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Published in: European Journal of Nutrition 5/2017

01-08-2017 | Original Contribution

Free-choice high-fat diet alters circadian oscillation of energy intake in adolescent mice: role of prefrontal cortex

Authors: Danila Del Rio, Paula Stucchi, Francisco Hernández-Nuño, Victoria Cano, Lidia Morales, Julie A. Chowen, Nuria Del Olmo, Mariano Ruiz-Gayo

Published in: European Journal of Nutrition | Issue 5/2017

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Abstract

Purpose

Our aim was to characterize the effect of an unfamiliar high-fat diet (HFD) on circadian feeding behaviour, plasma parameters, body weight (BW), and gene expression in the prefrontal cortex (PFC) of adolescent male mice. To this end, mice were allowed to consume a HFD during 48 h, but one group was allowed a free choice of HFD or normal chow (FC-HFD), while the other was restricted to a non-optional unfamiliar HFD feeding (NOP-HFD).

Methods

Energy intake was monitored at 6-h intervals during 48 h. Mice cohorts were killed at 6-h intervals after 48-h dietary treatment, and PFC samples dissected for RT-PCR analysis.

Results

Mice on the FC-HFD protocol avoided eating the standard chow, showed lower energy intake and lower BW increase than NOP-HFD mice. All animals with access to HFD exhibited nocturnal overeating, but diurnal hyperphagia was more prominent in the FC-HFD cohort. A robust increase in tyrosine hydroxylase (Th) gene expression was detected specifically during the light period of the circadian cycle in FC-HFD mice. In contrast, both protocols similarly up-regulated the expression of cytosolic malic enzyme (Me1), which is very sensitive to HFD.

Conclusion

Our data show that the PFC participates in driving motivational feeding during HFD-evoked hyperphagia and also suggest that sensory neural pathways might be relevant for the onset of eating disorders and overweight. Moreover, we have observed that animals that had the possibility of choosing between standard chow and HFD were more hyperphagic and specifically displayed an overexpression of the tyrosine hydroxylase gene.
Literature
2.
go back to reference La Fleur SE, Luijendijk MC, Van der Zwaal EM, Brans MA, Adan RA (2014) The snacking rat as model of human obesity: effects of a free-choice high-fat high-sugar diet on meal patterns. Int J Obes 38(5):643–649CrossRef La Fleur SE, Luijendijk MC, Van der Zwaal EM, Brans MA, Adan RA (2014) The snacking rat as model of human obesity: effects of a free-choice high-fat high-sugar diet on meal patterns. Int J Obes 38(5):643–649CrossRef
3.
go back to reference Salamone JD, Correa M (2013) Dopamine and food addiction: lexicon badly needed. Biol Psychiatry 73(9):e15–e24CrossRef Salamone JD, Correa M (2013) Dopamine and food addiction: lexicon badly needed. Biol Psychiatry 73(9):e15–e24CrossRef
4.
go back to reference Bo S, Fadda M, Castiglione A, Ciccone G, De Francesco A, Fedele D et al (2015) Is the timing of caloric intake associated with variation in diet-induced thermogenesis and in the metabolic pattern? A randomized cross-over study. Int J Obes. doi:10.1038/ijo.2015.138 Bo S, Fadda M, Castiglione A, Ciccone G, De Francesco A, Fedele D et al (2015) Is the timing of caloric intake associated with variation in diet-induced thermogenesis and in the metabolic pattern? A randomized cross-over study. Int J Obes. doi:10.​1038/​ijo.​2015.​138
5.
go back to reference Kohsaka A, Laposky AD, Ramsey KM, Estrada C, Joshu C, Kobayashi Y et al (2007) High-fat diet disrupts behavioral and molecular circadian rhythms in mice. Cell Metab 6(5):414–421CrossRef Kohsaka A, Laposky AD, Ramsey KM, Estrada C, Joshu C, Kobayashi Y et al (2007) High-fat diet disrupts behavioral and molecular circadian rhythms in mice. Cell Metab 6(5):414–421CrossRef
6.
go back to reference Stucchi P, Gil-Ortega M, Merino B, Guzmán-Ruiz R, Cano V, Valladolid-Acebes I et al (2012) Circadian feeding drive of metabolic activity in adipose tissue and not hyperphagia triggers overweight in mice: is there a role of the pentose–phosphate pathway? Endocrinology 153:690–699CrossRef Stucchi P, Gil-Ortega M, Merino B, Guzmán-Ruiz R, Cano V, Valladolid-Acebes I et al (2012) Circadian feeding drive of metabolic activity in adipose tissue and not hyperphagia triggers overweight in mice: is there a role of the pentose–phosphate pathway? Endocrinology 153:690–699CrossRef
7.
go back to reference Hatori M, Vollmers C, Zarrinpar A, Di Tacchio L, Bushong EA, Gill S et al (2012) Time-restricted feeding without reducing caloric intake prevents metabolic diseases in mice fed a high-fat diet. Cell Metab 15(6):848–860CrossRef Hatori M, Vollmers C, Zarrinpar A, Di Tacchio L, Bushong EA, Gill S et al (2012) Time-restricted feeding without reducing caloric intake prevents metabolic diseases in mice fed a high-fat diet. Cell Metab 15(6):848–860CrossRef
8.
go back to reference Murray S, Tulloch A, Gold MS, Avena NM (2014) Hormonal and neural mechanisms of food reward, eating behaviour and obesity. Nat Rev Endocrinol 10(9):540–552CrossRef Murray S, Tulloch A, Gold MS, Avena NM (2014) Hormonal and neural mechanisms of food reward, eating behaviour and obesity. Nat Rev Endocrinol 10(9):540–552CrossRef
9.
go back to reference Morales L, Del Olmo N, Valladolid-Acebes I, Fole A, Cano V, Merino B et al (2012) Shift of circadian feeding pattern by high-fat diets is coincident with reward deficits in obese mice. PLoS ONE 7:e36139CrossRef Morales L, Del Olmo N, Valladolid-Acebes I, Fole A, Cano V, Merino B et al (2012) Shift of circadian feeding pattern by high-fat diets is coincident with reward deficits in obese mice. PLoS ONE 7:e36139CrossRef
10.
go back to reference Privitera GJ, Zavala AR, Sanabria F, Sotak KL (2011) High fat diet intake during pre and periadolescence impairs learning of a conditioned place preference in adulthood. Behav Brain Funct 7:21CrossRef Privitera GJ, Zavala AR, Sanabria F, Sotak KL (2011) High fat diet intake during pre and periadolescence impairs learning of a conditioned place preference in adulthood. Behav Brain Funct 7:21CrossRef
11.
go back to reference Valladolid-Acebes I, Fole A, Martín M, Morales L, Cano MV, Ruiz-Gayo M et al (2013) 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 106:18–25CrossRef Valladolid-Acebes I, Fole A, Martín M, Morales L, Cano MV, Ruiz-Gayo M et al (2013) 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 106:18–25CrossRef
12.
go back to reference Del Rio D, Cano V, Martín-Ramos M, Gómez M, Morales L, Del Olmo N et al (2015) Involvement of the dorsomedial prefrontal cortex in high-fat food conditioning in adolescent mice. Behav Brain Res 283C:227–232 Del Rio D, Cano V, Martín-Ramos M, Gómez M, Morales L, Del Olmo N et al (2015) Involvement of the dorsomedial prefrontal cortex in high-fat food conditioning in adolescent mice. Behav Brain Res 283C:227–232
13.
go back to reference Del Parigi A, Chen K, Salbe AD, Hill JO, Wing RR, Reiman EM et al (2007) Successful dieters have increased neural activity in cortical areas involved in the control of behavior. Int J Obes 31(3):440–448CrossRef Del Parigi A, Chen K, Salbe AD, Hill JO, Wing RR, Reiman EM et al (2007) Successful dieters have increased neural activity in cortical areas involved in the control of behavior. Int J Obes 31(3):440–448CrossRef
14.
go back to reference Kishiyama MM, Yonelinas AP, Knight RT (2009) Novelty enhancements in memory are dependent on lateral prefrontal cortex. J Neurosci 29(25):8114–8118CrossRef Kishiyama MM, Yonelinas AP, Knight RT (2009) Novelty enhancements in memory are dependent on lateral prefrontal cortex. J Neurosci 29(25):8114–8118CrossRef
15.
go back to reference Huo Y, Fang Q, Shi Y-L, Zhang Y-H, Zhang J-X (2014) Chronic exposure to a predator or its scent does not inhibit male–male competition in male mice lacking brain serotonin. Front Behav Neurosci. doi:10.3389/fnbeh.2014.00116 Huo Y, Fang Q, Shi Y-L, Zhang Y-H, Zhang J-X (2014) Chronic exposure to a predator or its scent does not inhibit male–male competition in male mice lacking brain serotonin. Front Behav Neurosci. doi:10.​3389/​fnbeh.​2014.​00116
16.
go back to reference Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCΤ method. Methods 25:402–408CrossRef Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCΤ method. Methods 25:402–408CrossRef
17.
go back to reference Somoza B, Guzmán R, Cano V, Merino B, Ramos MP, Díez-Fernández C et al (2007) Induction of cardiac uncoupling protein-2 expression and adenosine 5′-monophosphate-activated protein kinase phosphorylation during early states of diet-induced obesity in mice. Endocrinology 148(3):924–931CrossRef Somoza B, Guzmán R, Cano V, Merino B, Ramos MP, Díez-Fernández C et al (2007) Induction of cardiac uncoupling protein-2 expression and adenosine 5′-monophosphate-activated protein kinase phosphorylation during early states of diet-induced obesity in mice. Endocrinology 148(3):924–931CrossRef
18.
go back to reference Bake T, Murphy M, Morgan DG, Mercer JG (2014) Large, binge-type meals of high fat diet change feeding behaviour and entrain food anticipatory activity in mice. Appetite 77:60–71CrossRef Bake T, Murphy M, Morgan DG, Mercer JG (2014) Large, binge-type meals of high fat diet change feeding behaviour and entrain food anticipatory activity in mice. Appetite 77:60–71CrossRef
19.
go back to reference la Fleur SE, Houshyar H, Roy M, Dallman MF (2005) Choice of lard, but not total lard calories, damps adrenocorticotropin responses to restraint. Endocrinology 146:2193–2199CrossRef la Fleur SE, Houshyar H, Roy M, Dallman MF (2005) Choice of lard, but not total lard calories, damps adrenocorticotropin responses to restraint. Endocrinology 146:2193–2199CrossRef
20.
go back to reference Lincoln G, Messager S, Andersson H, Hazlerigg D (2002) Temporal expression of seven clock genes in the suprachiasmatic nucleus and the pars tuberalis of the sheep: evidence for an internal coincidence timer. Proc Natl Acad Sci USA 99(21):13890–13895CrossRef Lincoln G, Messager S, Andersson H, Hazlerigg D (2002) Temporal expression of seven clock genes in the suprachiasmatic nucleus and the pars tuberalis of the sheep: evidence for an internal coincidence timer. Proc Natl Acad Sci USA 99(21):13890–13895CrossRef
21.
22.
go back to reference Sun X, Kroemer NB, Veldhuizen MG, Babbs AE, De Araujo IE, Gitelman DR et al (2015) Basolateral amygdala response to food cues in the absence of hunger is associated with weight gain susceptibility. J Neurosci 35(20):7964–7976CrossRef Sun X, Kroemer NB, Veldhuizen MG, Babbs AE, De Araujo IE, Gitelman DR et al (2015) Basolateral amygdala response to food cues in the absence of hunger is associated with weight gain susceptibility. J Neurosci 35(20):7964–7976CrossRef
23.
go back to reference Maliphol AB, Garth DJ, Medler KF (2013) Diet-induced obesity reduces the responsiveness of the peripheral taste receptor cells. PLoS ONE 8(11):e79403CrossRef Maliphol AB, Garth DJ, Medler KF (2013) Diet-induced obesity reduces the responsiveness of the peripheral taste receptor cells. PLoS ONE 8(11):e79403CrossRef
24.
go back to reference Ishikawa A, Ambroggi F, Nicola SM, Fields HL (2008) Dorsomedial prefrontal cortex contribution to behavioral and nucleus accumbens neuronal responses to incentive cues. J Neurosci 28(19):5088–5098CrossRef Ishikawa A, Ambroggi F, Nicola SM, Fields HL (2008) Dorsomedial prefrontal cortex contribution to behavioral and nucleus accumbens neuronal responses to incentive cues. J Neurosci 28(19):5088–5098CrossRef
25.
go back to reference El-Haschimi K, Pierroz DD, Hileman SM, Bjørbaek C, Flier JS (2000) Two defects contribute to hypothalamic leptin resistance in mice with diet-induced obesity. J Clin Invest 105(12):1827–1832CrossRef El-Haschimi K, Pierroz DD, Hileman SM, Bjørbaek C, Flier JS (2000) Two defects contribute to hypothalamic leptin resistance in mice with diet-induced obesity. J Clin Invest 105(12):1827–1832CrossRef
26.
go back to reference Simon NW, Beas BS, Montgomery KS, Haberman RP, Bizon JL, Setlow B (2013) Prefrontal cortical–striatal dopamine receptor mRNA expression predicts distinct forms of impulsivity. Eur J Neurosci 37:1779–1788CrossRef Simon NW, Beas BS, Montgomery KS, Haberman RP, Bizon JL, Setlow B (2013) Prefrontal cortical–striatal dopamine receptor mRNA expression predicts distinct forms of impulsivity. Eur J Neurosci 37:1779–1788CrossRef
27.
go back to reference Ballard IC, Murty VP, McKell-Carter R, MacInnes JJ, Huettel SA, Adcock RA (2011) Dorsolateral prefrontal cortex drives mesolimbic dopaminergic regions to initiate motivated behavior. J Neurosci 31(28):10340–10346CrossRef Ballard IC, Murty VP, McKell-Carter R, MacInnes JJ, Huettel SA, Adcock RA (2011) Dorsolateral prefrontal cortex drives mesolimbic dopaminergic regions to initiate motivated behavior. J Neurosci 31(28):10340–10346CrossRef
28.
go back to reference Cho S, Neff NH, Hadjiconstantinou M (1997) Regulation of tyrosine hydroxylase and aromatic l-amino acid decarboxylase by dopaminergic drugs. Eur J Pharmacol 323(2–3):149–157CrossRef Cho S, Neff NH, Hadjiconstantinou M (1997) Regulation of tyrosine hydroxylase and aromatic l-amino acid decarboxylase by dopaminergic drugs. Eur J Pharmacol 323(2–3):149–157CrossRef
29.
go back to reference Van de Giessen E, La Fleur SE, De Bruin K, Van den Brink W, Booij J (2012) Free-choice and no-choice high-fat diets affect striatal dopamine D2/3 receptor availability, caloric intake, and adiposity. Obesity 20(8):1738–1740CrossRef Van de Giessen E, La Fleur SE, De Bruin K, Van den Brink W, Booij J (2012) Free-choice and no-choice high-fat diets affect striatal dopamine D2/3 receptor availability, caloric intake, and adiposity. Obesity 20(8):1738–1740CrossRef
30.
go back to reference Dazzi L, Talani G, Biggio F, Utzeri C, Lallai V, Licheri V et al (2014) Involvement of the cannabinoid CB1 receptor in modulation of dopamine output in the prefrontal cortex associated with food restriction in rats. PLoS ONE 9(3):e92224CrossRef Dazzi L, Talani G, Biggio F, Utzeri C, Lallai V, Licheri V et al (2014) Involvement of the cannabinoid CB1 receptor in modulation of dopamine output in the prefrontal cortex associated with food restriction in rats. PLoS ONE 9(3):e92224CrossRef
31.
go back to reference Di Marzo V, Ligresti A, Cristino L (2009) The endocannabinoid system as a link between homoeostatic and hedonic pathways involved in energy balance regulation. Int J Obes 33:S18–S24CrossRef Di Marzo V, Ligresti A, Cristino L (2009) The endocannabinoid system as a link between homoeostatic and hedonic pathways involved in energy balance regulation. Int J Obes 33:S18–S24CrossRef
32.
go back to reference Das Neves Duarte JM, Kulak A, Gholam-Razaee MM, Cuenod M, Gruetter R, Do KQ (2012) N-acetylcysteine normalizes neurochemical changes in the glutathione-deficient schizophrenia mouse model during development. Biol Psychiatry 71(11):1006–1014CrossRef Das Neves Duarte JM, Kulak A, Gholam-Razaee MM, Cuenod M, Gruetter R, Do KQ (2012) N-acetylcysteine normalizes neurochemical changes in the glutathione-deficient schizophrenia mouse model during development. Biol Psychiatry 71(11):1006–1014CrossRef
33.
go back to reference Guix FX, Uribesalgo I, Coma M, Muñoz FJ (2005) The physiology and pathophysiology of nitric oxide in the brain. Prog Neurobiol 76(2):126–152CrossRef Guix FX, Uribesalgo I, Coma M, Muñoz FJ (2005) The physiology and pathophysiology of nitric oxide in the brain. Prog Neurobiol 76(2):126–152CrossRef
34.
go back to reference Tao H, Szeszel-Fedorowicz W, Amir-Ahmady B, Gibson MA, Stabile LP, Salati LM (2002) Inhibition of the splicing of glucose-6-phosphate dehydrogenase precursor mRNA by polyunsaturated fatty acids. J Biol Chem 277:31270–31278CrossRef Tao H, Szeszel-Fedorowicz W, Amir-Ahmady B, Gibson MA, Stabile LP, Salati LM (2002) Inhibition of the splicing of glucose-6-phosphate dehydrogenase precursor mRNA by polyunsaturated fatty acids. J Biol Chem 277:31270–31278CrossRef
35.
go back to reference Hassel B, Bråthe A (2000) Neuronal pyruvate carboxylation supports formation of transmitter glutamate. J Neurosci 20(4):1342–1347 Hassel B, Bråthe A (2000) Neuronal pyruvate carboxylation supports formation of transmitter glutamate. J Neurosci 20(4):1342–1347
36.
go back to reference McKenna MC, Tildon JT, Stevenson JH, Huang X, Kingwell KG (1995) Regulation of mitochondrial and cytosolic malic enzymes from cultured rat brain astrocytes. Neurochem Res 20(12):1491–1501CrossRef McKenna MC, Tildon JT, Stevenson JH, Huang X, Kingwell KG (1995) Regulation of mitochondrial and cytosolic malic enzymes from cultured rat brain astrocytes. Neurochem Res 20(12):1491–1501CrossRef
37.
go back to reference Valladolid-Acebes I, Merino B, Principato A, Fole A, Barbas C, Lorenzo MP et al (2012) High-fat diets induce changes in hippocampal glutamate metabolism and neurotransmission. Am J Physiol Endocrinol Metab 302:E396–E402CrossRef Valladolid-Acebes I, Merino B, Principato A, Fole A, Barbas C, Lorenzo MP et al (2012) High-fat diets induce changes in hippocampal glutamate metabolism and neurotransmission. Am J Physiol Endocrinol Metab 302:E396–E402CrossRef
38.
go back to reference Bruce-Keller AJ, White CL, Gupta S, Knight AG, Pistell PJ, Ingram DK et al (2010) NOX activity in brain aging: exacerbation by high fat diet. Free Radic Biol Med 49(1):22–30CrossRef Bruce-Keller AJ, White CL, Gupta S, Knight AG, Pistell PJ, Ingram DK et al (2010) NOX activity in brain aging: exacerbation by high fat diet. Free Radic Biol Med 49(1):22–30CrossRef
Metadata
Title
Free-choice high-fat diet alters circadian oscillation of energy intake in adolescent mice: role of prefrontal cortex
Authors
Danila Del Rio
Paula Stucchi
Francisco Hernández-Nuño
Victoria Cano
Lidia Morales
Julie A. Chowen
Nuria Del Olmo
Mariano Ruiz-Gayo
Publication date
01-08-2017
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nutrition / Issue 5/2017
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-016-1225-x

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