Western-style diet induces object recognition deficits and alters complexity of dendritic arborization in the hippocampus and entorhinal cortex of male rats

References

• Adult Obesity Facts. Centers for Disease Control and Prevention [Internet]. Centers for Disease Control and Prevention; 2015 Sep. Available from: http://www.cdc.gov/obesity/data/adult.html
   Google Scholar
• Bogers RP, Bemelmans WJE, Hoogenveen RT, Boshuizen HC, Woodward M, Knekt P, et al. Association of overweight with increased risk of coronary heart disease partly independent of blood pressure and cholesterol levels: a meta-analysis of 21 cohort studies including more than 300 000 persons. Arch Intern Med 2007;167(16):1720–8.
   PubMedGoogle Scholar
• Stranahan AM, Norman ED, Lee K, Cutler RG, Telljohann RS, Egan JM, et al. Diet-induced insulin resistance impairs hippocampal synaptic plasticity and cognition in middle-aged rats. Hippocampus 2008;18(11):1085–8.
   PubMed Web of Science ®Google Scholar
• Mattson MP, Mattson MP. The impact of dietary energy intake on cognitive aging. Front Aging Neurosci 2010;2:5.
   PubMed Web of Science ®Google Scholar
• Kanoski SE, Davidson TL. Western diet consumption and cognitive impairment: links to hippocampal dysfunction and obesity. Physiol Behav 2011;103(1):59–68.
   PubMed Web of Science ®Google Scholar
• Stranahan AM, Mattson MP. Impact of energy intake and expenditure on neuronal plasticity. Neuromol Med 2008;10(4):209–18.
   PubMed Web of Science ®Google Scholar
• Luchsinger JA, Gustafson DR. Adiposity, type 2 diabetes and Alzheimer’s disease. J Alzheimers Dis JAD 2009;16(4):693–704.
   PubMed Web of Science ®Google Scholar
• Naderali EK, Ratcliffe SH, Dale MC. Review: obesity and Alzheimer’s disease: a link between body weight and cognitive function in old age. Am J Alzheimers Dis Other Demen 2009;24(6):445–9.
   PubMed Web of Science ®Google Scholar
• Valladolid-Acebes I, Stucchi P, Cano V, Fernández-Alfonso MS, Merino B, Gil-Ortega M, et al. High-fat diets impair spatial learning in the radial-arm maze in mice. Neurobiol Learn Mem 2011;95(1):80–5.
   PubMed Web of Science ®Google Scholar
• Cui Y, Shu Y, Zhu Y, Shi Y, Le G. High-fat diets impair spatial learning of mice in the Y-maze paradigm: ameliorative potential of α-lipoic acid. J Med Food 2012;15(8):713–7.
   PubMed Web of Science ®Google Scholar
• Heyward FD, Walton RG, Carle MS, Coleman MA, Garvey WT, Sweatt JD. Adult mice maintained on a high-fat diet exhibit object location memory deficits and reduced hippocampal SIRT1 gene expression. Neurobiol Learn Mem 2012;98(1):25–32.
   PubMed Web of Science ®Google Scholar
• Darling JN, Ross AP, Bartness TJ, Parent MB. Predicting the effects of a high-energy diet on fatty liver and hippocampal-dependent memory in male rats. Obesity 2013;21(5):910–7.
   PubMed Web of Science ®Google Scholar
• Jurdak N, Lichtenstein AH, Kanarek RB. Diet-induced obesity and spatial cognition in young male rats. Nutr Neurosci 2008;11(2):48–54.
   PubMed Web of Science ®Google Scholar
• Marwitz SE, Woodie LN, Blythe SN. Western-style diet induces insulin insensitivity and hyperactivity in adolescent male rats. Physiol Behav 2015;151:147–54.
   PubMed Web of Science ®Google Scholar
• Antunes M, Biala G. The novel object recognition memory: neurobiology, test procedure, and its modifications. Cogn Process 2012;13(2):93–110.
   PubMed Web of Science ®Google Scholar
• Davidson TL, Monnot A, Neal AU, Martin AA, Horton JJ, Zheng W. The effects of a high-energy diet on hippocampal-dependent discrimination performance and blood-brain barrier integrity differ for diet-induced obese and diet-resistant rats. Physiol Behav 2012;107(1):26–33.
   PubMed Web of Science ®Google Scholar
• Stranahan AM, Mattson MP. Bidirectional metabolic regulation of neurocognitive function. Neurobiol Learn Mem 2011;96(4):507–16.
   PubMed Web of Science ®Google Scholar
• Kosari S, Badoer E, Nguyen JCD, Killcross AS, Jenkins TA. Effect of western and high fat diets on memory and cholinergic measures in the rat. Behav Brain Res 2012;235(1):98–103.
   PubMed Web of Science ®Google Scholar
• Valladolid-Acebes I, Fole A, Martín M, Morales L, Victoria Cano M, Ruiz-Gayo M, et al. Spatial memory impairment and changes in hippocampal morphology are triggered by high-fat diets in adolescent mice. Is there a role of leptin? Neurobiol Learn Mem 2013;106:18–25.
   PubMed Web of Science ®Google Scholar
• Hargrave SL, Davidson TL, Zheng W, Kinzig KP. Western diets induce blood-brain barrier leakage and alter spatial strategies in rats. Behav Neurosci 2016;130(1):123–35.
   PubMed Web of Science ®Google Scholar
• Muller AP, Cammarota M, De OD, Rotta LN, Portela LV, Souza DO, et al. Different effect of high fat diet and physical exercise in the hippocampal signaling. Neurochem Res 2008;33(5):880–5.
   PubMed Web of Science ®Google Scholar
• Park HR, Park M, Choi J, Park K-Y, Chung HY, Lee J. A high-fat diet impairs neurogenesis: involvement of lipid peroxidation and brain-derived neurotrophic factor. Neurosci Lett 2010;482(3):235–9.
   PubMed Web of Science ®Google Scholar
• Pistell PJ, Morrison CD, Gupta S, Knight AG, Keller JN, Ingram DK, et al. Cognitive impairment following high fat diet consumption is associated with brain inflammation. J Neuroimmunol 2010;219(1–2):25–32.
   PubMed Web of Science ®Google Scholar
• Kanoski SE. Cognitive and neuronal systems underlying obesity. Physiol Behav 2012;106(3):337–44.
   PubMed Web of Science ®Google Scholar
• Lindqvist A, Mohapel P, Bouter B, Frielingsdorf H, Pizzo D, Brundin P, et al. High-fat diet impairs hippocampal neurogenesis in male rats. Eur J Neurol 2006;13(12):1385–8.
   PubMed Web of Science ®Google Scholar
• Moraes JC, Coope A, Morari J, Cintra DE, Roman EA, Pauli JR, et al. High-Fat diet induces apoptosis of hypothalamic neurons. PLoS ONE 2009;4(4):e5045.
   PubMed Web of Science ®Google Scholar
• Wilson DIG, Langston RF, Schlesiger MI, Wagner M, Watanabe S, Ainge JA. Lateral entorhinal cortex is critical for novel object-context recognition. Hippocampus 2013;23(5):352–66.
   PubMed Web of Science ®Google Scholar
• Brown CM, Mulcahey TA, Filipek NC, Wise PM. Production of proinflammatory cytokines and chemokines during neuroinflammation: novel roles for estrogen receptors α and β. Endocrinology 2010;151(10):4916–25.
   PubMed Web of Science ®Google Scholar
• Gibb R, Kolb B. A method for vibratome sectioning of Golgi-Cox stained whole rat brain. J Neurosci Methods 1998;79(1):1–4.
   PubMed Web of Science ®Google Scholar
• Morris RGM, Schenk F, Tweedie F, Jarrard LE. Ibotenate lesions of hippocampus and/or subiculum: dissociating components of allocentric spatial learning. Eur J Neurosci 1990;2(12):1016–28.
   PubMed Web of Science ®Google Scholar
• Kitamura T, Macdonald CJ, Tonegawa S. Entorhinal–hippocampal neuronal circuits bridge temporally discontiguous events. Learn Mem 2015;22(9):438–43.
   PubMed Web of Science ®Google Scholar
• Preston AR, Eichenbaum H. Interplay of hippocampus and prefrontal Cortex in memory. Curr Biol 2013;23(17):R764–R773.
   PubMed Web of Science ®Google Scholar
• Xu H, Hsiao MC, Song D, Berger TW. Recording place cells from multiple sub-regions of the rat hippocampus with a customized micro-electrode array. In: 2014 36th Annual International Conference of the IEEE Engineering in Medicine and Biology Society. 2014. pp. 4876–9.
   Google Scholar
• Stackman RW, Cohen SJ, Lora JC, Rios LM. Temporary inactivation reveals that the CA1 region of the mouse dorsal hippocampus plays an equivalent role in the retrieval of long-term object memory and spatial memory. Neurobiol Learn Mem 2016;133:118–28.
   PubMed Web of Science ®Google Scholar
• Tronel S, Charrier V, Sage C, Maitre M, Leste-Lasserre T, Abrous DN. Adult-born dentate neurons are recruited in both spatial memory encoding and retrieval. Hippocampus 2015;25(11):1472–9.
   PubMed Web of Science ®Google Scholar
• Ekstrom AD, Bazih AJ, Suthana NA, Al-Hakim R, Ogura K, Zeineh M, et al. Advances in high-resolution imaging and computational unfolding of the human hippocampus. Neuroimage 2009;47(1):42–9.
   PubMed Web of Science ®Google Scholar
• Deller T, Martinez A, Nitsch R, Frotscher M. A novel entorhinal projection to the Rat dentate gyrus: direct innervation of proximal dendrites and cell bodies of granule cells and GABAergic neurons. J Neurosci 1996;16(10):3322–33.
   PubMed Web of Science ®Google Scholar
• Snow WM, Pahlavan PS, Djordjevic J, McAllister D, Platt EE, Alashmali S, et al. Morris Water Maze training in mice elevates hippocampal levels of transcription factors nuclear factor (erythroid-derived 2)-like 2 and nuclear factor kappa B p65. Front Mol Neurosci 2015;8:70.
   PubMed Web of Science ®Google Scholar
• Miyoshi E, Wietzikoski EC, Bortolanza M, Boschen SL, Canteras NS, Izquierdo I, et al. Both the dorsal hippocampus and the dorsolateral striatum are needed for rat navigation in the Morris water maze. Behav Brain Res 2012;226(1):171–8.
   PubMed Web of Science ®Google Scholar
• Svensson M, Hallin T, Broms J, Ekstrand J, Tingström A. Spatial memory impairment in Morris water maze after electroconvulsive seizures. Acta Neuropsychiatr 2017;29(1):17–26.
   PubMed Web of Science ®Google Scholar
• Laeremans A, Sabanov V, Ahmed T, Nys J, Van de Plas B, Vinken K, et al. Distinct and simultaneously active plasticity mechanisms in mouse hippocampus during different phases of Morris water maze training. Brain Struct Funct 2015;220(3):1273–90.
   PubMed Web of Science ®Google Scholar
• Maass A, Schütze H, Speck O, Yonelinas A, Tempelmann C, Heinze H-J, et al. Laminar activity in the hippocampus and entorhinal cortex related to novelty and episodic encoding. Nat Commun 2014;5:5547.
   PubMed Web of Science ®Google Scholar
• Di Paola M, Macaluso E, Carlesimo GA, Tomaiuolo F, Worsley KJ, Fadda L, et al. Episodic memory impairment in patients with Alzheimer’s disease is correlated with entorhinal cortex atrophy. A voxel-based morphometry study. J Neurol 2007;254(6):774–81.
   PubMed Web of Science ®Google Scholar
• Wyss JM, Chambless BD, Kadish I, van Groen T. Age-related decline in water maze learning and memory in rats: strain differences. Neurobiol Aging 2000;21(5):671–81.
   PubMed Web of Science ®Google Scholar
• 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):429–40.
   PubMed Web of Science ®Google Scholar
• Bocarsly ME, Fasolino M, Kane GA, LaMarca EA, Kirschen GW, Karatsoreos IN, et al. Obesity diminishes synaptic markers, alters microglial morphology, and impairs cognitive function. Proc Natl Acad Sci U S A 2015;112(51):15731–6.
   PubMed Web of Science ®Google Scholar
• Beilharz JE, Maniam J, Morris MJ. Short exposure to a diet rich in both fat and sugar or sugar alone impairs place, but not object recognition memory in rats. Brain Behav Immun 2014;37:134–41.
   PubMed Web of Science ®Google Scholar
• Morganstern I, Ye Z, Liang S, Fagan S, Leibowitz SF. Involvement of cholinergic mechanisms in the behavioral effects of dietary fat consumption. Brain Res 2012;1470:24–34.
   PubMed Web of Science ®Google Scholar
• Flores G, Flores-Gómez GD, de Jesús Gomez-Villalobos M. Neuronal changes after chronic high blood pressure in animal models and its implication for vascular dementia. Synap 2016;70(5):198–205.
   PubMed Web of Science ®Google Scholar
• Vuong B, Odero G, Rozbacher S, Stevenson M, Kereliuk SM, Pereira TJ, et al. Exposure to gestational diabetes mellitus induces neuroinflammation, derangement of hippocampal neurons, and cognitive changes in rat offspring. J Neuroinflamm 2017;14(1):80.
   PubMedGoogle Scholar
• Wainwright PE, Bulman-Fleming MB, Lévesque S, Mutsaers L, McCutcheon D. A saturated-fat diet during development alters dendritic growth in mouse brain. Nutr Neurosci 1998;1(1):49–58.
   PubMedGoogle Scholar
• Bastian TW, von Hohenberg WC, Mickelson DJ, Lanier LM, Georgieff MK. Iron deficiency impairs developing hippocampal neuron gene expression, energy metabolism, and dendrite complexity. Dev Neurosci 2016;38:264–76.
   PubMed Web of Science ®Google Scholar
• Monserrat Hernández-Hernández E, Serrano-García C, Antonio Vázquez-Roque R, Díaz A, Monroy E, Rodríguez-Moreno A, et al. Chronic administration of resveratrol prevents morphological changes in prefrontal cortex and hippocampus of aged rats. Synap 2016;70(5):206–17.
   PubMed Web of Science ®Google Scholar
• Solis-Gaspar C, Vazquez-Roque RA, De Jesús Gómez-Villalobos M, Flores G. Cerebrolysin improves memory and ameliorates neuronal atrophy in spontaneously hypertensive, aged rats. Synap 2016;70(9):378–89.
   PubMed Web of Science ®Google Scholar
• Wu Y, Dissing-Olesen L, MacVicar BA, Stevens B. Microglia: dynamic mediators of synapse development and plasticity. Trends Immunol 2015;36(10):605–13.
   PubMed Web of Science ®Google Scholar
• Medinilla V, Johnson O, Gasparini S. Features of proximal and distal excitatory synaptic inputs to layer V neurons of the rat medial entorhinal cortex. J Physiol 2013;591(Pt 1):169–83.
   PubMed Web of Science ®Google Scholar
• Hao S, Dey A, Yu X, Stranahan AM. Dietary obesity reversibly induces synaptic stripping by microglia and impairs hippocampal plasticity. Brain Behav Immun 2016;51:230–9.
   PubMed Web of Science ®Google Scholar
• Kastellakis G, Cai DJ, Mednick SC, Silva AJ, Poirazi P. Synaptic clustering within dendrites: an emerging theory of memory formation. Prog Neurobiol 2015;126:19–35.
   PubMed Web of Science ®Google Scholar
• Castro GC, Areias MF, Weissmann L, Quaresma PGF, Katashima CK, Saad MJA, et al. Diet-induced obesity induces endoplasmic reticulum stress and insulin resistance in the amygdala of rats. FEBS Open Biol 2013;3:443–9.
   PubMed Web of Science ®Google Scholar
• Erion DM, Lapworth A, Amor PA, Bai G, Vera NB, Clark RW, et al. The hepatoselective glucokinase activator PF-04991532 ameliorates hyperglycemia without causing hepatic steatosis in diabetic rats. PLoS ONE 2014;9(5):e97139.
   PubMed Web of Science ®Google Scholar
• Boitard C, Cavaroc A, Sauvant J, Aubert A, Castanon N, Layé S, et al. Impairment of hippocampal-dependent memory induced by juvenile high-fat diet intake is associated with enhanced hippocampal inflammation in rats. Brain Behav Immun 2014;40:9–17.
   PubMed Web of Science ®Google Scholar
• Ekdahl CT, Claasen J-H, Bonde S, Kokaia Z, Lindvall O. Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci 2003;100(23):13632–7.
   PubMed Web of Science ®Google Scholar