Brain and behavioral perturbations in rats following Western diet access

Appetite

Volumn 93, Issue , 2015, Pages 35-43

  Hargrave, Sara L ^a,b   Davidson, Terry L ^b   Lee, Tien Jui ^a   Kinzig, Kimberly P ^a  

^a PURDUE UNIVERSITY   (United States)

^b AMERICAN UNIVERSITY   (United States)

Author keywords

GLUT1; Hippocampus; MCT1; Obesity; Spontaneous alternation; Vicarious trial and error

Indexed keywords

3 HYDROXYBUTYRIC ACID; GLUCOSE; GLUCOSE TRANSPORTER 1; INSULIN; KETONE; MONOCARBOXYLATE TRANSPORTER 1; COTRANSPORTER; GLUCOSE BLOOD LEVEL; MESSENGER RNA; MONOCARBOXYLATE TRANSPORT PROTEIN 1; MONOCARBOXYLATE TRANSPORTER; SLC2A1 PROTEIN, RAT;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CALORIC INTAKE; COGNITION; CONTROLLED STUDY; FAT CONTENT; FOOD INTAKE; GLUCOSE BLOOD LEVEL; HIPPOCAMPUS; INSULIN BLOOD LEVEL; KETOGENIC DIET; MALE; NONHUMAN; OBESITY; PROTEIN EXPRESSION; RAT; WEIGHT GAIN; WESTERN DIET; ADVERSE EFFECTS; ANALYSIS; ANIMAL; BLOOD; BRAIN; DEMENTIA; LEARNING; MEMORY; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; BLOOD GLUCOSE; BRAIN; COGNITION; DEMENTIA; DIET, WESTERN; GLUCOSE TRANSPORTER TYPE 1; HIPPOCAMPUS; INSULIN; KETOGENIC DIET; KETONES; LEARNING; MALE; MEMORY; MONOCARBOXYLIC ACID TRANSPORTERS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SYMPORTERS;

EID: 84939571088     PISSN: 01956663     EISSN: 10958304     Source Type: Journal    
DOI: 10.1016/j.appet.2015.03.037     Document Type: Article

References (96)

1. Addis D.R., Moscovitch M., McAndrews M.P. Consequences of hippocampal damage across the autobiographical memory network in left temporal lobe epilepsy. Brain: A Journal of Neurology 2007, 130:2327-2342. 10.1093/brain/awm166.
2. Addis D.R., Schacter D.L. Constructive episodic simulation. Temporal distance and detail of past and future events modulate hippocampal engagement. Hippocampus 2008, 18:227-237. 10.1002/hipo.20405.
3. Agranat-Meged A.N., Deitcher C., Goldzweig G., Leibenson L., Stein M., Galili-Weisstub E. Childhood obesity and attention deficit/hyperactivity disorder. A newly described comorbidity in obese hospitalized children. International Journal of Eating Disorders 2005, 37(4):357-359.
4. Akman C.I., Engelstad K., Hinton V.J., Ullner P., Koenigsberger D., Leary L., et al. Acute hyperglycemia produces transient improvement in glucose transporter type 1 deficiency. Annals of Neurology 2010, 67:31-40. 10.1002/ana.21797.
5. Albelda N., Joel D. Current animal models of obsessive compulsive disorder. An update. Neuroscience 2012, 211:83-106. 10.1016/j.neuroscience.2011.08.070.
6. Asin K.E., Fibiger H.C. Spontaneous and delayed spatial alternation following damage to specific neuronal elements within the nucleus medianus raphe. Behavioural Brain Research 1984, 13:241-250.
7. Bailey T., Rivara C., Rocher A., Hof P. The nature and effects of cortical microvascular pathology in aging and Alzheimer's disease. Neurological Research 2004, 26:573-578.
8. Barañano K.W., Hartman A.L. The ketogenic diet. Uses in epilepsy and other neurologic illnesses. Current Treatment Options in Neurology 2008, 10:410-419.
9. Benoit S.C., Davis J.F., Davidson T.L. Learned and cognitive controls of food intake. Brain Research 2010, 1350:71-76.
10. Blass E.M., Anderson D.R., Kirkorian H.L., Pempek T.A., Price I., Koleini M.F. On the road to obesity. Television viewing increases intake of high-density foods. Physiology & Behavior 2006, 88:597-604. 10.1016/j.physbeh.2006.05.035.
11. Boado R.J. Brain-derived peptides increase the expression of a blood-brain barrier GLUT1 glucose transporter reporter gene. Neuroscience Letters 1996, 220(1):53-56. 10.1016/S0304-3940(96)13237-7.
12. Boado R.J., Pardridge W.M. Glucose deprivation causes posttranscriptional enhancement of brain capillary endothelial glucose transporter gene expression via GLUT1 mRNA stabilization. Journal of Neurochemistry 1993, 60(6):2290-2296. 10.1111/j.1471-4159.1993.tb03516.x.
13. 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, Behavior, and Immunity 2014, 40:9-17.
14. Boitard C., Etchamendy N., Sauvant J., Aubert A., Tronel S., Marighetto A., et al. Juvenile, but not adult exposure to high-fat diet impairs relational memory and hippocampal neurogenesis in mice. Hippocampus 2012, 22(11):2095-2100.
15. Buckner R.L., Carroll D.C. Self-projection and the brain. Trends in Cognitive Sciences 2007, 11:49-57. 10.1016/j.tics.2006.11.004.
16. Caston J., Vasseur F., Delhaye-Bouchaud N., Mariani J. Delayed spontaneous alternation in intact and cerebellectomized control and lurcher mutant mice. Differential role of cerebellar cortex and deep cerebellar nuclei. Behavioral Neuroscience 1997, 111:214-218.
17. Cordeira J., Rios M. Weighing in the role of BDNF in the central control of eating behavior. Molecular Neurobiology 2011, 44:441-448. 10.1007/s12035-011-8212-2.
18. Cortes-Campos C., Elizondo R., Llanos P., Uranga R.M., Nualart F., Garcia M.A. MCT expression and lactate influx/efflux in tanycytes involved in glia-neuron metabolic interaction. PLoS ONE 2011, 6. 10.1371/journal.pone.0016411.
19. Costantini L.C., Vogel J.L., Barr L.J., Henderson S.T. Clinical efficacy of AC-1202 (AC-1202TM) in mild to moderate Alzheimer's disease 2007, Proceedings of the 59th Annual Meeting of the American Academy of Neurology Conference; 28 April to 5 May 2007; Boston, MA.
20. Cserjési R., Molnár D., Luminet O., Lénárd L. Is there any relationship between obesity and mental flexibility in children?. Appetite 2007, 49:675-678. 10.1016/j.appet.2007.04.001.
21. de la Monte S.M. Insulin resistance and Alzheimer's disease. BMB Reports 2009, 42:475.
22. Davidson T.L., Hargrave S.L., Swithers S.E., Sample C.H., Fu X., Kinzig K.P., et al. Inter-relationships among diet, obesity and hippocampal-dependent cognitive function. Neuroscience 2013, 253:110-122. 10.1016/j.neuroscience.2013.08.044.
23. Davidson T.L., Kanoski S.E., Schier L.A., Clegg D.J., Benoit S.C. A potential role for the hippocampus in energy intake and body weight regulation. Current Opinion in Pharmacology 2007, 7:613-616.
24. Davidson T.L., Monnot A., Neal A.U., Martin A.A., Horton J.J., 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. Physiology & Behavior 2012, 107:26-33.
25. De Vivo D.C., Trifiletti R.R., Jacobson R.I., Ronen G.M., Behmand R.A., Harik S.I. Defective glucose transport across the blood-brain barrier as a cause of persistent hypoglycorrhachia, seizures, and developmental delay. The New England Journal of Medicine 1991, 325:703-709. 10.1056/NEJM199109053251006.
26. De Vivo D.C., Wang D. Glut1 deficiency. CSF glucose. How low is too low?. Revue Neurologique 2008, 164:877-880. 10.1016/j.neurol.2008.10.001.
27. Delgado-Rico E., Río-Valle J.S., González-Jiménez E., Campoy C., Verdejo-García A. BMI predicts emotion-driven impulsivity and cognitive inflexibility in adolescents with excess weight. Obesity 2012, 20:1604-1610. 10.1038/oby.2012.47.
28. Dember W.N., Fowler H. Spontaneous alternation behavior. Psychological Bulletin 1958, 55:412-428. 10.1037/h0045446.
29. Deshmukh-Taskar P., Nicklas T.A., Morales M., Yang S.J., Zakeri I., Berenson G.S. Tracking of overweight status from childhood to young adulthood. The Bogalusa Heart Study. European Journal of Clinical Nutrition 2005, 60(1):48-57.
30. Ding F., Yao J., Rettberg J.R., Chen S., Brinton R.D. Early decline in glucose transport and metabolism precedes shift to ketogenic system in female aging and alzheimer's mouse brain. Implication for bioenergetic intervention. PLoS ONE 2013, 8. 10.1371/journal.pone.0079977.
31. Ding F., Yao J., Zhao L., Mao Z., Chen S., Brinton R.D. Ovariectomy induces a shift in fuel availability and metabolism in the hippocampus of the female transgenic model of familial Alzheimer's. PLoS ONE 2013, 8:e59825. 10.1371/journal.pone.0059825.
32. Divac I., Wikmark R.G.E., Gade A. Spontaneous alternation in rats with lesions in the frontal lobes. An extension of the frontal lobe syndrome. Physiological Psychology 1975, 3:39-42. 10.3758/BF03326820.
33. Ekdahl C.T., Kokaia Z., Lindvall O. Brain inflammation and adult neurogenesis. The dual role of microglia. Neuroscience 2009, 158(3):1021-1029.
34. Estes W.K., Schoeffler M.S. Analysis of variables influencing alternation after forced trials. Journal of Comparative and Physiological Psychology 1955, 48:357-362. 10.1037/h0043836.
35. Flegal K.M., Carroll M.D., Ogden C.L., Curtin L.R. Prevalence and trends in obesity among US adults, 1999-2008. JAMA. The Journal of the American Medical Association 2010, 303:235-241.
36. Forsythe C.E., Phinney S.D., Fernandez M.L., Quann E.E., Wood R.J., Bibus D.M., et al. Comparison of low fat and low carbohydrate diets on circulating fatty acid composition and markers of inflammation. Lipids 2008, 43:65-77.
37. Friedman J.R.L., Thiele E.A., Wang D., Levine K.B., Cloherty E.K., Pfeifer H.H., et al. Atypical GLUT1 deficiency with prominent movement disorder responsive to ketogenic diet. Movement Disorders. Official Journal of the Movement Disorder Society 2006, 21:241-245. 10.1002/mds.20660.
38. Gerlai R. A new continuous alternation task in T-maze detects hippocampal dysfunction in mice. A strain comparison and lesion study. Behavioural Brain Research 1998, 95:91-101. 10.1016/S0166-4328(97)00214-3.
39. Henderson S.T., Vogel J.L., Barr L.J., Garvin F., Jones J.J., Costantini L.C. Study of the ketogenic agent AC-1202 in mild to moderate Alzheimer's disease. A randomized, double-blind, placebo-controlled, multicenter trial. Nutrition and Metabolism 2009, 6:31.
40. Hu D., Amsel A. A simple test of the vicarious trial-and-error hypothesis of hippocampal function. Proceedings of the National Academy of Sciences of the United States of America 1995, 92:5506-5509.
41. Kaczmarczyk M.M., Machaj A.S., Chiu G.S., Lawson M.A., Gainey S.J., York J.M., et al. Methylphenidate prevents high-fat diet (HFD)-induced learning/memory impairment in juvenile mice. Psychoneuroendocrinology 2013, 38:1553-1564. 10.1016/j.psyneuen.2013.01.004.
42. Kalaria R.H.N., Harik S.I. Reduced glucose transporter at the blood-brain barrier and in cerebral cortex in Alzheimer disease. Journal of Neurochemistry 1989, 53:1083-1088.
43. Kamijo K., Khan N.A., Pontifex M.B., Scudder M.R., Drollette E.S., Raine L.B., et al. The relation of adiposity to cognitive control and scholastic achievement in preadolescent children. Obesity 2012, 20(12):2406-2411.
44. Kamijo K., Pontifex M.B., Khan N.A., Raine L.B., Scudder M.R., Drollette E.S., et al. The negative association of childhood obesity to cognitive control of action monitoring. Cerebral Cortex 2014, 24(3):654-662.
45. Kanoski S.E., Davidson T.L. Western diet consumption and cognitive impairment. Links to hippocampal dysfunction and obesity. Physiology & Behavior 2011, 103:59-68.
46. Kanoski S.E., Meisel R.L., Mullins A.J., Davidson T.L. The effects of energy-rich diets on discrimination reversal learning and on BDNF in the hippocampus and prefrontal cortex of the rat. Behavioural Brain Research 2007, 182:57-66.
47. Kanoski S.E., Zhang Y., Zheng W., Davidson T.L. The effects of a high-energy diet on hippocampal function and blood-brain barrier integrity in the rat. Journal of Alzheimer's Disease 2010, 21:207-219.
48. Kinzig K.P., Hargrave S.L., Hyun J., Moran T.H. Energy balance and hypothalamic effects of a high-protein/low-carbohydrate diet. Physiology & Behavior 2007, 92(3):454-460.
49. Kinzig K.P., Honors M.A., Hargrave S.L. Insulin sensitivity and glucose tolerance are altered by maintenance on a ketogenic diet. Endocrinology 2010, 151(7):3105-3114.
50. König B., Koch A., Giggel K., Dordschbal B., Eder K., Stangl G.I. Monocarboxylate transporter (MCT)-1 is up-regulated by PPARα. Biochimica et Biophysica Acta 2008, 1780(6):899-904. http://dx.doi.org/10.1016/j.bbagen.2008.03.002.
51. Kumagai A.K., Kang Y.-S., Boado R.J., Pardridge W.M. Upregulation of blood-brain barrier GLUT1 glucose transporter protein and mRNA in experimental chronic hypoglycemia. Diabetes 1995, 44:1399-1404. 10.2337/diab.44.12.1399.
52. Kwon Y.S., Jeong S.-W., Kim D.W., Choi E.S., Son B.K. Effects of the ketogenic diet on neurogenesis after kainic acid-induced seizures in mice. Epilepsy Research 2008, 78:186-194.
53. Lalonde R. The neurobiological basis of spontaneous alternation. Neuroscience & Biobehavioral Reviews 2002, 26:91-104. 10.1016/S0149-7634(01)00041-0.
54. Leino R.L., Gerhart D.Z., Duelli R., Enerson B.E., Drewes L.R. Diet-induced ketosis increases monocarboxylate transporter (MCT1) levels in rat brain. Neurochemistry International 2001, 38:519-527. 10.1016/S0197-0186(00)00102-9.
55. Lennartz R. The role of extramaze cues in spontaneous alternation in a plus-maze. Learning & Behavior 2008, 36(2):138-144. 10.3758/LB.36.2.138.
56. Lipska B.K., Aultman J.M., Verma A., Weinberger D.R., Moghaddam B. Neonatal damage of the ventral hippocampus impairs working memory in the rat. Neuropsychopharmacology 2002, 27:47-54. 10.1016/S0893-133X(02)00282-8.
57. Lutas A., Yellen G. The ketogenic diet. Metabolic influences on brain excitability and epilepsy. Trends in Neurosciences 2013, 36(1):32-40.
58. Maher F., Vannucci S.J., Simpson I.A. Glucose transporter proteins in brain. FASEB Journal. Official Publication of the Federation of American Societies for Experimental Biology 1994, 8:1003-1011.
59. Maurer M.H., Canis M., Kuschinsky W., Duelli R. Correlation between local monocarboxylate transporter 1 (MCT1) and glucose transporter 1 (GLUT1) densities in the adult rat brain. Neuroscience Letters 2004, 355:105-108. 10.1016/j.neulet.2003.10.056.
60. McCall A.L., Van Bueren A.M., Nipper V., Moholt-Siebert M., Downes H., Lessov N. Forebrain ischemia increases Glut1 protein in brain microvessels and parenchyma. Journal of Cerebral Blood Flow and Metabolism 1996, 16(1):69-76.
61. Molteni R., Barnard R.J., Ying Z., Roberts C.K., Gomez-Pinilla F. A high-fat, refined sugar diet reduces hippocampal brain-derived neurotrophic factor, neuronal plasticity, and learning. Neuroscience 2002, 112:803-814.
62. Mooradian A., Chung H., Shah G. GLUT-1 expression in the cerebra of patients with Alzheimer's disease. Neurobiology of Aging 1997, 18:469-474.
63. Mosconi L. Brain glucose metabolism in the early and specific diagnosis of Alzheimer's disease. European Journal of Nuclear Medicine and Molecular Imaging 2005, 32:486-510. 10.1007/s00259-005-1762-7.
64. Mosconi L., Mistur R., Switalski R., Tsui W.H., Glodzik L., Li Y., et al. FDG-PET changes in brain glucose metabolism from normal cognition to pathologically verified Alzheimer's disease. European Journal of Nuclear Medicine and Molecular Imaging 2009, 36:811-822. 10.1007/s00259-008-1039-z.
65. Nagase H., Bray G.A., York D.A. Pyruvate and hepatic pyruvate dehydrogenase levels in rat strains sensitive and resistant to dietary obesity. American Journal of Physiology - Regulatory Integrative and Comparative Physiology 1996, 270(3):R489-R495.
66. Nehlig A. Brain uptake and metabolism of ketone bodies in animal models. Prostaglandins, Leukotrienes, and Essential Fatty Acids 2004, 70:265-275. 10.1016/j.plefa.2003.07.006.
67. Ogden C.L., Carroll M.D., Kit B.K., Flegal K.M. Prevalence of childhood and adult obesity in the United States, 2011-2012. JAMA. The Journal of the American Medical Association 2014, 311(8):806-814.
68. Packard M.G., McGaugh J.L. Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiology of Learning and Memory 1996, 65:65-72. 10.1006/nlme.1996.0007.
69. Pardridge W.M., Triguero D., Farrell C.R. Downregulation of blood-brain barrier glucose transporter in experimental diabetes. Diabetes 1990, 39:1040-1044.
70. Pellerin L., Bouzier-Sore A.-K., Aubert A., Serres S., Merle M., Costalat R., et al. Activity-dependent regulation of energy metabolism by astrocytes. An update. Glia 2007, 55:1251-1262. 10.1002/glia.20528.
71. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 2001, 29:e45.
72. Pistell P.J., Morrison C.D., Gupta S., Knight A.G., Keller J.N., Ingram D.K., et al. Cognitive impairment following high fat diet consumption is associated with brain inflammation. Journal of Neuroimmunology 2010, 219:25-32.
73. Qutub A.A., Hunt C.A. Glucose transport to the brain. A systems model. Brain Research Reviews 2005, 49:595-617. 10.1016/j.brainresrev.2005.03.002.
74. Ramm-Pettersen A., Stabell K.E., Nakken K.O., Selmer K.K. Does ketogenic diet improve cognitive function in patients with GLUT1-DS? A 6- to 17-month follow-up study. Epilepsy & Behavior 2014, 39:111-115. 10.1016/j.yebeh.2014.08.015.
75. Roberts L.M., Black D.S., Raman C., Woodford K., Zhou M., Haggerty J.E., et al. Subcellular localization of transporters along the rat blood-brain barrier and blood-cerebral-spinal fluid barrier by in vivo biotinylation. Neuroscience 2008, 155:423-438. 10.1016/j.neuroscience.2008.06.015.
76. Schaefer C.A., Brown A.S., Wyatt R.J., Kline J., Begg M.D., Bresnahan M.A., et al. Maternal prepregnant body mass and risk of schizophrenia in adult offspring. Schizophrenia Bulletin 2000, 26(2):275-286.
77. Schmidt B., Papale A., Redish A.D., Markus E.J. Conflict between place and response navigation strategies. Effects on vicarious trial and error (VTE) behaviors. Learning & Memory (Cold Spring Harbor, N.Y.) 2013, 20:130-138. 10.1101/lm.028753.112.
78. Schurr A., West C.A., Rigor B.M. Lactate-supported synaptic function in the rat hippocampal slice preparation. Science 1988, 240(4857):1326-1328. 10.1126/science.3375817.
79. Sharman M.J., Kraemer W.J., Love D.M., Avery N.G., Gómez A.L., Scheett T.P., et al. A ketogenic diet favorably affects serum biomarkers for cardiovascular disease in normal-weight men. The Journal of Nutrition 2002, 132:1879-1885.
80. Sharman M.J., Volek J.S. Weight loss leads to reductions in inflammatory biomarkers after a very-low-carbohydrate diet and a low-fat diet in overweight men. Clinical Science 2004, 107:365-370.
81. Stefani M.R., Nicholson G.M., Gold P.E. ATP-sensitive potassium channel blockade enhances spontaneous alternation performance in the rat. A potential mechanism for glucose-mediated memory enhancement. Neuroscience 1999, 93:557-563.
82. Stranahan A.M., Norman E.D., Lee K., Cutler R.G., Telljohann R.S., Egan J.M., et al. Diet-induced insulin resistance impairs hippocampal synaptic plasticity and cognition in middle-aged rats. Hippocampus 2008, 18:1085-1088.
83. Suddendorf T., Corballis M.C. The evolution of foresight. What is mental time travel, and is it unique to humans?. Behavioral and Brain Sciences 2007, 30:299-313. 10.1017/S0140525X07001975.
84. Suzuki A., Stern S.A., Bozdagi O., Huntley G.W., Walker R.H., Magistretti P.J., et al. Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 2011, 144:810-823. 10.1016/j.cell.2011.02.018.
85. van der Meer M., Kurth-Nelson Z., Redish A.D. Information processing in decision-making systems. The Neuroscientist. A Review Journal Bringing Neurobiology, Neurology and Psychiatry 2012, 18:342-359. 10.1177/1073858411435128.
86. Van der Auwera I., Wera S., Van Leuven F., Henderson S.T. A ketogenic diet reduces amyloid beta 40 and 42 in a mouse model of Alzheimer's disease. Nutrition & Metabolism 2005, 2:28.
87. Vannucci S.J., Simpson I.A. Developmental switch in brain nutrient transporter expression in the rat. American Journal of Physiology. Endocrinology and Metabolism 2003, 285:E1127-E1134. 10.1152/ajpendo.00187.2003.
88. Volek J., Sharman M., Gomez A., Judelson D.A., Rubin M.R., Watson G., et al. Comparison of energy-restricted very low-carbohydrate and low-fat diets on weight loss and body composition in overweight men and women. Nutrition and Metabolism 2004, 1:13.
89. Voss J.L., Warren D.E., Gonsalves B.D., Federmeier K.D., Tranel D., Cohen N.J. Spontaneous revisitation during visual exploration as a link among strategic behavior, learning, and the hippocampus. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:E402-E409. 10.1073/pnas.1100225108.
90. Wang Y., Beydoun M.A., Liang L., Caballero B., Kumanyika S.K. Will all Americans become overweight or obese? Estimating the progression and cost of the US obesity epidemic. Obesity 2008, 16:2323-2330.
91. Whitmer R.A., Gunderson E.P., Barrett-Connor E., Quesenberry C.P., Yaffe K. Obesity in middle age and future risk of dementia. A 27 year longitudinal population based study. BMJ (Clinical Research Ed.) 2005, 330:1360.
92. Wu A., Ying Z., Gomez-Pinilla F. The interplay between oxidative stress and brain-derived neurotrophic factor modulates the outcome of a saturated fat diet on synaptic plasticity and cognition. European Journal of Neuroscience 2004, 19:1699-1707.
93. Wu Z., Guo H., Chow N., Sallstrom J., Bell R.D., Deane R., et al. Role of the MEOX2 homeobox gene in neurovascular dysfunction in Alzheimer disease. Nature Medicine 2005, 11:959-965.
94. Yadin E., Friedman E., Bridger W.H. Spontaneous alternation behavior. An animal model for obsessive-compulsive disorder?. Pharmacology, Biochemistry, and Behavior 1991, 40:311-315. 10.1016/0091-3057(91)90559-K.
95. Yau P.L., Castro M.G., Tagani A., Tsui W.H., Convit A. Obesity and metabolic syndrome and functional and structural brain impairments in adolescence. Pediatrics 2012, 130(4):e856-e864.
96. Zilberter Y., Zilberter T., Bregestovski P. Neuronal activity in vitro and the in vivo reality. The role of energy homeostasis. Trends in Pharmacological Sciences 2010, 31:394-401. 10.1016/j.tips.2010.06.005.