rate of the cognitive decline in probable Alzheimer’s disease. European Neurology. 2003;50(1):1–9.
    1. Ruitenberg A, Den Heijer T, Bakker SLM, et al. Cerebral hypoperfusion and clinical onset of dementia: the Rotterdam Study. Annals of Neurology. 2005;57(6):789–794.
    1. Francis ST, Head K, Morris PG, Macdonald IA. The effect of flavanol-rich cocoa on the fMRI response to a cognitive task in healthy young people. Journal of Cardiovascular Pharmacology. 2006;47(supplement 2):S215–S220.
    1. Fisher ND, Sorond FA, Hollenberg NK. Cocoa flavanols and brain perfusion. Journal of Cardiovascular Pharmacology. 2006;47(supplement 2):S210–S214.
    1. Spalding KL, Bergmann O, Alkass K, et al. Dynamics of hippocampal neurogenesis in adult humans. Cell. 2013;153(6):1219–1227.
    1. Lee SW, Clemenson GD, Gage FH. New neurons in an aged brain. Behavioural Brain Research. 2012;227(2):497–507.
    1. Dauncey MJ. Genomic and epigenomic insights into nutrition and brain disorders. Nutrients. 2013;5(3):887–914.
    1. Milenkovic D, Deval C, Gouranton E, et al. Modulation of miRNA expression by dietary polyphenols in apoE deficient mice: a new mechanism of the action of polyphenols. PLoS ONE. 2012;7(1)e29837
    1. Sinn N, Milte C, Howe PR. Oiling the brain: a review of randomized controlled trials of omega-3 fatty acids in psychopathology across the lifespan. Nutrients. 2010;2(2):128–170.
    1. Wollen KA. Alzheimer’s disease: the pros and cons of pharmaceutical, nutritional, botanical, and stimulatory therapies, with a discussion of treatment strategies from the perspective of patients and practitioners. Alternative Medicine Review. 2010;15(3):223–244.
    1. Yanai S, Okaichi Y, Okaichi H. Long-term dietary restriction causes negative effects on cognitive functions in rats. Neurobiology of Aging. 2004;25(3):325–332.
    1. Aggarwal A, Monsivais P, Cook AJ, Drewnowski A. Does diet cost mediate the relation between socioeconomic position and diet quality? European Journal of Clinical Nutrition. 2011;65(9):1059–1066.
    1. Turrell G, Lynch JW, Kaplan GA, et al. Socioeconomic position across the lifecourse and cognitive function in late middle age. The Journals of Gerontology B: Psychological Sciences and Social Sciences. 2002;57(1):S43–S51.
    1. Karlamangla AS, Miller-Martinez D, Aneshensel CS, Seeman TE, Wight RG, Chodosh J. Trajectories of cognitive function in late life in the United States: demographic and socioeconomic predictors. American Journal of Epidemiology. 2009;170(3):331–342.
    1. Hackman DA, Farah MJ, Meaney MJ. Socioeconomic status and the brain: mechanistic insights from human and animal research. Nature Reviews Neuroscience. 2010;11(9):651–659.
    1. Parrott MD, Shatenstein B, Ferland G, et al. Relationship between diet quality and cognition depends on socioeconomic position in healthy older adults. Journal of Nutrition. 2013;143(11):1767–1773.
    1. Steffener J, Stern Y. Exploring the neural basis of cognitive reserve in aging. Biochimica et Biophysica Acta. 2012;1822(3):467–473.

Source: PubMed

3
Suscribir