Adaptations in brain reward circuitry underlie palatable food cravings and anxiety induced by high-fat diet withdrawal
Abstract
Objective To identify the emotional and motivational processes that reinstate palatable food intake following removal of high-fat diet (HFD) and associated neuroadaptations tied to neurochemical and behavioural changes underlying dopaminergic function.Methods Adult male C57Bl6 mice were placed on a HFD (58% kcal fat) or ingredient-matched, low-fat diet (LFD; 11% kcal fat) for 6 weeks. At the end of diet-regimen mice were either maintained on their respective diets, or HFD and LFD were replaced with normal chow (withdrawal). Effort-based operant responding for sucrose and high-fat food rewards was measured along with basal and stress-induced corticosterone levels and anxiety (elevated-plus maze). Protein levels for tyrosine hydroxylase (TH), corticosterone releasing factor type 1 receptor (CRF-R1), brain-derived neurotrophic factor (BDNF), phospho-CREB (pCREB) and ΔFosB (truncated splice variant of FosB) were assessed in the amygdala, nucleus accumbens (NAc) and ventral tegmental area (VTA) via western immunoblotting.Results Six weeks of HFD resulting in significant weight gain elicited sucrose anhedonia, anxiety-like behaviour and hypothalamic-pituitary-adrenocortical axis (HPA) hypersensitivity to stress. Withdrawal from HFD but not LFD-potentiated anxiety and basal corticosterone levels and enhanced motivation for sucrose and high-fat food rewards. Chronic high-fat feeding reduced CRF-R1 and increased BDNF and pCREB protein levels in the amygdala and reduced TH and increased ΔFosB protein in NAc and VTA. Heightened palatable food reward in mice withdrawn from HFD coincided with increased BDNF protein levels in NAc and decreased TH and pCREB expression in the amygdala.Conclusion Anhedonia, anxiety and sensitivity to stressors develops during the course of HFD and may have a key role in a vicious cycle that perpetuates high-fat feeding and the development of obesity. Removal of HFD enhances stress responses and heightens vulnerability for palatable foods by increasing food-motivated behaviour. Lasting changes in dopamine and plasticity-related signals in reward circuitry may promote negative emotional states, overeating and palatable food relapse.
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Prolonged high-fat diet heightens stress and hypothalamic-pituitary-adrenal responses in rodents.
“To this end, rodent research has revealed that prolonged high-fat diet (HFD) elicits metabolic dysfunction and increases anxiety-and depressive-like behaviors [28][29][30][31][32][33][34][35][36], heightens stress and hypothalamic-pituitary-adrenal (HPA) responses [37,38], and triggers neurobehavioral deficits associated with blunted mesolimbic dopamine function [39][40][41].”
From The menace of obesity to depression and anxiety prevalence (2022) · cites this paper as [37]
In the absence of obesity development, saturated high-fat diets can still potentiate HPA reactivity and feedback and suppress behavioral responses to rewards in rodents.
“However, in the absence of obesity development, these diets can still potentiate HPA reactivity [37] and feedback [38] and suppress behavioral responses to rewards [41].”
From The menace of obesity to depression and anxiety prevalence (2022) · cites this paper as [37]
Prolonged saturated high-fat feeding that does not lead to significant adipose deposition fails to stimulate anxiety-like behaviors in rodents.
“The importance of excessive adipose mass to emotional deficits in obesity is highlighted by rodent studies showing that prolonged saturated high-fat feeding that does not lead to significant adipose deposition fails to stimulate anxiety-like behaviors [37,38].”
From The menace of obesity to depression and anxiety prevalence (2022) · cites this paper as [37]
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The Role of Microbiome, Dietary Supplements, and Probiotics in Autism Spectrum Disorder
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Hryhorczuk, C., Florea, M., Rodaros, D., Poirier, I., Daneault, C., Des Rosiers, C., Arvanitogiannis, A., Alquier, T., & Fulton, S. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.207 · Cited by 119 · see citing works
“…(Davis et al, 2008), decrease nucleus accumbens (NAc) DA overflow (Geiger et al, 2009), modulate DA-related behaviors and striatal neuroadaptive responses (Sharma et al, 2013; Sharma and Fulton, 2013; Teegarden et al, 2009; Vucetic et al, 2012), and blunt DA reuptake in the NAc (Cone et al, 2013).”
BackgroundCurrent nutritional approaches in managing autism spectrum disorder: A review
Çekici, H., & Şanlıer, N. (2017) · Nutritional Neuroscience · doi:10.1080/1028415x.2017.1358481 · Cited by 119 · see citing works
Habitual daily intake of a sweet and fatty snack modulates reward processing in humans
Thanarajah, S. E., DiFeliceantonio, A. G., Albus, K., Kuzmanovic, B., Rigoux, L., Iglesias, S., Hanßen, R., Schlamann, M., Cornely, O. A., Brüning, J. C., et al. (2023) · Cell Metabolism · doi:10.1016/j.cmet.2023.02.015 · Cited by 118 · see citing works
Beilharz, J. E., Kaakoush, N. O., Maniam, J., & Morris, M. J. (2018) · Molecular Psychiatry · doi:10.1038/mp.2017.38 · Cited by 116 · see citing works
Ly, V., Bottelier, M. A., Hoekstra, P. J., Vásquez, A. A., Buitelaar, J. K., & Rommelse, N. N. J. (2017) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-017-0959-1 · Cited by 114 · see citing works
Micanti, F., Iasevoli, F., Cucciniello, C., Costabile, R., Loiarro, G., Pecoraro, G., Pasanisi, F., Rossetti, G., & Galletta, D. (2017) · Eating and Weight Disorders - Studies on Anorexia, Bulimia and Obesity · doi:10.1007/s40519-016-0275-7 · Cited by 107 · see citing works
Décarie-Spain, L., Sharma, S., Hryhorczuk, C., Issa-Garcia, V., Barker, P. A., Arbour, N., Alquier, T., & Fulton, S. (2018) · Molecular Metabolism · doi:10.1016/j.molmet.2018.01.018 · Cited by 107 · see citing works
“At the end of the operant protocol above, Palm and Palm mice were transitioned from the palm HFD to standard chow, a manipulation which stimulates craving and food-seeking [22].”
BackgroundInfluentialHPA Axis Interactions with Behavioral Systems
Packard, A. E. B., Egan, A. E., & Ulrich‐Lai, Y. M. (2016) · Comprehensive physiology · doi:10.1002/cphy.c150042 · Cited by 130 · see citing works
The impact of junk foods on the adolescent brain
Reichelt, A. C., & Rank, M. M. (2017) · Birth Defects Research · doi:10.1002/bdr2.1173 · Cited by 102 · see citing works
Kim, S., Shou, J., Abera, S., & Ziff, E. B. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.11.041 · Cited by 103 · see citing works
“…several groups have shown that removal of a high-fat/sugar diet following long-term intermittent or regular intake can induce depression and anxiety-associated behavioral and physiological signs (Avena et al., 2008; Cottone et al., 2009a, 2009b; Sharma et al., 2013; Teegarden et al., 2008).”
BackgroundInfluentialAddiction-like Synaptic Impairments in Diet-Induced Obesity
Brown, R. M., Kupchik, Y. M., Spencer, S. M., García‐Keller, C., Spanswick, D. C., Lawrence, A. J., Simonds, S. E., Schwartz, D., Jordan, K. A., Jhou, T. C., et al. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.11.019 · Cited by 96 · see citing works
“Increased responding on a progressive ratio schedule is indicative of heightened motivation, possibly augmented by restricted access to the palatable diet during operant training (50,51).”
BackgroundReichelt, A. C. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00189 · Cited by 93 · see citing works
“…enduring changes in dopamine signaling within regions involved in reward processing, cognitive functions and motivation, including the nucleus accumbens (Rada et al., 2005; Sharma et al., 2013), the hippocampus (Kaczmarczyk et al., 2013; Krishna et al., 2015) and the PFC (Wakabayashi et al., 2015).”
BackgroundWallace, C. W., & Fordahl, S. C. (2021) · Nutrition Research Reviews · doi:10.1017/s0954422421000196 · Cited by 92 · see citing works
“Changes in dopamine tone or phasic dopamine release in the NAc may significantly impact food seeking 8,11 – 13 , reward 8,9,11,12 and satiety 11,13,14 .”
BackgroundMethodInfluentialJuvenile Obesity Enhances Emotional Memory and Amygdala Plasticity through Glucocorticoids
Boitard, C., Maroun, M., Tantot, F., Cavaroc, A., Sauvant, J., Marchand, A. R., Layé, S., Capuron, L., Darnaudéry, M., Castanon, N., et al. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.3122-14.2015 · Cited by 89 · see citing works
“…report indicating that chronic high-fat feeding in mice increases plasticity-related (BDNF and phospho-CREB) protein levels in the amygdala (Sharma et al., 2013) and suggests that juvenile exposure to HFD enhances protein synthesis after BLA stimulation, leading to long-term synaptic and…”
BackgroundKrishna, S., Keralapurath, M. M., Lin, Z., Wagner, J. J., Serre, C. B. D. L., Harn, D. A., & Filipov, N. M. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.03.068 · Cited by 84 · see citing works
Martire, S. I., Maniam, J., South, T., Holmes, N. M., Westbrook, R. F., & Morris, M. J. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.02.027 · Cited by 80 · see citing works
Liu, S., Globa, A. K., Mills, F., Naef, L., Qiao, M., Bamji, S. X., & Borgland, S. L. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1515724113 · Cited by 80 · see citing works
“Elevated anxiety has been associated with withdrawal from palatable foods (21, 23).”
BackgroundHigh-fat diet exacerbates cognitive rigidity and social deficiency in the BTBR mouse model of autism
Zilkha, N., Kuperman, Y., & Kimchi, T. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.01.070 · Cited by 68 · see citing works
“, 2013), anxiety-related behaviors (Sharma et al., 2013) and social interactions (Grissom and Reyes, 2013).”
Hardaway, J. A., Crowley, N. A., Bulik, C. M., & Kash, T. L. (2014) · Genes Brain & Behavior · doi:10.1111/gbb.12185 · Cited by 63 · see citing works
“Sharma et al. (2012) found that exposure to a high-fat diet increased weight and anxiety in male mice, and interestingly, decreased CRF1 receptor expression levels.”
BackgroundIncreased anxiety-like behavior is associated with the metabolic syndrome in non-stressed rats
Rebolledo-Solleiro, D., Roldán-Roldán, G., Díaz, D., Velasco, M., Larqué, C., Rico-Rosillo, G., Vega-Robledo, G. B., Zambrano, E., Hiriart, M., & Pérez de la Mora, M. (2017) · PLoS ONE · doi:10.1371/journal.pone.0176554 · Cited by 64 · see citing works
Auguste, S., Fisette, A., Fernandes, M. F., Hryhorczuk, C., Poitout, V., Alquier, T., & Fulton, S. (2016) · International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyw014 · Cited by 59 · see citing works
Persistent effects of obesity: A neuroplasticity hypothesis
Matikainen‐Ankney, B. A., & Kravitz, A. V. (2018) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.13665 · Cited by 56 · see citing works
“specific binding in obese and normal-weight individuals using PET with (N-[(11)C]methyl)benperidol.”
MethodNeuroscience of Compulsive Eating Behavior
Moore, C. F., Sabino, V., Koob, G. F., & Cottone, P. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00469 · Cited by 56 · see citing works
“…from palatable food, the emergence of a negative emotional state, characterized by anxiety- and depressive-like behavior (Figure 1B; Iemolo et al., 2012) (Cottone et al., 2008; Sharma et al., 2013), and enhanced stress-responsiveness (Avena et al., 2008; Blasio et al., 2014a), is observed.”
BackgroundFood and addiction among the ageing population
Murray, S. M., Kroll, C., & Avena, N. M. (2014) · Ageing Research Reviews · doi:10.1016/j.arr.2014.10.002 · Cited by 55 · see citing works
Spexin-Based Galanin Receptor Type 2 Agonist for Comorbid Mood Disorders and Abnormal Body Weight
Yun, S., Reyes‐Alcaraz, A., Lee, Y.-N., Yong, H. J., Choi, J., Ham, B., Sohn, J., Kim, D. H., Son, G. H., Kim, H., et al. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00391 · Cited by 55 · see citing works
Blanco-Gandía, M. C., Cantacorps, L., Aracil-Fernández, A., Montagud‐Romero, S., Aguilar, M. A., Manzanares, J., Valverde, O., Miñarro, J., & Rodríguez‐Arias, M. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.09.020 · Cited by 54 · see citing works
“After sustained ad libitum exposure to a high-fat diet, blocking access to said diet potentiates anxiety, elevation of the stress state and a reduction in the reward response (Teegarden and Bale, 2007; Sharma et al., 2013).”
BackgroundHryhorczuk, C., Décarie-Spain, L., Sharma, S., Daneault, C., Rosiers, C. D., Alquier, T., & Fulton, S. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.06.002 · Cited by 51 · see citing works
“Collectively, the findings suggest that while HPA tone and central feedback mechanisms are altered by saturated dietary lipids, the anxiogenic effects of high-fat feeding are absent in conditions of high-fat feeding without major metabolic dysfunction (Andre et al., 2014; Dutheil et al., 2015; Sharma et al., 2013; Sha…”
Energetic stress: The reciprocal relationship between energy availability and the stress response
Harrell, C. S., Gillespie, C. F., & Neigh, G. N. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.10.009 · Cited by 50 · see citing works
“Excess fat or sugar consumption elevates the glucocorticoid response to stress (Duong et al., 2012, Michopoulos et al., 2012, Sharma et al., 2013, Balsevich et al., 2014).”
de Lima, R. M. S., Bento, L. V. D. S., Lugon, M. D. M. V., Baraúna, V. G., Bittencourt, A. S., Dalmaz, C., & Bittencourt, A. P. S. D. V. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112399 · Cited by 50 · see citing works
Neurotrophins in the ventral tegmental area: Role in social stress, mood disorders and drug abuse
Nikulina, E. M., Johnston, C. E., Wang, J., & Hammer, R. P. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.05.028 · Cited by 47 · see citing works
“Specifically, mesolimbic BDNF expression was unaffected in mice fed low- or highfat diets, but BDNF increased in the NAc during withdrawal from a high-fat diet when mice exhibited elevated palatable food reward (Sharma et al., 2013).”
Do Dopaminergic Impairments Underlie Physical Inactivity in People with Obesity?
Kravitz, A. V., O’Neal, T. J., & Friend, D. M. (2016) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2016.00514 · Cited by 48 · see citing works
“High-fat diet reduced the levels of several enzymes involved in dopamine production in the VTA and NAc, and switching these obese mice to low-fat chow caused even further decreases in these enzymes (Carlin et al., 2013; Sharma et al., 2013).”
BackgroundWei, N.-L., Quan, Z.-F., Zhao, T., Yu, X.-D., Xie, Q., Zeng, J., Ma, F.-K., Wang, F., Tang, Q.-S., Wu, H., et al. (2019) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s204818 · Cited by 46 · see citing works
“The process underlying the shift from decreased to increased intake depends upon adaptations in the reward circuitry in the brain.(28) When animals are exposed to severe stress, dysregulated DA release and CRF in the reward circuitry drives the switch in the appetitive response to palatable food to an aversive respons…”
BackgroundEffect of high-fat diets on mood and learning performance in adolescent mice
Rio, D. D., Morales, L., Ruiz‐Gayo, M., & Olmo, N. D. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.04.052 · Cited by 46 · see citing works
Leffa, D. D., Valvassori, S. S., Varela, R. B., Lopes-Borges, J., Daumann, F., Longaretti, L. M., Dajori, A. L. F., Quevedo, J., & de Andrade, V. M. (2015) · Metabolic Brain Disease · doi:10.1007/s11011-015-9682-0 · Cited by 45 · see citing works
“It is also described in the literature that the high energydense foods are rewarding and their intake can recruit neural pathways and mechanisms linked to addiction (Sharma et al. 2013).”
BackgroundInfluentialDaily Fluctuation of Orexin Neuron Activity and Wiring: The Challenge of “Chronoconnectivity”
Azeez, I. A., Gallo, F. D., Cristino, L., & Bentivoglio, M. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.01061 · Cited by 44 · see citing works
Matikainen‐Ankney, B. A., Legaria, A. A., Pan, Y., Vachez, Y. M., Murphy, C. A., Schaefer, R. F., McGrath, Q., Wang, J. G., Bluitt, M. N., Ankney, K. C., et al. (2022) · Biological Psychiatry · doi:10.1016/j.biopsych.2022.10.003 · Cited by 43 · see citing works
Effects of high fat or high sucrose diet on behavioral-response to social defeat stress in mice
Eudave, D. M., BeLow, M. N., & Flandreau, E. I. (2018) · Neurobiology of Stress · doi:10.1016/j.ynstr.2018.05.005 · Cited by 43 · see citing works
“In mice, six weeks of HFD (58% kcal fat) caused anhedonia in a sucrose-preference test and anxiety-like behavior in the elevated plus maze (EPM) compared to mice fed an ingredientmatched low fat control diet (11% kcal fat) (Sharma et al., 2013).”
MethodGanji, A., Salehi, I., Sarihi, A., Shahidi, ., & Komaki, A. (2016) · Metabolic Brain Disease · doi:10.1007/s11011-016-9940-9 · Cited by 43 · see citing works
“Similarly, glutted high-fat feeding increases anxiety-like behavior and stress sensitivity in mice (Sharma et al. 2013; Sharma and Fulton 2013; Zemdegs et al. 2015; Auguste et al. 2016).”
BackgroundΔFOSB: A Potentially Druggable Master Orchestrator of Activity-Dependent Gene Expression
Robison, A. J., & Nestler, E. J. (2022) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.1c00723 · Cited by 42 · see citing works
Holahan, M. R., Smith, C. A., Luu, B. E., & Storey, K. B. (2018) · Toxicological Sciences · doi:10.1093/toxsci/kfy171 · Cited by 41 · see citing works
Chronic high fat diet consumption impairs sensorimotor gating in mice
Labouesse, M. A., Weber‐Stadlbauer, U., Langhans, W., & Meyer, U. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.06.003 · Cited by 40 · see citing works
“…effects contrast several reports of blunted dopaminergic activity following chronic HFD exposure in rats or mice when the dietary manipulations were initiated once the animals had reached adulthood (e.g., Davis et al., 2008; Li et al., 2009; Vucetic et al., 2012; Sharma et al., 2011).”
BackgroundThe rewarding effects of ethanol are modulated by binge eating of a high-fat diet during adolescence
Blanco-Gandía, M. C., Ledesma, J. C., Aracil-Fernández, A., Navarrete, F., Montagud‐Romero, S., Aguilar, M. A., Manzanares, J., Miñarro, J., & Rodríguez‐Arias, M. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.04.040 · Cited by 40 · see citing works
“On the other hand, most studies report decreased TH expression upon exposure to a high-fat diet (Sharma et al., 2012: Li et al., 2005).”
Dopamine signalling adaptations by prolonged high-fat feeding
Décarie-Spain, L., Hryhorczuk, C., & Fulton, S. (2016) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2016.03.010 · Cited by 39 · see citing works
Ji, S., Wang, L., & Li, L. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00704 · Cited by 37 · see citing works
The influence of COVID-19-related stress on food motivation
Smith, K., Jansen, E., Thapaliya, G., Aghababian, A. H., Chen, L., Sadler, J. R., & Carnell, S. (2021) · Appetite · doi:10.1016/j.appet.2021.105233 · Cited by 37 · see citing works
HPA Axis Interactions with Behavioral Systems
Packard, A. E. B., Egan, A. E., & Ulrich‐Lai, Y. M. (2016) · Comprehensive physiology · doi:10.1002/j.2040-4603.2016.tb00722.x · Cited by 35 · see citing works
“For example, mice that have become obese following prolonged (6-12 weeks) ad libitum access to a high fat diet have increased plasma corticosterone following restraint stress (490, 491).”
Analyses of meal patterns across dietary shifts
Treesukosol, Y., & Moran, T. H. (2013) · Appetite · doi:10.1016/j.appet.2013.12.004 · Cited by 35 · see citing works
Grayson, B. E., Hakala-Finch, A. P., Kekulawala, M., Laub, H. N., Egan, A. E., Ressler, I. B., Woods, S. C., Herman, J. P., Seeley, R. J., Benoit, S. C., et al. (2014) · Stress · doi:10.3109/10253890.2014.967677 · Cited by 35 · see citing works
“Collectively, these results are similar to other reports in which rodents consuming HFD (without other food options) for varying amounts of time have increased HPA activity (Kamara et al., 1998; Sharma et al., 2013; Tannenbaum et al., 1997), and are consistent with some clinical evidence suggesting that increased adip…”
BackgroundResultMartín-Pérez, C., Contreras‐Rodríguez, O., Vilar‐López, R., & Verdejo‐García, A. (2018) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2018.06.039 · Cited by 35 · see citing works
Méquinion, M., Foldi, C. J., & Andrews, Z. B. (2020) · Frontiers in Nutrition · doi:10.3389/fnut.2019.00190 · Cited by 34 · see citing works
“However, dysregulation of the HPA axis can prove maladaptive by promoting mood disorders, such as anxiety, depression, and compulsion (130), or metabolic disorders such as overeating and excessive weight gain (131, 132).”
BackgroundAnhedonia induced by high-fat diet in mice depends on gut microbiota and leptin
Hassan, A. M., Mancano, G., Kashofer, K., Liebisch, G., Farzi, A., Zenz, G., Claus, S. P., & Holzer, P. D. (2020) · Nutritional Neuroscience · doi:10.1080/1028415x.2020.1751508 · Cited by 34 · see citing works
Changes in gene expression and sensitivity of cocaine reward produced by a continuous fat diet
Blanco-Gandía, M. C., Aracil-Fernández, A., Montagud‐Romero, S., Aguilar, M. A., Manzanares, J., Miñarro, J., & Rodríguez‐Arias, M. (2017) · Psychopharmacology · doi:10.1007/s00213-017-4630-9 · Cited by 33 · see citing works
“In line with our results, several studies have reported an increase in anxiety levels up to 24 h after cessation of continuous access to a HFD (Teegarden and Bale 2007; Cottone et al. 2009; Sharma et al. 2013).”
ResultCamacho‐Morales, A., Montalvo-Martínez, L., Cárdenas-Pérez, R. E., Fuentes‐Mera, L., & Garza‐Ocañas, L. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.05.014 · Cited by 32 · see citing works
Slomp, M., Belegri, E., Blancas‐Velazquez, A. S., Diepenbroek, C., Eggels, L., Gumbs, M. C. R., Joshi, A., Koekkoek, L. L., Lamuadni, K., Ugur, M., et al. (2019) · Journal of Neuroendocrinology · doi:10.1111/jne.12718 · Cited by 31 · see citing works
Short‐term high‐fat diet primes excitatory synapses for long‐term depression in orexin neurons
Linehan, V., Fang, L. Z., & Hirasawa, M. (2017) · The Journal of Physiology · doi:10.1113/jp275177 · Cited by 29 · see citing works
“While a high-fat diet is known to induce various types of functional and structural plasticity within the reward circuitry (Johnson & Kenny, 2010; Vucetic et al. 2012; Labouèbe et al. 2013; Sharma et al. 2013), plastic changes in orexin neurons during a high-fat diet are poorly understood.”
Intermittent access to a nutritionally complete high-fat diet attenuates alcohol drinking in rats
Sirohi, S., Cleef, A. V., & Davis, J. F. (2016) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2016.12.009 · Cited by 28 · see citing works
“been shown to induce anxiolytic behavior and increase in food motivation, whereas increase in anxiety-like behavior and decrease in food motivation has been reported following chronic HFD exposure in rodents (Davis et al., 2008; la Fleur et al., 2007; Sharma et al., 2012; Ulrich-Lai et al., 2010).”
Sanderlin, A. H., Todem, D., & Bozoki, A. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00164 · Cited by 28 · see citing works
Converging vulnerability factors for compulsive food and drug use
Serafine, K. M., O’Dell, L. E., & Zorrilla, E. P. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108556 · Cited by 28 · see citing works
“Behavioral signs of a negative emotional state also are documented in animals following palatable food access (Sharma et al., 2013).”
BackgroundGLP-1/dexamethasone inhibits food reward without inducing mood and memory deficits in mice
Décarie-Spain, L., Fisette, A., Zhu, Z., Yang, B., DiMarchi, R. D., Tschöp, M. H., Finan, B., Fulton, S., & Clemmensen, C. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.03.035 · Cited by 27 · see citing works
“Forced swim test (FST) Animals were placed in a water-filled recipient (1600mL of water at 23 ± 2 °C) for 6min, as described previously (Sharma et al., 2013).”
Nutritional Controls of Food Reward
Fernandes, M. F., Sharma, S., Hryhorczuk, C., Auguste, S., & Fulton, S. E. (2013) · Canadian Journal of Diabetes · doi:10.1016/j.jcjd.2013.04.004 · Cited by 27 · see citing works
Modulation of high fat diet-induced microbiome changes, but not behaviour, by minocycline
Hasebe, K., Rivera, L. R., Smith, C. M., Allnutt, T. R., Crowley, T. M., Nelson, T. M., Dean, O. M., McGee, S. L., Walder, K. R., & Gray, L. J. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.09.001 · Cited by 26 · see citing works
Development of the Highly Processed Food Withdrawal Scale for Children
Parnarouskis, L., LaFata, E. M., Lumeng, J. C., & Gearhardt, A. N. (2019) · Appetite · doi:10.1016/j.appet.2019.104553 · Cited by 26 · see citing works
Dopamine pathway imbalance in mice lacking Magel2, a Prader-Willi syndrome candidate gene.
Gibson, C. L., Vitaterna, M. H., & Wevrick, R. (2016) · Behavioral Neuroscience · doi:10.1037/bne0000150 · Cited by 26 · see citing works
A novel designer drug, 25N-NBOMe, exhibits abuse potential via the dopaminergic system in rodents
Seo, J., Hur, K., Ko, Y., Kim, K., Lee, B., Kim, Y., Kim, S., Kim, S., Lee, Y. S., Kim, H., et al. (2019) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2019.07.002 · Cited by 25 · see citing works
Moazzam, S., Jarmasz, J. S., Jin, Y., Siddiqui, T. J., & Cattini, P. A. (2021) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2021.105147 · Cited by 25 · see citing works
(-)-Epicatechin mitigates anxiety-related behavior in a mouse model of high fat diet-induced obesity
Kang, J., Wang, Z., Cremonini, E., Gall, G. L., Pontifex, M. G., Müller, M. M., Vauzour, D., & Oteiza, P. I. (2022) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2022.109158 · Cited by 25 · see citing works
d’Oplinter, A. D. W., Verce, M., Huwart, S. J. P., Lessard‐Lord, J., Depommier, C., Hul, M. V., Desjardins, Y., Cani, P. D., & Everard, A. (2023) · Microbiome · doi:10.1186/s40168-023-01526-w · Cited by 24 · see citing works
“Moreover, it has already been shown that mice fed with a HFD for 6 weeks then suddenly switched on a low-fat diet showed increased operant response for sucrose and fat reward pellets, suggesting craving for palatable food [38].”
BackgroundModulatory Effects of Food Restriction on Brain and Behavioral Effects of Abused Drugs
Carr, K. D. (2020) · Current Pharmaceutical Design · doi:10.2174/1381612826666200204141057 · Cited by 23 · see citing works
Mayberry, H. L., Bavley, C. C., Karbalaei, R., Peterson, D. R., Bongiovanni, A. R., Ellis, A. S., Downey, S. H., Toussaint, A. B., & Wimmer, M. E. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-022-01289-2 · Cited by 22 · see citing works
“Opioid exposure induces changes in the expression and phosphorylation states of transcription factors ERK, CREB, and ΔFosB, as well as plasticityrelated genes and nuclear receptors [36, 40–43].”
BackgroundLinking drug and food addiction: an overview of the shared neural circuits and behavioral phenotype
Passeri, A., Municchi, D., Cavalieri, G., Babicola, L., Ventura, R., & Segni, M. D. (2023) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2023.1240748 · Cited by 24 · see citing works
Mediterranean X Western based diets: Opposite influences on opioid reinstatement
Milanesi, L. H., Rossato, D. R., Dias, V. T., Kronbauer, M., D’avila, L. F., Somacal, S., Duarte, T., Duarte, M. M. F. M., Emanuelli, T., & Bürger, M. E. (2019) · Toxicology Letters · doi:10.1016/j.toxlet.2019.03.009 · Cited by 24 · see citing works
Matikainen‐Ankney, B. A., Ali, M. A. S., Miyazaki, N. L., Fry, S. A., Licholai, J. A., & Kravitz, A. V. (2020) · Obesity · doi:10.1002/oby.22758 · Cited by 24 · see citing works
“Withdrawal from palatable food can increase preference (16), lever pressing (17), and cravings (18) for such foods.”
BackgroundWei, T., Mueed, A., Luo, T., Sun, Y., Zhang, B., Zheng, L., Deng, Z., & Li, J. (2024) · Food Chemistry · doi:10.1016/j.foodchem.2024.138560 · Cited by 23 · see citing works
Bello, N. T., Yeh, C., & James, M. H. (2019) · Frontiers in Psychology · doi:10.3389/fpsyg.2019.01966 · Cited by 23 · see citing works
Kiyici, S., Koca, N., Sigirli, D., Aslan, B. B., Guclu, M., & Kisakol, G. (2020) · Metabolic Syndrome and Related Disorders · doi:10.1089/met.2019.0108 · Cited by 22 · see citing works
Muñoz-Escobar, G., Guerrero‐Vargas, N. N., & Escobar, C. (2019) · Scientific Reports · doi:10.1038/s41598-019-54540-0 · Cited by 22 · see citing works
van den Heuvel, J. K., Eggels, L., Fliers, E., Kalsbeek, A., Adan, R. A. H., & la Fleur, S. E. (2014) · PLoS ONE · doi:10.1371/journal.pone.0087729 · Cited by 22 · see citing works
“Paralleling our results, most studies report a downregulation in dopamine signaling and decreased TH expression upon high fat diet exposure [29,30].”
ResultVega-Torres, J. D., Azadian, M. M., Rios-Orsini, R. A., Reyes-Rivera, A. L., Ontiveros‐Ángel, P., & Figueroa, J. D. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00562 · Cited by 20 · see citing works
de Ceglia, M., Bonaventura, M. V. M. D., Romano, A., Friuli, M., Bonaventura, E. M. D., Gavito, A., Botticelli, L., Gaetani, S., de Fonseca, F. R., & Cifani, C. (2023) · International Journal of Eating Disorders · doi:10.1002/eat.23917 · Cited by 21 · see citing works
- Authors
- Sharma, S., Fernandes, M. F., & Fulton, S.
- Affiliations
- Université de Montréal (CA)
- Corresponding author
- Fulton, S
- Venue
- International Journal of Obesity
- Published
- 2012-12-11
- Volume
- 37
- Issue
- 9
- Pages
- 1183-1191
- ISSN
- 0307-0565 (ISSN-L)
- 1476-5497
- OpenAlex
- W1969236009
- Cited by
- 231
- References
- 64
- Citations by year
- 2026: 8 · 2025: 13 · 2024: 14 · 2023: 20 · 2022: 12 · 2021: 20 · 2020: 19 · 2019: 26 · 2018: 22 · 2017: 16 · 2016: 27 · 2015: 10 · 2014: 16 · 2013: 8
- FWCI
- 4.48
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- International Journal of Obesity (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Canadian Institutes of Health Research
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Social Sciences › Psychology › Clinical Psychology › Eating Disorders and Behaviors
- Keywords
- food reward, anhedonia, anxiety, stress sensitivity, corticosterone, hypothalamic-pituitary-adrenal axis, dopamine, tyrosine hydroxylase, brain-derived neurotrophic factor, CREB, ΔFosB, amygdala, nucleus accumbens, ventral tegmental area, obesity, overeating, relapse
- MeSH terms
- CRF Receptor, Type 1, Animals, Anxiety, Behavior, Animal, Brain, Disease Models, Animal, Dopamine, Male, Mice, Inbred C57BL, Motor Activity, Neuronal Plasticity, Obesity, Promoter Regions, Genetic, Reward, Stress, Psychological, Sucrose, Tyrosine 3-Monooxygenase, Blotting, Western, Receptors, Corticotropin-Releasing Hormone, Brain-Derived Neurotrophic Factor, Mice, Diet, High-Fat
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