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Impact of cafeteria feeding during lactation in the rat on novel object discrimination in the offspring

  • Thomas M. Wright (a1), Madeleine V. King (a2), William G. Davey (a1), Simon C. Langley-Evans (a3) and Jörg-Peter W. Voigt (a1)...

Abstract

There is increasing evidence that hyperenergetic diets have an impact on memory in rodents. However, it is largely unknown how diets, such as a cafeteria diet (CD), that mimic a Western-type diet act on learning and memory, in particular when fed during early stages of development. Here, we fed lactating dams a CD and exposed both male and female offspring to a novel object discrimination (NOD) task, a two-trial test of recognition memory in which rats exposed to two identical objects during a training/familiarisation trial can discriminate a novel from a familiar object during the subsequent choice trial. The choice trial was performed following inter-trial interval (ITI) delays of up to 4 h. Maternal diet did not have an impact on exploration of the objects by either sex during the familiarisation trial. Control males discriminated the novel from the familiar object, indicating intact memory with an ITI of 1 h, but not 2 or 4 h. The CD delayed this natural forgetting in male rats such that discrimination was also evident after a 2 h ITI. In contrast, control females exhibited discrimination following both 1 and 2 h ITI, but the CD impaired performance. In summary, the present study shows that maternal exposure to the CD programmes NOD in the adult. In better-performing females, dietary programming interferes with NOD, whereas NOD was improved in males after lactational CD feeding.

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Copyright

Corresponding author

* Corresponding author: J.-P. W. Voigt, fax +44 115 9516440, email peter.voigt@nottingham.ac.uk

References

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1 Stranahan, AM & Mattson, MP (2008) Impact of energy intake and expenditure on neuronal plasticity. Neuromol Med 10, 209218.
2 Winocur, G & Greenwood, CE (2005) Studies of the effects of high fat diets on cognitive function in a rat model. Neurobiol Aging 26, Suppl. 1, 4649.
3 Heyward, FD, Walton, RG, Carle, MS, et al. (2012) Adult mice maintained on a high-fat diet exhibit object location memory deficits and reduced hippocampal SIRT1 gene expression. Neurobiol Learn Mem 98, 2532.
4 Kosari, S, Badoer, E, Nguyen, JC, et al. (2012) Effect of western and high fat diets on memory and cholinergic measures in the rat. Behav Brain Res 235, 98103.
5 McNay, EC, Ong, CT, McCrimmon, RJ, et al. (2010) Hippocampal memory processes are modulated by insulin and high-fat-induced insulin resistance. Neurobiol Learn Mem 93, 546553.
6 Pintana, H, Apaijai, N, Pratchayasakul, W, et al. (2012) Effects of metformin on learning and memory behaviors and brain mitochondrial functions in high fat diet induced insulin resistant rats. Life Sci 91, 409414.
7 Beilharz, JE, Maniam, J & Morris, MJ (2014) 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 37, 134141.
8 Valladolid-Acebes, I, Stucchi, P, Cano, V, et al. (2011) High-fat diets impair spatial learning in the radial-arm maze in mice. Neurobiol Learn Mem 95, 8085.
9 Woo, J, Shin, KO, Park, SY, et al. (2013) Effects of exercise and diet change on cognition function and synaptic plasticity in high fat diet induced obese rats. Lipids Health Dis 12, 144.
10 Davidson, TL, Hargrave, SL, Swithers, SE, et al. (2013) Inter-relationships among diet, obesity and hippocampal-dependent cognitive function. Neuroscience 253, 110122.
11 Jurdak, N & Kanarek, RB (2009) Sucrose-induced obesity impairs novel object recognition learning in young rats. Physiol Behav 96, 15.
12 Ennaceur, A & Delacour, J (1988) A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data. Behav Brain Res 31, 4759.
13 Wu, T, Deng, S, Li, WG, et al. (2013) Maternal obesity caused by overnutrition exposure leads to reversal learning deficits and striatal disturbance in rats. PLOS ONE 8, e78876.
14 Bilbo, SD & Tsang, V (2010) Enduring consequences of maternal obesity for brain inflammation and behavior of offspring. FASEB J 24, 21042115.
15 Rodriguez, JS, Rodriguez-Gonzalez, GL, Reyes-Castro, LA, et al. (2012) Maternal obesity in the rat programs male offspring exploratory, learning and motivation behavior: prevention by dietary intervention pre-gestation or in gestation. Int J Dev Neurosci 30, 7581.
16 Tozuka, Y, Kumon, M, Wada, E, et al. (2010) Maternal obesity impairs hippocampal BDNF production and spatial learning performance in young mouse offspring. Neurochem Int 57, 235247.
17 Sclafani, A & Springer, D (1976) Dietary obesity in adult rats: similarities to hypothalamic and human obesity syndromes. Physiol Behav 17, 461471.
18 Rothwell, NJ & Stock, MJ (1979) Combined effects of cafeteria and tube-feeding on energy balance in the rat. Proc Nutr Soc 38, 5A.
19 Rothwell, NJ & Stock, MJ (1988) The cafeteria diet as a tool for studies of thermogenesis. J Nutr 118, 925928.
20 Prats, E, Monfar, M, Castella, J, et al. (1989) Energy intake of rats fed a cafeteria diet. Physiol Behav 45, 263272.
21 Sampey, BP, Vanhoose, AM, Winfield, HM, et al. (2011) Cafeteria diet is a robust model of human metabolic syndrome with liver and adipose inflammation: comparison to high-fat diet. Obesity (Silver Spring) 19, 11091117.
22 White, CL, Pistell, PJ, Purpera, MN, et al. (2009) Effects of high fat diet on Morris maze performance, oxidative stress, and inflammation in rats: contributions of maternal diet. Neurobiol Dis 35, 313.
23 Bayol, SA, Simbi, BH & Stickland, NC (2005) A maternal cafeteria diet during gestation and lactation promotes adiposity and impairs skeletal muscle development and metabolism in rat offspring at weaning. J Physiol 567, 951961.
24 Benkalfat, NB, Merzouk, H, Bouanane, S, et al. (2011) Altered adipose tissue metabolism in offspring of dietary obese rat dams. Clin Sci (Lond) 121, 1928.
25 Akyol, A, McMullen, S & Langley-Evans, SC (2012) Glucose intolerance associated with early-life exposure to maternal cafeteria feeding is dependent upon post-weaning diet. Br J Nutr 107, 964978.
26 Wright, TM, Fone, KC, Langley-Evans, SC, et al. (2011) Exposure to maternal consumption of cafeteria diet during the lactation period programmes feeding behaviour in the rat. Int J Dev Neurosci 29, 785793.
27 Wright, T, Langley-Evans, SC & Voigt, JP (2011) The impact of maternal cafeteria diet on anxiety-related behaviour and exploration in the offspring. Physiol Behav 103, 164172.
28 Dere, E, Huston, JP & De Souza Silva, MA (2007) The pharmacology, neuroanatomy and neurogenetics of one-trial object recognition in rodents. Neurosci Biobehav Rev 31, 673704.
29 Murphy, M & Mercer, JG (2013) Diet-regulated anxiety. Int J Edocrinol 2013, 701967.
30 Ross, AP, Darling, JN & Parent, MB (2013) High energy diets prevent the enhancing effects of emotional arousal on memory. Behav Neurosci 127, 771779.
31 Akyol, A, Langley-Evans, SC & McMullen, S (2009) Obesity induced by cafeteria feeding and pregnancy outcome in the rat. Br J Nutr 102, 16011610.
32 King, MV, Sleight, AJ, Woolley, ML, et al. (2004) 5-HT6 receptor antagonists reverse delay-dependent deficits in novel object discrimination by enhancing consolidation – an effect sensitive to NMDA receptor antagonism. Neuropharmacology 47, 195204.
33 Warneke, W, Klaus, S, Fink, H, et al. (2014) The impact of cafeteria diet feeding on physiology and anxiety-related behaviour in male and female Sprague–Dawley rats of different ages. Pharmacol Biochem Behav 116, 4554.
34 Esteve, M, Rafecas, I, Fernandezlopez, JA, et al. (1994) Effect of a cafeteria diet on energy-intake and balance in Wistar rats. Physiol Behav 56, 6571.
35 Llado, I, Pico, C, Palou, A, et al. (1995) Protein and amino-acid intake in cafeteria fed obese rats. Physiol Behav 58, 513519.
36 Daniel, ZC, Akyol, A, McMullen, S, et al. (2014) Exposure of neonatal rats to maternal cafeteria feeding during suckling alters hepatic gene expression and DNA methylation in the insulin signalling pathway. Genes Nutr 9, 365.
37 Sutcliffe, JS, Marshall, KM & Neill, JC (2007) Influence of gender on working and spatial memory in the novel object recognition task in the rat. Behav Brain Res 177, 117125.
38 Ghi, P, Orsetti, M, Gamalero, SR, et al. (1999) Sex differences in memory performance in the object recognition test. Possible role of histamine receptors. Pharmacol Biochem Behav 64, 761766.
39 Walf, AA, Rhodes, ME & Frye, CA (2006) Ovarian steroids enhance object recognition in naturally cycling and ovariectomized, hormone-primed rats. Neurobiol Learn Mem 86, 3546.
40 McEwen, BS, Akama, KT, Spencer-Segal, JL, et al. (2012) Estrogen effects on the brain: actions beyond the hypothalamus via novel mechanisms. Behav Neurosci 126, 416.
41 Gold, PE (1995) Role of glucose in regulating the brain and cognition. Am J Clin Nutr 61, 987S995S.
42 McNay, EC & Gold, PE (2002) Food for thought: fluctuations in brain extracellular glucose provide insight into the mechanisms of memory modulation. Behav Cogn Neurosci Rev 1, 264280.
43 Van Lieshout, RJ (2013) Role of maternal adiposity prior to and during pregnancy in cognitive and psychiatric problems in offspring. Nutr Rev 71, Suppl. 1, S95S101.
44 Sullivan, EL, Nousen, EK & Chamlou, KA (2014) Maternal high fat diet consumption during the perinatal period programs offspring behavior. Physiol Behav 123, 236242.

Keywords

Impact of cafeteria feeding during lactation in the rat on novel object discrimination in the offspring

  • Thomas M. Wright (a1), Madeleine V. King (a2), William G. Davey (a1), Simon C. Langley-Evans (a3) and Jörg-Peter W. Voigt (a1)...

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