Neurochemical and electrophysiological deficits in the ventral hippocampus and selective behavioral alterations caused by high-fat diet in female C57BL/6 mice

Neuroscience

Volumn 297, Issue , 2015, Pages 170-181

  Krishna, S ^a   Keralapurath, M M ^a   Lin, Z ^a   Wagner, J J ^a   de La Serre, C B ^b   Harn, D A ^a   Filipov, N M ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

Anxiety; Dopamine; High fat diet (HFD); Long term potentiation (LTP); Ventral hippocampus (vHIP)

Indexed keywords

4 HYDROXY 3 METHOXYPHENYLETHYLENE GLYCOL; 5 HYDROXYINDOLEACETIC ACID; BRAIN MONOAMINE; DIHYDROXYPHENYLACETIC ACID; DOPAMINE; HOMOVANILLIC ACID; NORADRENALIN; SEROTONIN; BIOGENIC AMINE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; BEHAVIOR DISORDER; BRAIN ELECTROPHYSIOLOGY; BRAIN LEVEL; BRAIN SLICE; C57BL 6 MOUSE; COGNITION; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE METABOLISM; DORSAL HIPPOCAMPUS; EMOTIONAL DISORDER; ESTRUS CYCLE; EX VIVO STUDY; EXPERIMENTAL BEHAVIORAL TEST; FEMALE; FORCED SWIM TEST; GRIP STRENGTH TEST; HIPPOCAMPUS; LIPID DIET; LOCOMOTION; LONG TERM POTENTIATION; MARBLE BURYING TEST; MOUSE; NERVE CELL PLASTICITY; NERVOUS SYSTEM PARAMETERS; NEUROCHEMISTRY; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; NUCLEUS ACCUMBENS; OPEN FIELD TEST; PAIRED PULSE RATIO; POLE TEST; PREFRONTAL CORTEX; PRIORITY JOURNAL; VENTRAL HIPPOCAMPUS; YOUNG ADULT; ADVERSE EFFECTS; ANALYSIS OF VARIANCE; ANIMAL; ANIMAL BEHAVIOR; BODY WEIGHT; BRAIN DISEASES; C57BL MOUSE; EATING; ELECTROSTIMULATION; EXPLORATORY BEHAVIOR; METABOLISM; MUSCLE STRENGTH; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY; PSYCHOMOTOR PERFORMANCE; SWIMMING;

ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; BIOGENIC MONOAMINES; BODY WEIGHT; BRAIN DISEASES; DIET, HIGH-FAT; EATING; ELECTRIC STIMULATION; ESTROUS CYCLE; EXPLORATORY BEHAVIOR; FEMALE; HIPPOCAMPUS; LONG-TERM POTENTIATION; MICE; MICE, INBRED C57BL; MUSCLE STRENGTH; PSYCHOMOTOR PERFORMANCE; SWIMMING;

EID: 84927747505     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.03.068     Document Type: Article

References (74)

1. Adhikari A., Topiwala M.A., Gordon J.A. Synchronized activity between the ventral hippocampus and the medial prefrontal cortex during anxiety. Neuron 2010, 65:257-269.
2. An X.L., Zou J.X., Wu R.Y., Yang Y., Tai F.D., Zeng S.Y., Jia R., Zhang X., Liu E.Q., Broders H. Strain and sex differences in anxiety-like and social behaviors in C57BL/6J and BALB/cJ mice. Exp Anim 2011, 60:111-123.
3. Anchan D., Clark S., Pollard K., Vasudevan N. GPR30 activation decreases anxiety in the open field test but not in the elevated plus maze test in female mice. Brain Behav 2014, 4:51-59.
4. Antunes M., Biala G. The novel object recognition memory: neurobiology, test procedure, and its modifications. Cogn Process 2012, 13:93-110.
5. Balasubramanian P., Jagannathan L., Mahaley R.E., Subramanian M., Gilbreath E.T., Mohankumar P.S., Mohankumar S.M. High fat diet affects reproductive functions in female diet-induced obese and dietary resistant rats. J Neuroendocrinol 2012, 24:748-755.
6. Balkaya M., Krober J.M., Rex A., Endres M. Assessing post-stroke behavior in mouse models of focal ischemia. J Cereb Blood Flow Metab 2013, 33:330-338.
7. Bannerman D.M., Rawlins J.N., McHugh S.B., Deacon R.M., Yee B.K., Bast T., Zhang W.N., Pothuizen H.H., Feldon J. Regional dissociations within the hippocampus - memory and anxiety. Neurosci Biobehav Rev 2004, 28:273-283.
8. Beery A.K., Zucker I. Sex bias in neuroscience and biomedical research. Neurosci Biobehav Rev 2011, 35:565-572.
9. Bray G.A., Paeratakul S., Popkin B.M. Dietary fat and obesity: a review of animal, clinical and epidemiological studies. Physiol Behav 2004, 83:549-555.
10. Brooks S.P., Dunnett S.B. Tests to assess motor phenotype in mice: a user's guide. Nat Rev Neurosci 2009, 10:519-529.
11. Caligioni CS (2009) Assessing reproductive status/stages in mice. Curr Protoc Neurosci Appendix 4: Appendix 4I.
12. Carey A.N., Gomes S.M., Shukitt-Hale B. Blueberry supplementation improves memory in middle-aged mice fed a high-fat diet. J Agric Food Chem 2014, 62:3972-3978.
13. Castagne V, Moser P, Roux S, Porsolt RD (2011) Rodent models of depression: forced swim and tail suspension behavioral despair tests in rats and mice. Curr Protoc Neurosci Chapter 8: Unit 8 10A.
14. Chudasama H.P., Bhatt P.A. Evaluation of anti-obesity activity of duloxetine in comparison with sibutramine along with its anti-depressant activity: an experimental study in obese rats. Can J Physiol Pharmacol 2009, 87:900-907.
15. Coban A., Filipov N.M. Dopaminergic toxicity associated with oral exposure to the herbicide atrazine in juvenile male C57BL/6 mice. J Neurochem 2007, 100:1177-1187.
16. Collins S., Martin T.L., Surwit R.S., Robidoux J. Genetic vulnerability to diet-induced obesity in the C57BL/6J mouse: physiological and molecular characteristics. Physiol Behav 2004, 81:243-248.
17. Cone J.J., Chartoff E.H., Potter D.N., Ebner S.R., Roitman M.F. Prolonged high fat diet reduces dopamine reuptake without altering DAT gene expression. PLoS One 2013, 8:e58251.
18. Cyrenne D.L., Brown G.R. Effects of suppressing gonadal hormones on response to novel objects in adolescent rats. Horm Behav 2011, 60:625-631.
19. Davis J.F., Tracy A.L., Schurdak J.D., Tschop M.H., Lipton J.W., Clegg D.J., Benoit S.C. Exposure to elevated levels of dietary fat attenuates psychostimulant reward and mesolimbic dopamine turnover in the rat. Behav Neurosci 2008, 122:1257-1263.
20. Del Rosario A., McDermott M.M., Panee J. Effects of a high-fat diet and bamboo extract supplement on anxiety- and depression-like neurobehaviours in mice. Br J Nutr 2012, 108:1143-1149.
21. Diz-Chaves Y., Kwiatkowska-Naqvi A., Von Hulst H., Pernia O., Carrero P., Garcia-Segura L.M. Behavioral effects of estradiol therapy in ovariectomized rats depend on the age when the treatment is initiated. Exp Gerontol 2012, 47:93-99.
22. Fanselow M.S., Dong H.W. Are the dorsal and ventral hippocampus functionally distinct structures?. Neuron 2010, 65:7-19.
23. Fleming S.M., Salcedo J., Fernagut P.O., Rockenstein E., Masliah E., Levine M.S., Chesselet M.F. Early and progressive sensorimotor anomalies in mice overexpressing wild-type human alpha-synuclein. J Neurosci 2004, 24:9434-9440.
24. Gadalla T.M. Association of obesity with mood and anxiety disorders in the adult general population. Chronic Dis Can 2009, 30:29-36.
25. Gaikwad U., Parle M., Kumar A., Gaikwad D. Effect of ritanserin and leuprolide alone and combined on marble-burying behavior of mice. Acta Pol Pharm 2010, 67:523-527.
26. Heyward F.D., Walton R.G., Carle M.S., Coleman M.A., Garvey W.T., Sweatt J.D. Adult mice maintained on a high-fat diet exhibit object location memory deficits and reduced hippocampal SIRT1 gene expression. Neurobiol Learn Mem 2012, 98:25-32.
27. Hilakivi-Clarke L., Cho E., Onojafe I. High-fat diet induces aggressive behavior in male mice and rats. Life Sci 1996, 58:1653-1660.
28. Huang X.F., Yu Y., Zavitsanou K., Han M., Storlien L. Differential expression of dopamine D2 and D4 receptor and tyrosine hydroxylase mRNA in mice prone, or resistant, to chronic high-fat diet-induced obesity. Brain Res Mol Brain Res 2005, 135:150-161.
29. Hwang L.L., Wang C.H., Li T.L., Chang S.D., Lin L.C., Chen C.P., Chen C.T., Liang K.C., Ho I.K., Yang W.S., Chiou L.C. Sex differences in high-fat diet-induced obesity, metabolic alterations and learning, and synaptic plasticity deficits in mice. Obesity (Silver Spring) 2010, 18:463-469.
30. Jurdak N., Kanarek R.B. Sucrose-induced obesity impairs novel object recognition learning in young rats. Physiol Behav 2009, 96:1-5.
31. Kaczmarczyk M.M., Machaj A.S., Chiu G.S., Lawson M.A., Gainey S.J., York J.M., Meling D.D., Martin S.A., Kwakwa K.A., Newman A.F., Woods J.A., Kelley K.W., Wang Y., Miller M.J., Freund G.G. Methylphenidate prevents high-fat diet (HFD)-induced learning/memory impairment in juvenile mice. Psychoneuroendocrinology 2013, 38:1553-1564.
32. Kalueff A.V., Nguyen M. Testing anxiolytic drugs in the C57BL/6J mouse strain. J Pharmacol Toxicol Methods 2014, 69:205-207.
33. Kanter R., Caballero B. Global gender disparities in obesity: a review. Adv Nutr 2012, 3:491-498.
34. Karimi S.A., Salehi I., Komaki A., Sarihi A., Zarei M., Shahidi S. Effect of high-fat diet and antioxidants on hippocampal long-term potentiation in rats: an in vivo study. Brain Res 2013, 1539:1-6.
35. Keralapurath M.M., Clark J.K., Hammond S., Wagner J.J. Cocaine- or stress-induced metaplasticity of LTP in the dorsal and ventral hippocampus. Hippocampus 2014, 24:577-590.
36. Krishna S., Dodd C.A., Hekmatyar S.K., Filipov N.M. Brain deposition and neurotoxicity of manganese in adult mice exposed via the drinking water. Arch Toxicol 2014, 88:47-64.
37. Lai M., Chandrasekera P.C., Barnard N.D. You are what you eat, or are you? The challenges of translating high-fat-fed rodents to human obesity and diabetes. Nutr Diabetes 2014, 4:e135.
38. Lee A.K., Mojtahed-Jaberi M., Kyriakou T., Astarloa E.A., Arno M., Marshall N.J., Brain S.D., O'Dell S.D. Effect of high-fat feeding on expression of genes controlling availability of dopamine in mouse hypothalamus. Nutrition 2010, 26:411-422.
39. Levin B.E., Triscari J., Sullivan A.C. The effect of diet and chronic obesity on brain catecholamine turnover in the rat. Pharmacol Biochem Behav 1986, 24:299-304.
40. Lin Z., Dodd C.A., Filipov N.M. Short-term atrazine exposure causes behavioral deficits and disrupts monoaminergic systems in male C57BL/6 mice. Neurotoxicol Teratol 2013, 39:26-35.
41. Lin Z., Dodd C.A., Xiao S., Krishna S., Ye X., Filipov N.M. Gestational and lactational exposure to atrazine via the drinking water causes specific behavioral deficits and selectively alters monoaminergic systems in C57BL/6 mouse dams, juvenile and adult offspring. Toxicol Sci 2014, 141:90-102.
42. Liu L., Gu H., Zhao Y., An L., Yang J. Glypican 4 may be involved in the adipose tissue redistribution in high-fat feeding C57BL/6J mice with peroxisome proliferators-activated receptor gamma agonist rosiglitazone treatment. Exp Ther Med 2014, 8:1813-1818.
43. Meguid M.M., Fetissov S.O., Varma M., Sato T., Zhang L., Laviano A., Rossi-Fanelli F. Hypothalamic dopamine and serotonin in the regulation of food intake. Nutrition 2000, 16:843-857.
44. Mizunoya W., Ohnuki K., Baba K., Miyahara H., Shimizu N., Tabata K., Kino T., Sato Y., Tatsumi R., Ikeuchi Y. Effect of dietary fat type on anxiety-like and depression-like behavior in mice. SpringerPlus 2013, 2:165.
45. Molteni R., Wu A., Vaynman S., Ying Z., Barnard R.J., Gomez-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, 123:429-440.
46. Moore S.J., Deshpande K., Stinnett G.S., Seasholtz A.F., Murphy G.G. Conversion of short-term to long-term memory in the novel object recognition paradigm. Neurobiol Learn Mem 2013, 105:174-185.
47. Murphy M., Mercer J.G. Diet-regulated anxiety. Int J Endocrinol 2013, 2013:701967.
48. Nishikawa H., Hata T., Itoh E., Funakami Y. A role for corticotropin-releasing factor in repeated cold stress-induced anxiety-like behavior during forced swimming and elevated plus-maze tests in mice. Biol Pharm Bull 2004, 27:352-356.
49. Pechnick R.N., Chesnokova V.M., Kariagina A., Price S., Bresee C.J., Poland R.E. Reduced immobility in the forced swim test in mice with a targeted deletion of the leukemia inhibitory factor (LIF) gene. Neuropsychopharmacology 2004, 29:770-776.
50. Petry N.M., Barry D., Pietrzak R.H., Wagner J.A. Overweight and obesity are associated with psychiatric disorders: results from the National Epidemiologic Survey on Alcohol and Related Conditions. Psychosom Med 2008, 70:288-297.
51. Rachman I.M., Unnerstall J.R., Pfaff D.W., Cohen R.S. Estrogen alters behavior and forebrain c-fos expression in ovariectomized rats subjected to the forced swim test. Proc Natl Acad Sci USA 1998, 95:13941-13946.
52. Rojo M.L., Soderstrom I., Olsson T., Fowler C.J. Changes in cannabinoid CB(1) receptor functionality in the female rat prefrontal cortex following a high fat diet. Life Sci 2013, 92:757-762.
53. Sallis J.F., Glanz K. Physical activity and food environments: solutions to the obesity epidemic. Milbank Q 2009, 87:123-154.
54. Sato M., Kawakami T., Kondoh M., Takiguchi M., Kadota Y., Himeno S., Suzuki S. Development of high-fat-diet-induced obesity in female metallothionein-null mice. FASEB J 2010, 24:2375-2384.
55. Sharma S., Fulton S. Diet-induced obesity promotes depressive-like behaviour that is associated with neural adaptations in brain reward circuitry. Int J Obes (Lond) 2013, 37:382-389.
56. Sharma S., Zhuang Y., Gomez-Pinilla F. High-fat diet transition reduces brain DHA levels associated with altered brain plasticity and behaviour. Sci Rep 2012, 2:431.
57. Sharma S., Fernandes M.F., Fulton S. Adaptations in brain reward circuitry underlie palatable food cravings and anxiety induced by high-fat diet withdrawal. Int J Obes (Lond) 2013, 37:1183-1191.
58. Shi H.S., Yin X., Song L., Guo Q.J., Luo X.H. Neuropeptide Trefoil factor 3 improves learning and retention of novel object recognition memory in mice. Behav Brain Res 2012, 227:265-269.
59. Slattery D.A., Cryan J.F. Using the rat forced swim test to assess antidepressant-like activity in rodents. Nat Protoc 2012, 7:1009-1014.
60. Stefanko D.P., Barrett R.M., Ly A.R., Reolon G.K., Wood M.A. Modulation of long-term memory for object recognition via HDAC inhibition. Proc Natl Acad Sci USA 2009, 106:9447-9452.
61. Stevens G.A., Singh G.M., Lu Y., Danaei G., Lin J.K., Finucane M.M., Bahalim A.N., McIntire R.K., Gutierrez H.R., Cowan M., Paciorek C.J., Farzadfar F., Riley L., Ezzati M. National, regional, and global trends in adult overweight and obesity prevalences. Popul Health Metr 2012, 10:22.
62. Stranahan A.M., Norman E.D., Lee K., Cutler R.G., Telljohann R.S., Egan J.M., Mattson M.P. Diet-induced insulin resistance impairs hippocampal synaptic plasticity and cognition in middle-aged rats. Hippocampus 2008, 18:1085-1088.
63. Swinburn B.A., Caterson I., Seidell J.C., James W.P. Diet, nutrition and the prevention of excess weight gain and obesity. Public Health Nutr 2004, 7:123-146.
64. Terrell D.F. Overweight and obesity prevalence rates among youth in the Carolinas. N C Med J 2002, 63:281-286.
65. Thomas A., Burant A., Bui N., Graham D., Yuva-Paylor L.A., Paylor R. Marble burying reflects a repetitive and perseverative behavior more than novelty-induced anxiety. Psychopharmacology (Berl) 2009, 204:361-373.
66. Thompson A.M., Swant J., Gosnell B.A., Wagner J.J. Modulation of long-term potentiation in the rat hippocampus following cocaine self-administration. Neuroscience 2004, 127:177-185.
67. Vaanholt L.M., Jonas I., Doornbos M., Schubert K.A., Nyakas C., Garland T., Visser G.H., van Dijk G. Metabolic and behavioral responses to high-fat feeding in mice selectively bred for high wheel-running activity. Int J Obes (Lond) 2008, 32:1566-1575.
68. Valladolid-Acebes I., Stucchi P., Cano V., Fernandez-Alfonso M.S., Merino B., Gil-Ortega M., Fole A., Morales L., Ruiz-Gayo M., Del Olmo N. High-fat diets impair spatial learning in the radial-arm maze in mice. Neurobiol Learn Mem 2011, 95:80-85.
69. Valladolid-Acebes I., Merino B., Principato A., Fole A., Barbas C., Lorenzo M.P., Garcia A., Del Olmo N., Ruiz-Gayo M., Cano V. High-fat diets induce changes in hippocampal glutamate metabolism and neurotransmission. Am J Physiol Endocrinol Metab 2012, 302:E396-E402.
70. Wang Y., Beydoun M.A. The obesity epidemic in the United States - gender, age, socioeconomic, racial/ethnic, and geographic characteristics: a systematic review and meta-regression analysis. Epidemiol Rev 2007, 29:6-28.
71. White H.M., Acton A.J., Considine R.V. The angiogenic inhibitor TNP-470 decreases caloric intake and weight gain in high-fat fed mice. Obesity (Silver Spring) 2012, 20:2003-2009.
72. WHO (2000) Obesity: preventing and managing the global epidemic. Report of a WHO consultation. World Health Organ Tech Rep Ser 894:i-xii, 1-253.
73. Yamada N., Katsuura G., Ochi Y., Ebihara K., Kusakabe T., Hosoda K., Nakao K. Impaired CNS leptin action is implicated in depression associated with obesity. Endocrinology 2011, 152:2634-2643.
74. Zarrindast M.R., Naghdi-Sedeh N., Nasehi M., Sahraei H., Bahrami F., Asadi F. The effects of dopaminergic drugs in the ventral hippocampus of rats in the nicotine-induced anxiogenic-like response. Neurosci Lett 2010, 475:156-160.