Maternal obesity caused by overnutrition exposure leads to reversal learning deficits and striatal disturbance in rats

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Wu, Ting ^a,b,c   Deng, Shining ^b   Li, Wei Guang ^b   Yu, Yongguo ^b   Li, Fei ^b   Mao, Meng ^a,c  

^a SICHUAN UNIVERSITY   (China)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c CHENGDU WOMEN S AND CHILDREN S CENTRAL HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

LEPTIN; STAT3 PROTEIN;

ADULT; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; BREEDING; CONTROLLED STUDY; DOPAMINE HOMEOSTASIS; FEMALE; FOOD INTAKE; HOMEOSTASIS; LEARNING DISORDER; LIPID DIET; LOCOMOTION; MALE; MATERNAL NUTRITION; MATERNAL OBESITY; NEUROLOGIC DISEASE; NONHUMAN; OVERNUTRITION; PREGNANCY OUTCOME; RAT; STRIATAL DISTURBANCE; VISUAL DISCRIMINATION;

ANIMALS; BLOTTING, WESTERN; COGNITION DISORDERS; CORPUS STRIATUM; DOPAMINE; FEEDING BEHAVIOR; FEMALE; HYPOTHALAMUS; MALE; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; MOTOR ACTIVITY; OBESITY; OVERNUTRITION; PHOSPHORYLATION; PREGNANCY; PREGNANCY COMPLICATIONS; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, WISTAR; REVERSAL LEARNING; STAT3 TRANSCRIPTION FACTOR;

EID: 84892410788     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0078876     Document Type: Article

References (44)

1. Gallou-Kabani C, Junien C (2005) Nutritional epigenomics of metabolic syndrome: new perspective against the epidemic. Diabetes 54: 1899-1906.
2. Harding JE (2001) The nutritional basis of the fetal origins of adult disease. Int J Epidemiol 30: 15-23.
3. Basatemur E, Gardiner J, Williams C, Melhuish E, Barnes J, et al. (2013) Maternal prepregnancy BMI and child cognition: a longitudinal cohort study. Pediatrics 131: 56-63.
4. Bilbo SD, Tsang V (2010) Enduring consequences of maternal obesity for brain inflammation and behavior of offspring. FASEB J 24: 2104-2115.
5. Tozuka Y, Kumon M, Wada E, Onodera M, Mochizuki H, et al. (2010) Maternal obesity impairs hippocampal BDNF production and spatial learning performance in young mouse offspring. Neurochem Int 57: 235-247.
6. Tozuka Y, Wada E, Wada K (2009) Diet-induced obesity in female mice leads to peroxidized lipid accumulations and impairment of hippocampal neurogenesis during the early life of their offspring. FASEB J 23: 1920-1934.
7. Elliott R, McKenna PJ, Robbins TW, Sahakian BJ (1995) Neuropsychological evidence for frontostriatal dysfunction in schizophrenia. Psychol Med 25: 619-630.
8. Hill EL (2004) Executive dysfunction in autism. Trends Cogn Sci 8: 26-32.
9. Pantelis C, Barber FZ, Barnes TR, Nelson HE, Owen AM, et al. (1999) Comparison of set-shifting ability in patients with chronic schizophrenia and frontal lobe damage. Schizophr Res 37: 251-270.
10. Traykov L, Raoux N, Latour F, Gallo L, Hanon O, et al. (2007) Executive functions deficit in mild cognitive impairment. Cogn Behav Neurol 20: 219-224.
11. Peterson DA, Elliott C, Song DD, Makeig S, Sejnowski TJ, et al. (2009) Probabilistic reversal learning is impaired in Parkinson's disease. Neuroscience 163: 1092-1101.
12. Kehagia AA, Murray GK, Robbins TW (2010) Learning and cognitive flexibility: frontostriatal function and monoaminergic modulation. Curr Opin Neurobiol 20: 199-204.
13. Castañé A, Theobald DE, Robbins TW (2010) Selective lesions of the dorsomedial striatum impair serial spatial reversal learning in rats. Behav Brain Res 210: 74-83.
14. Clarke HF, Robbins TW, Roberts AC (2008) Lesions of the medial striatum in monkeys produce perseverative impairments during reversal learning similar to those produced by lesions of the orbitofrontal cortex. J Neurosci 28: 10972-10982.
15. Jones B, Mishkin M (1972) Limbic lesions and the problem of stimulus - reinforcement associations. Exp Neurol 36: 362-377.
16. Dias R, Robbins TW, Roberts AC (1996) Dissociation in prefrontal cortex of affective and attentional shifts. Nature 380: 69-72.
17. Chudasama Y, Robbins TW (2003) Dissociable contributions of the orbitofrontal and infralimbic cortex to pavlovian autoshaping and discrimination reversal learning: further evidence for the functional heterogeneity of the rodent frontal cortex. J Neurosci 23: 8771-8780.
18. Izquierdo A, Belcher AM, Scott L, Cazares VA, Chen J, et al. (2010) Reversal-specific learning impairments after a binge regimen of methamphetamine in rats: possible involvement of striatal dopamine. Neuropsychopharmacology 35: 505-514.
19. Paxinos G, Watson C, editors (2003) The rat brain atlas in stereotaxic coordinates. 5th edition: Academic Press: San Diego.
20. Couvreur O, Ferezou J, Gripois D, Serougne C, Crépin D, et al. (2011) Unexpected long-term protection of adult offspring born to high-fat fed dams against obesity induced by a sucrose-rich diet. PLoS One 6: e18043.
21. van der Meulen JA, Joosten RN, de Bruin JP, Feenstra MG (2007) Dopamine and noradrenaline efflux in the medial prefrontal cortex during serial reversals and extinction of instrumental goal-directed behavior. Cereb Cortex 17: 1444-1453.
22. Burghardt PR, Love TM, Stohler CS, Hodgkinson C, Shen PH, et al. (2012) Leptin regulates dopamine responses to sustained stress in humans. J Neurosci 32: 15369-15376.
23. Myers MG, Jr., Munzberg H, Leinninger GM, Leshan RL (2009) The geometry of leptin action in the brain: more complicated than a simple ARC. Cell Metabolism 9: 117-123.
24. Ruager-Martin R, Hyde MJ, Modi N (2010) Maternal obesity and infant outcomes. Early Hum Dev 86: 715-722.
25. Sebire NJ, Jolly M, Harris JP, Wadsworth J, Joffe M, et al. (2001) Maternal obesity and pregnancy outcome: a study of 287,213 pregnancies in London. Int J Obes Relat Metab Disord 25: 1175-1182.
26. Boney CM, Verma A, Tucker R, Vohr BR (2005) Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics 115: e290-296.
27. Férézou-Viala J, Roy AF, Sérougne C, Gripois D, Parquet M, et al. (2007) Long-term consequences of maternal high-fat feeding on hypothalamic leptin sensitivity and diet-induced obesity in the offspring. Am J Physiol Regul Integr Comp Physiol 293: R1056-1062.
28. Rodriguez A (2010) Maternal pre-pregnancy obesity and risk for inattention and negative emotionality in children. J Child Psychol Psychiatry 51: 134-143.
29. Rodriguez A, Miettunen J, Henriksen TB, Olsen J, Obel C, et al. (2008) Maternal adiposity prior to pregnancy is associated with ADHD symptoms in offspring: evidence from three prospective pregnancy cohorts. Int J Obes (Lond) 32: 550-557.
30. Gorski JN, Dunn-Meynell AA, Hartman TG, Levin BE (2006) Postnatal environment overrides genetic and prenatal factors influencing offspring obesity and insulin resistance. Am J Physiol Regul Integr Comp Physiol 291: R768-778.
31. Guo F, Jen KL (1995) High-fat feeding during pregnancy and lactation affects offspring metabolism in rats. Physiol Behav 57: 681-686.
32. Birrell JM, Brown VJ (2000) Medial frontal cortex mediates perceptual attentional set shifting in the rat. J Neurosci 20: 4320-4324.
33. Bussey TJ, Everitt BJ, Robbins TW (1997) Dissociable effects of cingulate and medial frontal cortex lesions on stimulus-reward learning using a novel Pavlovian autoshaping procedure for the rat: implications for the neurobiology of emotion. Behav Neurosci 111: 908-919.
34. Bussey TJ, Muir JL, Everitt BJ, Robbins TW (1997) Triple dissociation of anterior cingulate, posterior cingulate, and medial frontal cortices on visual discrimination tasks using a touchscreen testing procedure for the rat. Behav Neurosci 111: 920-936.
35. Ragozzino M (2007) The contribution of the medial prefrontal cortex, orbitofrontal cortex, and dorsomedial striatum to behavioral flexibility. Ann N Y Acad Sci 1121: 355-375.
36. Tait DS, Brown VJ (2007) Difficulty overcoming learned non-reward during reversal learning in rats with ibotenic acid lesions of orbital prefrontal cortex. Annals of the New York Academy of Sciences 1121: 407-420.
37. Tait D, Brown VJ. (2008) Lesions of the basal forebrain impair reversal learning but not shifting of attentional set in rats. Behav. Brain Res 187: 100-108.
38. Devauges V, Sara SJ (1990) Activation of the noradrenergic system facilitates an attentional shift in the rat. Behav Brain Res 39: 19-28.
39. Lapiz MD, Morilak DA (2006) Noradrenergic modulation of cognitive function in rat medial prefrontal cortex as measured by attentional set shifting capability. Neuroscience 137: 1039-1049.
40. Gobert A, Rivet JM, Cistarelli L, Melon C, Millan MJ (1997) Alpha2-adrenergic receptor blockade markedly potentiates duloxetine- and fluoxetine-induced increases in noradrenaline, dopamine, and serotonin levels in the frontal cortex of freely moving rats. J Neurochem 69: 2616-2619.
41. Matsumoto M, Yoshioka M, Togashi H, Mori K, Ueno K, et al. (1998) Effects of idazoxan on dopamine release in the prefrontal cortex of freely moving rats. Eur J Pharmacol 343: 165-170.
42. Williams KW, Scott MM, Elmquist JK (2009) From observation to experimentation: leptin action in the mediobasal hypothalamus. Am J Clin Nutr 89: 985S-990S.
43. Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, et al. (1996) Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med 334: 292-295.
44. Ring LE, Zeltser LM (2010) Disruption of hypothalamic leptin signaling in mice leads to early-onset obesity, but physiological adaptations in mature animals stabilize adiposity levels. J Clin Invest 120: 2931-2941.