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From Food Preference to Craving Behavioural Traits and Molecular Mechanisms Johan Alsiö

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From Food Preference to Craving Behavioural Traits and Molecular Mechanisms Johan Alsiö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rom Food Preference to Craving Behavioural Traits and Molecular Mechanisms Johan Alsiö To tutors and tutees today and in the future List of Papers This thesis is based on the following papers, which are referred to in the text by their Roman numerals. I Alsiö, J., Roman, E., Olszewski, PK., Jonsson, P., Fredriksson, F., Levine, AS., Meyerson, BJ., Hulting, A-L., Lindblom, J., Schiöth, HB. (2009) Inverse association of high-fat diet prefer- ence and anxiety-like behavior: a putative role for urocortin 2. Genes, Brain and Behavior 8:193–202 II Alsiö, J., Pickering, C., Stephansson, O., Roman, E., Hulting, A-L., Lindblom, J., Schiöth, HB. (2010) Locomotor adaptation and elevated expression of reward-relevant genes following free-choice high-fat diet exposure. Manuscript III Alsiö, J., Pickering, P., Roman, E., Hulting, A-L., Lindblom, J., Schiöth, HB. (2009) Motivation for sucrose in sated rats is pre- dicted by low anxiety-like behavior. Neuroscience Letters 454:193–197 IV Pickering, C.*, Alsiö, J.*, Hulting, A-L., Schiöth, HB. (2009) Withdrawal from free-choice high fat high sugar diet induces craving only in obesity-prone animals. Psychopharmacology 204:431–443 V Alsiö, J., Olszewski, PK., Hallsten Norbäck, A., Gunnarsson, Z., Levine, AS., Pickering, C., Schiöth, HB. (2010) Downregu- lation of nucleus accumbens D1 and D2 receptor expression oc- curs upon exposure to and persists long-term after withdrawal from palatable food: conclusions from diet-induced obesity models. Submitted manuscript VI Alsiö, J., Stenhammar, C., Benedict, C., Hulting, A-L., Mont- gomery, SM., Edlund, B., Schiöth, HB. (2010) Parental food preferences are associated with body weight disturbance in pre- school children. Manuscript * Equal contribution Reprints were made with permission from the respective publishers. Contents Introduction...................................................................................................13 Addictive-like behaviours in obesity........................................................13 Feeding for calories..................................................................................15 Hypothalamic appetite control.............................................................15 Monogenic obesity: severe but not common .......................................16 The thrifty genotype hypothesis ..........................................................16 Food preferences..................................................................................17 Feeding for pleasure.................................................................................18 The role of dopamine in food-motivated behaviours...........................18 Opioids and food intake.......................................................................22 Diet-induced obesity in the rat .................................................................25 Food craving.............................................................................................27 The phenomenology of food craving...................................................27 Animal models of craving ...................................................................29 Personality types in obesity......................................................................31 Emotional eating ......................................................................................32 The growing problem...............................................................................32 Aims..............................................................................................................34 Material and methods....................................................................................36 Diet-induced obesity and food choices ....................................................36 Gene expression measurements................................................................37 Exploration of novel environments: rodent models .................................41 Operant self-administration......................................................................43 Questionnaires..........................................................................................44 Results and discussion ..................................................................................46 General discussion....................................................................................59 Conclusions...................................................................................................66 Acknowledgements.......................................................................................68 References.....................................................................................................71 Abbreviations AAAD Aromatic L-amino acid decarboxylase ACTH Adrenocorticotropic hormone AgRP Agouti-related peptide ARC arcuate nucleus bACT -actin BMI Body mass index bTUB -tubulin CART Cocaine- and amphetamine-regulated transcript CRF2 Corticotropin-releasing factor receptor subtype 2 COMT Catechol-o-methyl transferase CORT Corticosterone CPu Caudate putamen CRF Corticotropin-releasing factor CYCLO Cyclophilin D1 Dopamine D1 receptor D2 Dopamine D2 receptor DAT Dopamine transporter DCR Dark corner room of the MCSF DEBQ Dutch Eating Behavior Questionnaire DIO Diet induced obesity DIST Distance moved in the open field DOR Delta opioid receptor DUR Duration EPM Elevated plus-maze FCI Food Craving Inventory fMRI Functional magnetic resonance imaging FRn Fixed ratio n, e.g. FR1 for fixed ratio 1 FRQ Frequency GALP Galanin-like peptide GAPDH Glyceraldehyde 3-phosphate dehydrogenase GHRF Growth hormone-releasing factor GRF Gonadotropin-releasing factor H3b Histone protein 3b HCD High-carbohydrate diet HF High-fat HFD High-fat diet HFHS High-fat high-sugar HPD High-protein diet HS High-sugar i.c.v. intracerebroventricular KOR Kappa opioid receptor LH Lateral hypothalamaus MCH Melanin-concentrating hormone MCSF Multivariate Concentric Square Field™ MOR Mu opioid receptor NAcc Nucleus accumbens NPB Neuropeptide B NPFF Neuropeptide FF NPY Neuropeptide Y OP Obesity-prone OR Obesity-resistant PET Positron emission tomography PFC Prefrontal cortex POMC Proopiomelanocortin PR Progressive ratio PrRP Prolactin-releasing peptide PVN Paraventricular nucleus qPCR Quantitative PCR RPL19 Ribosomal protein L19 RT-PCR Reverse transcriptase PCR SAP Stretched attend posture SDCA succinate dehydrogenase complex, subunit A SPSQ Swedish Parental Stress Questionnaire TH Tyrosine hydroxylase ToRC Time of response cessation TRH Thyrotropin-releasing hormone Ucn 2 Urocortin 2 WD Withdrawal VTA Ventral tegmental area Introduction We overeat not because of hunger but because of family and friends, packages and plates, names and numbers, labels and lights, colors and candles, shapes and smells, distractions and distances, cupboards and containers. Brian Wansink, Mindless eating Addictive-like behaviours in obesity For the first time in history, there are presently more people in the world suffering from obesity than from food shortage or starvation. The modern society is extremely obesogenic, with a sedentary lifestyle and easy access to refined food products, high in fat and sugar, high in calories, and highly pal- atable. However, not all individuals exposed to this environment become obese. Vulnerability to obesity may be caused by factors that are genetic or hormonal, affected by psychological and stressful conditions or pharmacol- ogical agents, and strengthened by cultural and familial settings. The vulner- able individual in the modern obesogenic environment gains weight and becomes obese, others remain lean. Once an obesity-prone individual has gained weight, it is exceedingly dif- ficult to lose this weight. A plethora of weight loss programs exists, but even though initial weight loss is often achieved if the subjects adhere to their regimen, the excessive body weight returns as soon as the program is dropped. During abstinence from energy-dense food, craving for food, espe- cially for palatable food, is commonly reported, causing relapse to consump- tion of energy-dense foods. The subject loses control over food intake. In recent years, studies have shown that there are important parallels be- tween obesity and drug addiction [295,302]. Drug addiction is a chronic relapsing disorder characterized by individual vulnerability and a progres- sion from recreational use, through repeated use, to compulsive use [273,286]. Ultimately, if a drug addict attempts to quit the drug, drug craving ensues that may remain for extended periods
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