Review

Research progress in food preferences mechanisms and their impact on obesity

  • Piao KANG ,
  • Ying ZHANG ,
  • Huating LI
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  • Department of Endocrinology and Metabolism, Shanghai Sixth People′s Hospital, Shanghai Jiao Tong University School of Medicine; Shanghai Diabetes Institute; Shanghai Key Laboratory of Diabetes Mellitus; Shanghai Clinical Center for Diabetes, Shanghai 200233, China
LI Huating, E-mail: huarting99@sjtu.edu.cn.

Received date: 2024-02-23

  Accepted date: 2024-08-15

  Online published: 2024-09-28

Supported by

National Natural Science Foundation of China(82270907);“Two-Hundred Talents” Program of Shanghai Jiao Tong University School of Medicine(20191830);Innovative Research Team of High-level Local Universities in Shanghai(SHSMUZDCX20212700);Shanghai “Top Priority” Clinical Medical Center Construction Project(2022ZZ01002)

Abstract

In recent years, the global prevalence of obesity has continued to rise, with a preference for high-sugar and high-fat foods being one of the primary contributors to this condition. Food preference refers to the degree of individual liking for specific foods, and its formation is closely related to the physiological effects such as satiety, satisfaction and reward that occur after food digestion in the gastrointestinal tract. With the continuous advancement of technologies such as neuroimaging and chemogenetics, the underlying neural and physiological mechanisms of food preference behavior are gradually being elucidated. Studies have shown that the digestion and absorption of food in the gastrointestinal tract can release chemical or electrical signals, which are transmitted to the central nervous system via neural pathways, humoral pathways and the gut-brain axis mediated by gut microbiota. Subsequently, these signals regulate feeding behavior by activating or inhibiting neurons in the nucleus of the solitary tract, the dopaminergic reward pathways and relevant neural circuits in the hypothalamus. Based on this, the article introduces the definition, evaluation methods and mechanisms of food preference, and reviews the pathways of food information transmission within the gut-brain axis, the reward circuits that modulate food preference and the application of food preference behavior to the treatment of obesity, in order to provide reference for research in the field of food preference and obesity treatment.

Cite this article

Piao KANG , Ying ZHANG , Huating LI . Research progress in food preferences mechanisms and their impact on obesity[J]. Journal of Shanghai Jiao Tong University (Medical Science), 2024 , 44(9) : 1190 -1196 . DOI: 10.3969/j.issn.1674-8115.2024.09.014

References

1 CHOOI Y C, DING C, MAGKOS F. The epidemiology of obesity[J]. Metabolism, 2019, 92: 6-10.
2 KOLIAKI C, DALAMAGA M, LIATIS S. Update on the obesity epidemic: after the sudden rise, is the upward trajectory beginning to flatten?[J]. Curr Obes Rep, 2023, 12(4): 514-527.
3 CHEN K, SHEN Z W, GU W J, et al. Prevalence of obesity and associated complications in China: a cross-sectional, real-world study in 15.8 million adults[J]. Diabetes Obes Metab, 2023, 25(11): 3390-3399.
4 CONGDON P, AMUGSI D. Editorial: the obesity epidemic: causes, context, prevention[J]. Front Public Health, 2022, 10: 1030180.
5 ROH E, CHOI K M. Hormonal gut-brain signaling for the treatment of obesity[J]. Int J Mol Sci, 2023, 24(4): 3384.
6 TARRAGON E, MORENO J J. Role of endocannabinoids on sweet taste perception, food preference, and obesity-related disorders[J]. Chem Senses, 2017, 43(1): 3-16.
7 OUSTRIC P, THIVEL D, DALTON M, et al. Measuring food preference and reward: application and cross-cultural adaptation of the Leeds Food Preference Questionnaire in human experimental research[J]. Food Qual Prefer, 2020, 80: 103824.
8 DE BRUIJN S E M, DE VRIES Y C, DE GRAAF C, et al. The reliability and validity of the Macronutrient and Taste Preference Ranking Task: a new method to measure food preferences[J]. Food Qual Prefer, 2017, 57: 32-40.
9 EDWIN THANARAJAH S, DIFELICEANTONIO A G, ALBUS K, et al. Habitual daily intake of a sweet and fatty snack modulates reward processing in humans[J]. Cell Metab, 2023, 35(4): 571-584.e6.
10 VAN GALEN K A, SCHRANTEE A, TER HORST K W, et al. Brain responses to nutrients are severely impaired and not reversed by weight loss in humans with obesity: a randomized crossover study[J]. Nat Metab, 2023, 5(6): 1059-1072.
11 LI M T, TAN H E, LU Z Y, et al. Gut-brain circuits for fat preference[J]. Nature, 2022, 610(7933): 722-730.
12 TAN H E, SISTI A C, JIN H, et al. The gut-brain axis mediates sugar preference[J]. Nature, 2020, 580(7804): 511-516.
13 ELIAN V, POPOVICI V, KARAMPELAS O, et al. Risks and benefits of SGLT-2 inhibitors for type 1 diabetes patients using automated insulin delivery systems: a literature review[J]. Int J Mol Sci, 2024, 25(4): 1972.
14 KAELBERER M M, BUCHANAN K L, KLEIN M E, et al. A gut-brain neural circuit for nutrient sensory transduction[J]. Science, 2018, 361(6408): eaat5236.
15 JAIME-LARA R B, BROOKS B E, VIZIOLI C, et al. A systematic review of the biological mediators of fat taste and smell[J]. Physiol Rev, 2023, 103(1): 855-918.
16 SPANIER B, ROHM F. Proton coupled oligopeptide transporter 1 (PepT1) function, regulation, and influence on the intestinal homeostasis[J]. Compr Physiol, 2018, 8(2): 843-869.
17 QIAN L, LI N, LU X C, et al. Enhanced BCAT1 activity and BCAA metabolism promotes RhoC activity in cancer progression[J]. Nat Metab, 2023, 5(7): 1159-1173.
18 BERTHOUD H R, MORRISON C D, ACKROFF K, et al. Learning of food preferences: mechanisms and implications for obesity & metabolic diseases[J]. Int J Obes (Lond), 2021, 45(10): 2156-2168.
19 LIU W W, BOHóRQUEZ D V. The neural basis of sugar preference[J]. Nat Rev Neurosci, 2022, 23(10): 584-595.
20 KHAN M S, SPANN R A, MüNZBERG H, et al. Protein appetite at the interface between nutrient sensing and physiological homeostasis[J]. Nutrients, 2021, 13(11): 4103.
21 MüNZBERG H, BERTHOUD H R, NEUHUBER W L. Sensory spinal interoceptive pathways and energy balance regulation[J]. Mol Metab, 2023, 78: 101817.
22 HUANG K P, GOODSON M L, VANG W, et al. Leptin signaling in vagal afferent neurons supports the absorption and storage of nutrients from high-fat diet[J]. Int J Obes (Lond), 2021, 45(2): 348-357.
23 WOODS C A, GUTTMAN Z R, HUANG D, et al. Insulin receptor activation in the nucleus accumbens reflects nutritive value of a recently ingested meal[J]. Physiol Behav, 2016, 159: 52-63.
24 GUZMáN A, HERNáNDEZ-CORONADO C G, ROSALES-TORRES A M, et al. Leptin regulates neuropeptides associated with food intake and GnRH secretion[J]. Ann Endocrinol, 2019, 80(1): 38-46.
25 JENSEN-CODY S O, FLIPPO K H, CLAFLIN K E, et al. FGF21 signals to glutamatergic neurons in the ventromedial hypothalamus to suppress carbohydrate intake[J]. Cell Metab, 2020, 32(2): 273-286.e6.
26 HILL C M, LAEGER T, DEHNER M, et al. FGF21 signals protein status to the brain and adaptively regulates food choice and metabolism[J]. Cell Rep, 2019, 27(10): 2934-2947.e3.
27 FLIPPO K H, JENSEN-CODY S O, CLAFLIN K E, et al. FGF21 signaling in glutamatergic neurons is required for weight loss associated with dietary protein dilution[J]. Sci Rep, 2020, 10(1): 19521.
28 YU K B, HSIAO E Y. Roles for the gut microbiota in regulating neuronal feeding circuits[J]. J Clin Invest, 2021, 131(10): e143772.
29 TREVELLINE B K, KOHL K D. The gut microbiome influences host diet selection behavior[J]. Proc Natl Acad Sci USA, 2022, 119(17): e2117537119.
30 YAO Z P, SCOTT K. Serotonergic neurons translate taste detection into internal nutrient regulation[J]. Neuron, 2022, 110(6): 1036-1050.e7.
31 DE WOUTERS D′OPLINTER A, RASTELLI M, VAN HUL M, et al. Gut microbes participate in food preference alterations during obesity[J]. Gut Microbes, 2021, 13(1): 1959242.
32 FAN S J, GUO W W, XIAO D, et al. Microbiota-gut-brain axis drives overeating disorders[J]. Cell Metab, 2023, 35(11): 2011-2027.e7.
33 WATTS A G, KANOSKI S E, SANCHEZ-WATTS G, et al. The physiological control of eating: signals, neurons, and networks[J]. Physiol Rev, 2022, 102(2): 689-813.
34 TELLEZ L A, HAN W F, ZHANG X B, et al. Separate circuitries encode the hedonic and nutritional values of sugar[J]. Nat Neurosci, 2016, 19(3): 465-470.
35 GEISLER C E, HAYES M R. Metabolic hormone action in the VTA: reward-directed behavior and mechanistic insights[J]. Physiol Behav, 2023, 268: 114236.
36 HAN W F, TELLEZ L A, PERKINS M H, et al. A neural circuit for gut-induced reward[J]. Cell, 2018, 175(3): 887-888.
37 FERNANDES A B, ALVES DA SILVA J, ALMEIDA J, et al. Postingestive modulation of food seeking depends on vagus-mediated dopamine neuron activity[J]. Neuron, 2020, 106(5): 778-788.e6.
38 BERRIOS J, LI C A, MADARA J C, et al. Food cue regulation of AGRP hunger neurons guides learning[J]. Nature, 2021, 595(7869): 695-700.
39 SAYAR-ATASOY N, YAVUZ Y, LAULE C, et al. Opioidergic signaling contributes to food-mediated suppression of AgRP neurons[J]. Cell Rep, 2024, 43(1): 113630.
40 NYEMA N T, MCKNIGHT A D, VARGAS-ELVIRA A G, et al. AgRP neuron activity promotes associations between sensory and nutritive signals to guide flavor preference[J]. Mol Metab, 2023, 78: 101833.
41 LIU H L, HE Y, BAI J L, et al. Hypothalamic Grb10 enhances leptin signalling and promotes weight loss[J]. Nat Metab, 2023, 5(1): 147-164.
42 BEAULIEU K, HOPKINS M, GIBBONS C, et al. Exercise training reduces reward for high-fat food in adults with overweight/obesity[J]. Med Sci Sports Exerc, 2020, 52(4): 900-908.
43 THACKRAY A E, HINTON E C, ALANAZI T M, et al. Exploring the acute effects of running on cerebral blood flow and food cue reactivity in healthy young men using functional magnetic resonance imaging[J]. Hum Brain Mapp, 2023, 44(9): 3815-3832.
44 ALABDULJABBAR K, AL-NAJIM W, LE ROUX C W. Food preferences after bariatric surgery: a review update[J]. Intern Emerg Med, 2023, 18(2): 351-358.
45 LI Y Q, PENG Y, SHEN Y B, et al. Dietary polyphenols: regulate the advanced glycation end products-RAGE axis and the microbiota-gut-brain axis to prevent neurodegenerative diseases[J]. Crit Rev Food Sci Nutr, 2023, 63(29): 9816-9842.
46 LI Y, QIN C, DONG L Z, et al. Whole grain benefit: synergistic effect of oat phenolic compounds and β-glucan on hyperlipidemia via gut microbiota in high-fat-diet mice[J]. Food Funct, 2022, 13(24): 12686-12696.
47 WENINGER S N, HERMAN C, MEYER R K, et al. Oligofructose improves small intestinal lipid-sensing mechanisms via alterations to the small intestinal microbiota[J]. Microbiome, 2023, 11(1): 169.
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