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Food preferences and aversions in human health and nutrition: how can pigs help the biomedical research?

Published online by Cambridge University Press:  19 August 2011

C. Clouard
Affiliation:
INRA, UMR1079 SENAH, Domaine de la Prise, 35590 Saint Gilles, France
M. C. Meunier-Salaün
Affiliation:
INRA, UMR1079 SENAH, Domaine de la Prise, 35590 Saint Gilles, France
D. Val-Laillet*
Affiliation:
INRA, UMR1079 SENAH, Domaine de la Prise, 35590 Saint Gilles, France
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Abstract

The establishment of food preferences and aversions determines the modulation of eating behaviour and the optimization of food intake. These phenomena rely on the learning and memory abilities of the organism and depend on different psychobiological mechanisms such as associative conditionings and sociocultural influences. After summarizing the various behavioural and environmental determinants of the establishment of food preferences and aversions, this paper describes several issues encountered in human nutrition when preferences and aversions become detrimental to health: development of eating disorders and obesity, aversions and anorexia in chemotherapy-treated or elderly patients and poor palatability of medical substances and drugs. Most of the relevant biomedical research has been performed in rodent models, although this approach has severe limitations, especially in the nutritional field. Consequently, the final aim of this paper is to discuss the use of the pig model to investigate the behavioural and neurophysiological mechanisms underlying the establishment of food preferences and aversions by reviewing the literature supporting analogies at multiple levels (general physiology and anatomy, sensory sensitivity, digestive function, cognitive abilities, brain features) between pigs and humans.

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Copyright © The Animal Consortium 2011

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References

Ackroff, K, Touzani, K, Peets, TK, Sclafani, A 2001. Flavor preferences conditioned by intragastric fructose and glucose: differences in reinforcement potency. Physiology & Behavior 72, 691703.CrossRefGoogle ScholarPubMed
Ackroff, K, Dym, C, Yiin, YM, Sclafani, A 2009. Rapid acquisition of conditioned flavor preferences in rats. Physiology & Behavior 97, 406413.CrossRefGoogle ScholarPubMed
Ahima, RS, Antwi, DA 2008. Brain regulation of appetite and satiety. Endocrinology Metabolism Clinics of North America 37, 811823.Google Scholar
Aleixandre de Artiñano, A, Miguel Castro, M 2009. Experimental rat models to study the metabolic syndrome. British Journal of Nutrition 102, 12461253.CrossRefGoogle ScholarPubMed
Andrews, PLR, Horn, CC 2006. Signals for nausea and emesis: implications for models of upper gastrointestinal diseases. Autonomic Neuroscience: Basic and Clinical 125, 100115.CrossRefGoogle ScholarPubMed
Andreyev, HJ, Norman, AR, Oates, J, Cunningham, D 1998. Why do patients with weight loss have a worse outcome when undergoing chemotherapy for gastrointestinal malignancies? European Journal of Cancer 34, 503509.Google Scholar
Archibald, AL, Bolund, L, Churcher, C, Fredholm, M, Groenen, MAM, Harlizius, B, Lee, KT, Milan, D, Rogers, J, Rothschild, MF, Uenishi, H, Wang, J, Schook, LB, The Swine Genome Sequencing Consortium 2010. Pig genome sequence – analysis and publication strategy. BMC Genomics 11, 438442.CrossRefGoogle ScholarPubMed
Arner, P 2005. Resistin: yet another adipokine tells us that men are not mice. Diabetologia 48, 22032205.CrossRefGoogle Scholar
Arya, R, Hansen, A, Taira, BR, Packy, T, Singer, AJ 2009. A comparison of the palatability of flavored oral contrasts. The American Journal of Emergency Medicine 27, 847850.Google Scholar
Augustine, KA, Rossi, RM 1999. Rodent mutant models of obesity and their correlations to human obesity. The Anatomical Record (New Anatomist) 257, 6472.3.0.CO;2-G>CrossRefGoogle ScholarPubMed
Baldo, BA, Kelley, AE 2007. Discrete neurochemical coding of distinguishable motivational processes: insights from nucleus accumbens control of feeding. Psychopharmacology 191, 439459.Google Scholar
Barbano, MF, Cador, M 2007. Opioids for hedonic experience and dopamine to get ready for it. Psychopharmacology 191, 497506.Google Scholar
Barbano, MF, Le Saux, M, Cador, M 2009. Involvement of dopamine and opioids in the motivation to eat: influence of palatability, homeostatic state, and behavioral paradigms. Psychopharmacology 203, 475487.Google Scholar
Baunez, C, Amalric, M, Robbins, TW 2002. Enhanced food-related motivation after bilateral lesions of the subthalamic nucleus. The Journal of Neurosciences 22, 562568.Google Scholar
Beauchamp, GK, Cowart, BJ, Mennella, JA, Marsh, RR 1994. Infant salt taste: developmental, methodological, and contextual factors. Developmental Psychobiology 27, 353365.Google Scholar
Beckoff, K, MacIntosh, CG, Chapman, IM, Wishart, JM, Morris, HA, Horowitz, M, Jones, KL 2001. Effects of glucose supplementation on gastric emptying, blood glucose homeostasis, and appetite in the elderly. American Journal of Physiology – Regulatory, Integrative and Comparative Physiology 280, R570R576.Google Scholar
Bellinger, DA, Merricks, EP, Nichols, TC 2006. Swine models of type 2 diabetes mellitus: insulin resistance, glucose tolerance, and cardiovascular complications. ILAR journal/National Research Council, Institute of Laboratory Animal Resources 47, 243258.Google Scholar
Bellisle, F 1999. Le comportement alimentaire humain. Approche scientifique. 138p.Google Scholar
Bellisle, F 2006. Des qualités organoleptiques des aliments aux choix alimentaires. Cahiers de Nutrition et de Diététiques 41, 269272.Google Scholar
Bergeron, R, Bolduc, J, Ramonet, Y, Meunier-Salaün, MC, Robert, S 2000. Feeding motivation and stereotypies in pregnant sows fed increasing levels of fibre and/or food. Applied Animal Behaviour Science 70, 2740.CrossRefGoogle ScholarPubMed
Bernhardson, BM, Tishelman, C, Rutqvist, LE 2007. Chemosensory changes experienced by patients undergoing cancer chemotherapy: a qualitative interview study. Journal of Pain and Symptom Management 34, 403412.CrossRefGoogle ScholarPubMed
Bernstein, IL 1978. Learned taste aversions in children receiving chemotherapy. Science 200, 13021303.CrossRefGoogle ScholarPubMed
Bernstein, IL 1999. Taste aversion learning: a contemporary perspective. Nutrition 15, 229234.Google Scholar
Bernstein, AM, Bloom, DE, Rosner, BA, Franz, M, Willett, WA 2010. Relation of food cost to healthfulness of diet among US women. The American Journal of Clinical Nutrition 92, 11971203.CrossRefGoogle ScholarPubMed
Berridge, KC 2000. Measuring hedonic impact in animals and infants: microstructure of affective taste reactivity patterns. Neuroscience & Biobehavioral Reviews 24, 173198.Google Scholar
Berridge, KC 2009. ‘Liking’ and ‘wanting’ food rewards: brain substrates and roles in eating disorders. Physiology & Behavior 97, 537550.Google Scholar
Berteretche, MV, Dalix, AM, d'Ornano, AM, Bellisle, F, Khayat, D, Faurion, A 2004. Decreased taste sensitivity in cancer patients under chemotherapy. Support Care Cancer 12, 571576.CrossRefGoogle ScholarPubMed
Biraben, A, Guérin, S, Bobillier, E, Val-Laillet, D, Malbert, CH 2008. Central activation after chronic vagus nerve stimulation in pigs: contribution of functional imaging. Bulletin de l'Académie Vétérinaire de France 161, 441448.Google Scholar
Birch, LL 1999. Development of food preferences. Annual Review of Nutrition 19, 4162.Google Scholar
Blundell, JE, Finlayson, G 2004. Is susceptibility to weight gain characterized by homeostatic or hedonic risk factors for overconsumption? Physiology & Behavior 82, 2125.Google Scholar
Broberg, DJ, Bernstein, IL 1987. Candy as a scapegoat in the prevention of food aversions in children receiving chemotherapy. Cancer 60, 23442347.Google Scholar
Brunstrom, JM, Mitchell, GL 2007. Flavor-nutrient learning in restrained and unrestrained eaters. Physiology & Behavior 90, 133141.CrossRefGoogle ScholarPubMed
Brunstrom, JM, Fletcher, HZ 2008. Flavour–flavour learning occurs automatically and only in hungry participants. Physiology & Behavior 93, 1319.Google Scholar
Burritt, EA, Provenza, FD 1996. Amount of experience and prior illness affect the acquisition and persistence of conditioned food aversions in lambs. Applied Animal Behaviour Science 48, 7380.Google Scholar
Campbell, A 1976. The feed intake of weaner pigs. Animal Production 23, 417419.Google Scholar
Casper, RC, Sullivan, EL, Tecott, L 2008. Relevance of animal models to human eating disorders and obesity. Psychopharmacology 199, 313329.Google Scholar
Casu, A, Echeverri, GJ, Bottino, R, van der Windt, DJ, He, J, Ekser, B, Ball, S, Ayares, D, Cooper, DKC 2010. Insulin secretion and glucose metabolism in alpha 1,3-galactosyltransferase knock-out pigs compared to wild-type pigs. Xenotransplantation 17, 131139.Google Scholar
Chalon, S, Hall, H, Saba, W, Garreau, L, Dolle, F, Halldin, C, Emond, P, Bottlaender, M, Deloye, JB, Helfenbein, J, Madelmont, JC, Bodard, S, Mincheva, Z, Besnard, JC, Guilloteau, D 2006. Pharmacological characterization of (E)-N-(4-fluorobut-2-enyl)-2beta-carbomethoxy-3beta-(4'-tolyl)nortropane (LBT-999) as a highly promising fluorinated ligand for the dopamine transporter. The Journal of Pharmacology and Experimental Therapeutics 317, 147152.CrossRefGoogle Scholar
Chima, CS, Barco, K, Dewitt, ML, Maeda, M, Teran, JC, Mullen, KD 1997. Relationship of nutritional status to length of stay, hospital costs, and discharge status of patients hospitalized in the medicine service. Journal of the American Dietetic Association 97, 975978; quiz 979–980.CrossRefGoogle ScholarPubMed
Clark, BA, Alloosh, M, Wenzel, JW, Sturek, M, Kostrominova, TY 2011. Effect of diet-induced obesity and metabolic syndrome on skeletal muscles of Ossabaw miniature swine. American Journal of Physiology – Endocrinology and Metabolism 300, E848E857.Google Scholar
Cole, GM, Ma, QL, Frautschy, SA 2010. Dietary fatty acids and the aging brain. Nutrition Reviews 68 (suppl. 2), S102S111.Google Scholar
Crogan, NL, Pasvogel, A 2003. The influence of protein–calorie malnutrition on quality of life in nursing homes. The Journals of Gerontology – Serie A: Biological Sciences and Medical Sciences 58, 159164.CrossRefGoogle ScholarPubMed
Cumming, P, M, GN, Jensen, SB, Bjarkam, CR, Gjedde, A 2003. Kinetics of the uptake and distribution of the dopamine D(2,3) agonist (R)-N-[1-(11)C]n-propylnorapomorphine in brain of healthy and MPTP-treated Göttingen miniature pigs. Nuclear Medicine and Biology 30, 547553.CrossRefGoogle Scholar
Cumming, P, Møller, M, Benda, K, Minuzzi, L, Jakobsen, S, Jensen, SB, Pakkenberg, B, Stark, AK, Gramsbergen, JB, Andreasen, MF, Olsen, AK 2007. A PET study of effects of chronic 3,4-methylenedioxymethamphetamine (MDMA, “Ecstasy”) on serotonin markers in Göttingen minipig brain. Synapse 61, 478487.Google Scholar
DeSesso, JM, Jacobson, CF 2001. Anatomical and physiological parameters affecting gastrointestinal absorption in humans and rats. Food and Chemical Toxicology 39, 209228.Google Scholar
Desgranges, B, Sevelinges, Y, Bonnefond, M, Levy, F, Ravel, N, Ferreira, G 2009. Critical role of insular cortex in taste but not odour aversion memory. The European Journal of Neuroscience 29, 16541662.CrossRefGoogle Scholar
Dong, GZ, Pluske, JR 2007. The low feed intake in newly-weaned pigs: problems and possible solutions. Asian–Australasian Journal of Animal Sciences 20, 440452.Google Scholar
Doty, RL, Shah, M 2008. Taste and smell. Encyclopedia of infant and early childhood development (ed. MM Haith and JB Benson), pp. 299308. Elsevier, Oxford, UK.CrossRefGoogle Scholar
Dourmad, JY, Etienne, M, Prunier, A, Noblet, J 1994. The effect of energy and protein-intake of sows on their longevity – a review. Livestock Production Science 40, 8797.Google Scholar
Drewnowski, A 1997. Why do we like fat? Journal of the American Dietetic Association 97 (suppl. 7), S58S62.Google Scholar
Durand, JP, Madelaine, I, Scotté, F 2009. Guidelines for prophylaxis and treatment of chemotherapy-induced nausea and vomiting. Bulletin du Cancer 96, 951960.Google ScholarPubMed
Dyson, MC, Alloosh, M, Vuchetich, JP, Mokelke, EA, Sturek, M 2006. Components of metabolic syndrome and coronary artery disease in female Ossabaw swine fed excess atherogenic diet. Comparative Medecine 56, 3545.Google ScholarPubMed
Edge, HL, Dalby, JA, Rowlinson, P, Varley, MA 2005. The effect of pellet diameter on the performance of young pigs. Livestock Production Science 97, 203209.Google Scholar
Epstein, JB, Phillips, N, Parry, J, Epstein, MS, Nevill, T, Stevenson-Moore, P 2002. Quality of life, taste, olfactory and oral function following high-dose chemotherapy and allogeneic hematopoietic cell transplantation. Bone Marrow Transplant 30, 785792.Google Scholar
Epstein, JB, Emerton, S, Kolbinson, DA, Le, ND, Phillips, N, Stevenson-Moore, P, Osoba, D 1999. Quality of life and oral function following radiotherapy for head and neck cancer. Head Neck 21, 111.Google Scholar
Ettrup, A, Kornum, B, Weikop, P, Knudsen, G 2011. An approach for serotonin depletion in pigs: effects on serotonin receptor binding. Synapse 65, 136145.CrossRefGoogle ScholarPubMed
Felix, B, Leger, ME, Albe-Fessard, D, Marcilloux, JC, Rampin, O, Laplace, JP 1999. Stereotaxic atlas of the pig brain. Brain Research Bulletin 49, 1137.CrossRefGoogle ScholarPubMed
Ferguson, SA, Gopee, NV, Paule, MG, Howard, PC 2009. Female mini-pig performance of temporal response differentiation, incremental repeated acquisition, and progressive ratio operant tasks. Behavioural Processes 80, 2834.Google Scholar
Ferreira, G 2004. Apprentissages alimentaires : mécanismes neurobiologiques impliqués dans le développement de l'aversion gustative chez le rat. Sciences des Aliments 24, 5369.CrossRefGoogle Scholar
Fetissov, SO, Petit, A, Déchelotte, P 2009. Pathophysiology of anorexia of aging. Nutrition Clinique et Métabolisme 23, 118123.Google Scholar
Forbes, JM 1995. Voluntary food intake and diet selection in farm animals. CAB International, Oxon, UK.Google Scholar
Frank, ME, Blizard, DA 1999. Chorda tympani responses in two inbred strains of mice with different taste preferences. Physiology & Behavior 67, 287297.Google Scholar
Gandarillas, M, Bas, F 2009. The domestic pig (Sus scrofa domestica) as a model for evaluating nutritional and metabolic consequences of bariatric surgery praticed on morbid obese humans. Ciencia e Investigacion Agraria 36, 163176.Google Scholar
Garcia, J, Ervin, FR, Koelling, RA 1966. Learning with prolonged delay of reinforcement. Psychonomic Science 5, 121122.Google Scholar
Garcia, J, Hankins, WG, Rusiniak, KW 1974. Behavioral regulation of the milieu interne in man and rat. Science 185, 824831.Google Scholar
Gaultier, A, Meunier-Salaün, MC, Malbert, CH, Val-Laillet, D. Flavours exposures after conditioned aversion or positive habituation trigger different brain activations in pigs. European Journal of Neuroscience (in press).Google Scholar
Gerrish, CJ, Mennella, JA 2001. Flavor variety enhances food acceptance in formula-fed infants. The American Journal of Clinical Nutrition 73, 10801085.Google Scholar
Gilbert, PE, Campbell, A, Kesner, RP 2003. The role of the amygdala in conditioned flavor preference. Neurobiology of Learning and Memory 79, 118121.Google Scholar
Ginane, C, Dumont, B 2006. Generalization of conditioned food aversions in grazing sheep and its implications for food categorization. Behavioural Processes 73, 178186.Google Scholar
Glaser, D, Manner, M, Tinti, JM, Nofre, C 2000. Gustatory responses of pigs to various natural and artificial compounds known to be sweet in man. Food Chemistry 68, 375385.Google Scholar
Grate, LL, Golden, JA, Hoopes, PJ, Hunter, JV, Duhaime, AC 2003. Traumatic brain injury in piglets of different ages: techniques for lesion analysis using histology and magnetic resonance imaging. Journal of Neuroscience Methods 123, 201206.CrossRefGoogle ScholarPubMed
Guillemet, R, Dourmad, JY, Meunier-Salaün, MC 2006. Feeding behaviour in primiparous lactating sows: impact of a high-fiber diet during pregnancy. Journal of Animal Science 84, 24742481.CrossRefGoogle ScholarPubMed
Guillemet, R, Comyn, S, Dourmad, JY, Meunier-Salaün, MC 2007. Gestating sows prefer concentrate diets to high-fibre diet in two choice tests. Applied Animal Behaviour Science 108, 251262.CrossRefGoogle Scholar
Guillemet, R, Guerin, C, Richard, F, Dourmad, JY, Meunier-Salaün, MC 2010. Feed transition between gestation and lactation is exhibited earlier in sows fed a high-fiber diet during gestation. Journal of Animal Science 88, 26372647.Google Scholar
Halaweish, FT, Kronberg, S, Hubert, MB, Rice, JA 2002. Toxic and aversive diterpenes of Euphorbia esula. Journal of Chemical Ecology 28, 15991611.Google Scholar
Halpin, CG, Skelhorn, J, Rowe, C 2008. Naïve predators and selection for rare conspicuous defended prey: the initial evolution of aposematism revisited. Animal Behaviour 75, 771781.Google Scholar
Hampson, SE, Martin, J, Jorgensen, J, Barker, M 2009. A social marketing approach to improving the nutrition of low-income women and children: an initial focus group study. Public Health Nutrition 12, 15631568.Google Scholar
Held, S, Baumgartner, J, KilBride, A, Byrne, RW, Mendl, M 2005. Foraging behaviour in domestic pigs (Sus scrofa): remembering and prioritizing food sites of different value. Animal Cognition 8, 114121.Google Scholar
Hellekant, G, Danilova, V 1996. Species differences toward sweeteners. Food Chemistry 56, 323328.Google Scholar
Hellekant, G, Danilova, V 1999. Taste in domestic pig, Sus scrofa. Journal of Animal Physiology and Animal Nutrition 82, 824.CrossRefGoogle Scholar
Hofman, MA 1985. Size and shape of the cerebral cortex in mammals. I. The cortical surface. Brain, Behavior and Evolution 27, 2840.Google Scholar
Holmes, S 1993. Food avoidance in patients undergoing cancer chemotherapy. Support Care Cancer 1, 326330.CrossRefGoogle ScholarPubMed
Houpt, TA 2000. Molecular neurobiology of ingestive behavior. Nutrition 16, 827836.Google Scholar
Houpt, KA, Zahorik, DM, Swartzman-Andert, JA 1990. Taste aversion learning in horses. Journal of Animal Science 68, 23402344.Google Scholar
Hursti, U-KK, Sjödén, P-O 1997. Food and general neophobia and their relationship with self-reported food choice: familial resemblance in Swedish families with children of ages 7–17 years. Appetite 29, 89103.CrossRefGoogle Scholar
Jokinen, MP, Clarkson, TB, Prichard, RW 1985. Animal models in atherosclerosis research. Experimental and Molecular Pathology 42, 128.Google Scholar
Kagansky, N, Berner, Y, Koren-Morag, N, Perelman, L, Knobler, H, Levy, S 2005. Poor nutritional habits are predictors of poor outcome in very old hospitalized patients. The American Journal of Clinical Nutrition 82, 784791; quiz 913–784.Google Scholar
Kelley, AE, Bakshi, VP, Haber, SN, Steininger, TL, Will, MJ, Zhang, M 2002. Opioid modulation of taste hedonics within the ventral striatum. Physiology & Behavior 76, 365377.Google Scholar
King, RH 1979. The effect of adding a feed flavour to the diets of young pigs before and after weaning. Australian Journal of Agriculture and Animal Husbandry 19, 695697.Google Scholar
Kornum, B, Knudsen, G 2011. Cognitive testing of pigs (Sus scrofa) in translational biobehavioral research. Neuroscience & Biobehavioral Reviews 35, 437451.Google Scholar
Langendijk, P, Bolhuis, JE, Laurenssen, BFA 2007. Effects of pre- and postnatal exposure to garlic and aniseed flavour on pre- and postweaning feed intake in pigs. Livestock Science 108, 284287.Google Scholar
Lawlor, PG, Lynch, PB, Caffrey, PJ, O'Doherty, JV 2003. The effect of choice feeding complete diets on the performance of weaned pigs. Animal Science 76, 401412.Google Scholar
Le, DS, Pannacciulli, N, Chen, K, Del Parigi, A, Salbe, AD, Reiman, EM, Krakoff, J 2006. Less activation of the left dorsolateral prefrontal cortex in response to a meal: a feature of obesity. The American Journal of Clinical Nutrition 84, 725731.CrossRefGoogle Scholar
Lévy, E, Scotté, F, Médioni, J, Oudard, S 2006. Nausées et vomissements chez les patients atteints de cancer. La Revue du Praticien 56, 20152019.Google Scholar
Li, X, Staszewski, L, Xu, H, Durick, K, Zoller, M, Adler, E 2002. Human receptors for sweet and umami taste. Proceedings of the National Academy of Sciences 99, 46924696.CrossRefGoogle ScholarPubMed
Li, S, Zhang, HY, Hu, CC, Lawrence, F, Gallagher, KE, Surapaneni, A, Estrem, ST, Calley, JN, Varga, G, Dow, ER, Chen, Y 2008. Assessment of diet-induced obese rats as an obesity model by comparative functional genomics. Obesity 16, 811818.Google Scholar
Lind, NM, Moustgaard, A, Jelsing, J, Vajta, G, Cumming, P, Hansen, AK 2007. The use of pigs in neuroscience: modeling brain disorders. Neuroscience & Biobehavioral Reviews 31, 728751.Google Scholar
Lind, NM, Olsen, AK, Moustgaard, A, Jensen, SB, Jakobsen, S, Hansen, AK, Arnfred, SM, Hemmingsen, RP, Gjedde, A, Cumming, P 2005. Mapping the amphetamine-evoked dopamine release in the brain of the Gottingen minipig. Brain Research Bulletin 65, 19.Google Scholar
Lindström, J, Peltonen, M, Eriksson, JG, Louheranta, A, Fogelholm, M, Usitupa, M, Tuomilehto, J 2006. High-fibre, low-fat diet predicts long-term weight loss and decreased type 2 diabetes risk: the Finnish Diabetes Prevention Study. Diabetologia 49, 912920.CrossRefGoogle ScholarPubMed
Liu, D, Hu, Y, Yang, X, Liu, Y, Wei, S, Jiang, Y 2011. Identification and genetic effects of a novel polymorphism in the distal promoter region of porcine leptin gene. Molecular Biology Reports 38, 20512057.Google Scholar
Liu, Y, Wang, Z, Yin, W, Li, Q, Cai, M, Zhang, C, Xiao, J, Hou, H, Li, H, Zu, X 2007. Severe insulin resistance and moderate glomerulosclerosis in a minipig model induced by high-fat/high-sucrose/high-cholesterol diet. Experimental animals/ Japanese Association for Laboratory Animal Science 56, 1120.Google Scholar
Lowe, MR, Levine, AS 2005. Eating motives and the controversy over dieting: eating less than needed versus less than wanted. Obesity Research 13, 797806.Google Scholar
Lowe, MR, Butryn, ML 2007. Hedonic hunger: a new dimension of appetite? Physiology & Behavior 91, 432439.Google Scholar
Lucas, F, Sclafani, A 1998. Flavor preferences conditioned by high-fat versus high-carbohydrate diets vary as a function of session length. Physiology & Behavior 66, 389395.CrossRefGoogle Scholar
Lucas, F, Azzara, AV, Sclafani, A 1997. Flavor preferences conditioned by intragastric polycose in rats: more concentrated polycose is not always more reinforcing. Physiology & Behavior 63, 714.Google Scholar
Mace, OJ, Affleck, J, Patel, N, Kellett, GL 2007. Sweet taste receptors in rat small intestine stimulate glucose absorption through apical GLUT2. Journal of Physiology 582, 379392.Google Scholar
MacIntosh, C, Morley, JE, Chapman, IM 2000. The anorexia of aging. Nutrition 16, 983995.Google Scholar
Mattes, RD 1994. Prevention of food aversions in cancer patients during treatment. Nutrition and Cancer 21, 1324.Google Scholar
Mattes, RD, Arnold, C, Boraas, M 1987. Learned food aversions among cancer chemotherapy patients. Incidence, nature, and clinical implications. Cancer 60, 25762580.3.0.CO;2-5>CrossRefGoogle ScholarPubMed
Ménard, D 2004. Functional development of the human gastrointestinal tract: hormone- and growth factor-mediated regulatory mechanisms. Canadian Journal of Gastroenterology 18, 3944.Google Scholar
Mennella, JA, Beauchamp, GK 1993. The effects of repeated exposure to garlic-flavored milk on the nursling's behavior. Pediatric Research 34, 805808.Google Scholar
Mennella, JA, Beauchamp, GK 1996. The human infants' response to vanilla flavors in mother's milk and formula. Infant Behaviour and Development 19, 1319.Google Scholar
Mennella, JA, Beauchamp, GK 2008. Optimizing oral medications for children. Clinical Therapeutics 30, 21202132.Google Scholar
Meunier-Salaün, MC, Picard, M 1996. Les facteurs de choix alimentaires chez le porc et les volailles. INRA Productions Animales 9, 339348.Google Scholar
Meunier-Salaün, MC, Bergeron, R 2005. Influence des facteurs alimentaires et environnementaux sur le comportement alimentaire: exemple du porc en croissance et de la truie. 41th conférence de Nutrition de l'Est du Canada (Animal Nutrition Association of Canada) 10–11 May, Montréal, CA, USA.Google Scholar
Meunier-Salaün, MC, Edwards, SA, Robert, S 2001. Effect of dietary fibre on the behaviour and health of the restricted fed sow. Animal Feed Science and Technology 90, 5369.Google Scholar
Meunier-Salaün, MC, Turro-Vincent, I, Picard, M 1997. Early feeding experience in chicks and piglets: effect of social factors. In Animal choices. BSAS occasional publication no. 20 (ed. JM Forbes, TLJ Lawrence, RG Rodway and MA Varley), pp. 115116. British Society of Animal Science, Edinburgh, UK.Google Scholar
Mikkelsen, M, Møller, A, Jensen, LH, Pedersen, A, Berg Harajehi, J, Pakkenberg, H 1999. MPTP-induced parkinsonism in minipigs: a behavioral, biochemical, and histological study. Neurotoxicology and teratology 21, 169175.Google Scholar
Miller, JS, Jagielo, JA, Spear, NE 1990. Changes in the retrievability of associations to elements of the compound CS determine the expression of overshadowing. Animal Learning & Behavior 18, 157161.CrossRefGoogle Scholar
Minuzzi, L, Losen, AK, Bender, D, Arnfred, S, Grant, R, Danielsen, EH, Cumming, P 2006. Quantitative autoradiography of ligands for dopamine receptors and transporters in brain of Göttingen minipigs: comparison with results in vivo. Synapse 59, 211219.Google Scholar
Miyoshi, N, Horiuchi, M, Inokuchi, Y, Miyamoto, Y, Miura, N, Tokunaga, S, Fujiki, M, Izumi, Y, Miyajima, H, Nagata, R, Misumi, K, Takeuchi, T, Tanimoto, A, Yasuda, N, Yoshida, H, Kawaguchi, H 2010. Novel microminipig model of atherosclerosis by high fat and high cholesterol diet, established in Japan. In Vivo 24, 671680.Google Scholar
Mizushige, T, Inoue, K, Fushiki, T 2007. Why is fat so tasty? Chemical reception of fatty acid on the tongue. Journal of Nutritional Science and Vitaminology (Tokyo) 53, 14.CrossRefGoogle ScholarPubMed
Mobini, S, Chambers, LC, Yeomans, MR 2007. Effects of hunger state on flavour pleasantness conditioning at home: flavour-nutrient learning vs. flavour–flavour learning. Appetite 48, 2028.CrossRefGoogle ScholarPubMed
Moran, AW, Al-Rammahi, MA, Arora, DK, Batchelor, SJ, Coulter, EA, Daly, K, Ionescu, C, Bravo, D, Shirazi-Beechey, SP 2010a. Expression of Na+/glucose co-transporter 1 (SGLT1) is enhanced by supplementation of the diet of weaning piglets with artificial sweeteners. British Journal of Nutrition 104, 637646.Google Scholar
Moran, AW, Al-Rammahi, MA, Arora, DK, Batchelor, DJ, Coulter, EA, Ionescu, C, Bravo, D, Shirazi-Beechey, SP 2010bBritish Journal of Nutrition 104, 647655.Google Scholar
Myers, KP 2007. Robust preference for a flavor paired with intragastric glucose acquired in a single trial. Appetite 48, 123127.Google Scholar
Myers, KP, Sclafani, A 2006. Development of learned flavor preferences. Developmental Psychobiology 48, 380388.Google Scholar
Niblock, MM, Luce, CJ, Belliveau, RA, Paterson, DS, Kelly, ML, Sleeper, LA, Filiano, JJ, Kinney, HC 2005. Comparative anatomical assessment of the piglet as a model for the developing human medullary serotonergic system. Brain Research Reviews 50, 169183.CrossRefGoogle Scholar
Nofre, C, Glaser, D, Tinti, JM, Wanner, M 2002. Gustatory responses of pigs to sixty compounds tasting sweet to humans. Journal of Animal Physiology and Animal Nutrition (Berlin) 86, 9096.Google Scholar
Ohrn, KE, Sjoden, PO, Wahlin, YB, Elf, M 2001. Oral health and quality of life among patients with head and neck cancer or haematological malignancies. Support Care Cancer 9, 528538.Google Scholar
Oostindjer, M, Bolhuis, JE, van den Brand, H, Roura, E, Kemp, B 2010. A prenatal exposure affects growth, health and behavior of newly weaned piglets. Physiology & Behavior 99, 579586.Google Scholar
Paradis, S, Cabanac, M 2004. Flavor aversion learning induced by lithium chloride in reptiles but not in amphibians. Behavioural Processes 67, 1118.Google Scholar
Pavlov, IP 1960. Conditioned reflexes: An investigation of the physiological activity of the cerebral cortex. Dover Publications, Inc. 1927, New York. 430p.Google Scholar
Pfister, JA, Stegelmeier, BL, Cheney, CD, Gardner, DR 2007. Effect of previous locoweed (Astragalus and Oxytropis species) intoxication on conditioned taste aversions in horses and sheep. Journal of Animal Science 85, 18361841.Google Scholar
Philippe, FX, Remience, V, Dourmad, JY, Cabaraux, JF, Vandenheede, M, Nicks, B 2008. Les fibres dans l'alimentation des truies gestantes : effets sur la nutrition, le comportement, les performances et les rejets dans l'environnement. INRA Productions Animales 21, 277290.Google Scholar
Pickering, C, Alsiö, J, Hulting, AL, Schiöth, HB 2009. Withdrawal from free-choice high-fat high-sugar diet induces craving only in obesity-prone animals. Psychopharmacology 204, 431443.Google Scholar
Pitkänen, A, Kemppainen, S 2002. Comparison of the distribution of calcium-binding proteins and intrinsic connectivity in the lateral nucleus of the rat, monkey, and human amygdala. Pharmacology, Biochemistry and Behavior 71, 369377.Google Scholar
Popkin, BM, Doak, CM 1998. The obesity epidemic is a worldwide phenomenon. Nutrition Reviews 56, 106114.Google Scholar
Prelusky, D 1993. The effect of low-level deoxynivalenol on neurotransmitter levels measured in pig cerebral spinal fluid. Journal of Environmental Science and Health. Part B 28, 731761.Google Scholar
Pritchett, CE, Pardee, AL, McGuirk, SR, Will, MJ 2010. The role of nucleus accumbens adenosine-opioid interaction in mediating palatable food intake. Brain Research 1306, 8592.Google Scholar
Ravasco, P 2005. Aspects of taste and compliance in patients with cancer. European Journal of Oncology Nursing 9 (suppl. 2), S84S91.CrossRefGoogle ScholarPubMed
Reilly, S 1999. The parabrachial nucleus and conditioned taste aversion. Brain Research Bulletin 48, 239254.Google Scholar
Reilly, S, Trifunovic, R 2000. Lateral parabrachial nucleus lesions in the rat: aversive and appetitive gustatory conditioning. Brain Research Bulletin 52, 269278.Google Scholar
Ripamonti, C, Zecca, E, Brunelli, C, Fulfaro, F, Villa, S, Balzarini, A, Bombardieri, E, De Conno, F 1998. A randomized, controlled clinical trial to evaluate the effects of zinc sulfate on cancer patients with taste alterations caused by head and neck irradiation. Cancer 82, 19381945.Google Scholar
Ritman, EL 2007. Small-animal CT – its difference from, and impact on clinical CT. Nuclear Instruments and Methods in Physics Research Section A 580, 968970.Google Scholar
Robert, S, Bergeron, R, Farmer, C, Meunier-Salaün, M-C 2002. Does the number of daily meals affect feeding motivation and behaviour of gilts fed high-fibre diets? Applied Animal Behaviour Science 76, 105117.Google Scholar
Røhl, L, Sakoh, M, Simonsen, CZ, Vestergaard-Poulsen, P, Sangill, R, Sørensen, JC, Bjarkam, CR, Gyldensted, C, Østergaard, L 2002. Time evolution of cerebral perfusion and apparent diffusion coefficient measured by magnetic resonance imaging in a porcine stroke model. Journal of Magnetic Resonance Imaging 15, 123129.Google Scholar
Roman, C, Lin, JY, Reilly, S 2009. Conditioned taste aversion and latent inhibition following extensive taste preexposure in rats with insular cortex lesions. Brain Research 1259, 6873.Google Scholar
Rosa-Neto, P, Gjedde, A, Olsen, AK, Jensen, SB, Munk, OL, Watanabe, H, Cumming, P 2004. MDMA-evoked changes in [11C]raclopride and [11C]NMSP binding in living pig brain. Synapse 53, 222233.Google Scholar
Sahni, D, Kaur, GD, Jit, H, Jit, I 2008. Anatomy & distribution of coronary arteries in pig in comparison with man. The Indian Journal of Medical Research 127, 564570.Google Scholar
Saikali, S, Meurice, P, Sauleau, P, Eliat, P-A, Bellaud, P, Randuineau, G, Vérin, M, Malbert, CH 2010. A three-dimensional digital segmented and deformable brain atlas of the domestic pig. Journal of Neuroscience Methods. Journal of Neuroscience Methods 192, 102109.Google Scholar
Saint-Dizier, H, Levy, F, Ferreira, G 2007. Influence of the mother in the development of flavored-food preference in lambs. Developmental Psychobiology 49, 98106.CrossRefGoogle ScholarPubMed
Sakoh, M, Røhl, L, Gyldensted, C, Gjedde, A, Østergaard, L 2000. Cerebral blood flow and blood volume measured by magnetic resonance imaging bolus tracking after acute stroke in pigs: comparison with [15O]H2O positron emission tomography. Stroke 31, 19581964.Google Scholar
Sauleau, P, Lapouble, E, Val-Laillet, D, Malbert, CH 2009. The pig model in brain imaging and neurosurgery. Animal 3, 11381151.Google Scholar
Schlatter, P, Beglinger, C, Drewe, J, Gutmann, H 2007. Glucagon-like peptide 1 receptor expression in primary porcine proximal tubular cells. Regulatory Peptides 141, 120128.Google Scholar
Schöne, F, Vetter, A, Hartung, H, Bergmann, H, Biertümpfel, A, Richter, G, Müller, S, Breitschuh, G 2006. Effects of essential oils from fennel (Foeniculi aetheroleum) and caraway (Carvi aetheroleum) in pigs. Journal of Animal Physiology and Animal Nutrition 90, 500510.Google Scholar
Schwartz, MD, Jacobsen, PB, Bovbjerg, DH 1996. Role of nausea in the development of aversions to a beverage paired with chemotherapy treatment in cancer patients. Physiology & Behavior 59, 659663.Google Scholar
Sclafani, A 2001. Post-ingestive positive controls of ingestive behavior. Appetite 36, 7983.Google Scholar
Sclafani, A 2007. Sweet taste signalling in the gut. Proceedings of the National Academy of Sciences 104, 1488714888.Google Scholar
Sclafani, A, Ackroff, K 1994. Glucose- and fructose-conditioned flavor preferences in rats: taste versus postingestive conditioning. Physiology & Behavior 56, 399405.Google Scholar
Shirazi-Beechey, SP, Moran, AW, Bravo, D, Al-Rammahi, M 2011. NONRUMINANT NUTRITION SYMPOSIUM: Intestinal glucose sensing and regulation of glucose absorption: Implications for swine nutrition. Journal of Animal Sciences 89, 18541862.Google Scholar
Singh-Manoux, A, Gourmelen, J, Lajnef, M, Sabia, S, Sitta, R, Menvielle, G, Melchior, M, Nabi, H, Lanoe, JL, Gueguen, A, Lert, F 2009. Prevalence of educational inequalities in obesity between 1970 and 2003 in France. Obesity Review 10, 511518.Google Scholar
Skelhorn, J, Rowe, C 2006. Prey palatability influences predator learning and memory. Animal Behaviour 71, 11111118.Google Scholar
Skelhorn, J, Griksaitis, D, Rowe, C 2008. Colour biases are more than a question of taste. Animal Behaviour 75, 827835.Google Scholar
Sola-Oriol, D, Roura, E, Torrallardona, D 2009. Feed preference in pigs: effect of cereal sources at different inclusion rates. Journal of Animal Science 87, 562570.Google Scholar
Speakman, J, Hambly, C, Mitchell, S, Król, E 2008. The contribution of animal models to the study of obesity. Laboratory Animals 42, 413432.Google Scholar
Spurlock, ME, Gabler, NK 2008. The development of porcine models of obesity and the metabolic syndrome. The Journal of Nutrition 138, 397402.Google Scholar
St-Arnaud-McKenzie, D, Paquet, C, Kergoat, MJ, Ferland, G, Dube, L 2004. Hunger and aversion: drives that influence food intake of hospitalized geriatric patients. The Journals of Gerontology – Series A: Biological Sciences and Medical Sciences 59, 13041309.Google Scholar
Stein, CJ, Colditz, GA 2004. The epidemic of obesity. The Journal of Clinical Endocrinology and Metabolism 89, 25222525.Google Scholar
Steiner, JE 1979. Human facial expressions in response to taste and smell stimulation. Advances in Child Development and Behavior 13, 257295.Google Scholar
Steinert, RE, Frey, F, Töpfer, A, Drewe, J, Beglinger, C 2011. Effects of carbohydrate sugars and artificial sweeteners on appetite and the secretion of gastrointestinal satiety peptides. British Journal of Nutrition 24, 19.Google Scholar
Stockhorst, U, Enck, P, Klosterhalfen, S 2007. Role of classical conditioning in learning gastrointestinal symptoms. World Journal of Gastroenterology 13, 34303437.Google Scholar
Stockhorst, U, Wiener, JA, Klosterhalfen, S, Klosterhalfen, W, Aul, C, Steingruber, HJ 1998. Effects of overshadowing on conditioned nausea in cancer patients: an experimental study. Physiology & Behavior 64, 743753.Google Scholar
Sturm, R 2002. The effects of obesity, smoking, and drinking on medical problems and costs. Health Affairs (Millwood) 21, 245253.Google Scholar
Tai, YC, Ruangma, A, Rowland, D, Siegel, S, Newport, DF, Chow, PL, Laforest, R 2005. Performance evaluation of the microPET focus: a third-generation microPET scanner dedicated to animal imaging. Journal of Nuclear Medicine 46, 455463.Google Scholar
Teegarden, SL, Bale, TL 2008. Effects of stress on dietary preference and intake are dependent on access and stress sensitivity. Physiology & Behavior 93, 713723.Google Scholar
Terrick, TD, Mumme, RL, Burghardt, GM 1995. Aposematic coloration enhances chemosensory recognition of noxious prey in the garter snake Thamnophis radix. Animal Behaviour 49, 857866.Google Scholar
Thanos, PK, Michaelides, M, Gispert, JD, Pascau, J, Soto-Montenegro, ML, Desco, M, Wang, R, Wang, GJ, Volkow, ND 2008. Differences in responses to food stimuli in a rat model of obesity: in-vivo assessment of brain glucose metabolism. International Journal of Obesity 32, 11711179.Google Scholar
Tinti, JM, Glaser, D, Wanner, M, Nofre, C 2000. Comparison of gustatory responses to amino acids in pigs and in humans. Lebensmittel-Wissenschaft und-Technologie 33, 578583.Google Scholar
Touzani, K, Sclafani, A 2005. Critical role of amygdala in flavor but not taste preference learning in rats. The European Journal of Neuroscience 22, 17671774.Google Scholar
Touzani, K, Sclafani, A 2007. Insular cortex lesions fail to block flavor and taste preference learning in rats. The European Journal of Neuroscience 26, 16921700.Google Scholar
Touzani, K, Bodnar, RJ, Sclafani, A 2009a. Lateral hypothalamus dopamine D1-like receptors and glucose-conditioned flavor preferences in rats. Neurobiology of Learning and Memory 92, 464467.Google Scholar
Touzani, K, Bodnar, RJ, Sclafani, A 2009b. Dopamine D1-like receptor antagonism in amygdala impairs the acquisition of glucose-conditioned flavor preference in rats. The European Journal of Neuroscience 30, 289298.Google Scholar
Treasure, JL, Owen, JB 1997. Intriguing links between animal behavior and anorexia nervosa. International Journal of Eating Disorders 21, 307311.Google Scholar
Val-Laillet, D, Guérin, S, Malbert, CH 2010a. Slower eating rate is independent to gastric emptying in obese minipigs. Physiology & Behavior 101, 462468.Google Scholar
Val-Laillet, D, Blat, S, Louveau, I, Malbert, CH 2010b. A computed tomography scan application to evaluate adiposity in a minipig model of human obesity. British Journal of Nutrition 104, 17171728.Google Scholar
Val-Laillet, D, Biraben, A, Randuineau, G, Malbert, CH 2010c. Chronic vagus nerve stimulation decreased weight gain, food consumption and sweet craving in adult obese minipig. Appetite 55, 245252.Google Scholar
Val-Laillet, D, Gaultier, A, Malbert, CH, Meunier-Salaün, MC 2010d. Conditioned flavor aversion and preference in pigs: a SPECT study. Proceedings of the 40th Annual Meeting of the Society for Neuroscience, San Diego, USA, November 2010.Google Scholar
Val-Laillet, D, Layec, S, Guérin, S, Meurice, P, Malbert, CH 2011. Changes in brain activity after a diet-induced obesity. Obesity 19, 749756.Google Scholar
Vodicka, P, JrSmetana, K, Dvorankova, B, Emerick, T, Xu, YZ, Ourednik, J, Ourednik, V, Motlik, J 2005. The miniature pig as an animal model in biomedical research. Annals of the New York Academy of Sciences 1049, 161171.Google Scholar
Volkow, ND, Wang, GJ, Telang, F, Fowler, JS, Thanos, PK, Logan, J, Alexoff, D, Ding, YS, Wong, C, Ma, Y, Pradhan, K 2008. Low dopamine striatal D2 receptors are associated with prefrontal metabolism in obese subjects: possible contributing factors. NeuroImage 42, 15371543.Google Scholar
Wang, GJ, Volkow, ND, Logan, J, Pappas, NR, Wong, CT, Zhu, W, Netusil, N, Fowler, JS 2001. Brain dopamine and obesity. The Lancet 357, 354357.Google Scholar
Wang, J, Zuo, CT, Jiang, YP, Guan, YH, Chen, ZP, Xiang, JD, Yang, LQ, Ding, ZT, Wu, JJ, Su, HL 2007. 18F-FP-CIT PET imaging and SPM analysis of dopamine transporters in Parkinson's disease in various Hoehn & Yahr stages. Journal of Neurology 254, 185190.Google Scholar
Wardle, J 2007. Eating behaviour and obesity. Obesity Review 8 (Suppl. 1), 7375.Google Scholar
Wardle, J, Cooke, L 2008. Genetic and environmental determinants of children's food preferences. The British Journal of Nutrition 99 (Suppl. 1), S15S21.Google Scholar
Warwick, ZS, Weingarten, HP 1994. Dissociation of palatability and calorie effects in learned flavor preferences. Physiology & Behavior 55, 501504.Google Scholar
Warwick, ZS, Weingarten, HP 1996. Flavor-postingestive consequence associations incorporate the behaviorally opposing effects of positive reinforcement and anticipated satiety: implications for interpreting two-bottle tests. Physiology & Behavior 60, 711715.Google Scholar
Wassum, KM, Ostlund, SB, Maidment, NT, Balleine, BW 2009. Distinct opioid circuits determine the palatability and the desirability of rewarding events. Proceedings of the National Academy of Sciences of the United States of America 106, 1251212517.Google Scholar
Watanabe, H, Andersen, F, Simonsen, CZ, Evans, SM, Gjedde, A, Cumming, P, DaNex Study Group 2001. MR-based statistical atlas of the Göttingen minipig brain. NeuroImage 14, 10891096.Google Scholar
Welzl, H, D'Adamo, P, Lipp, HP 2001. Conditioned taste aversion as a learning and memory paradigm. Behavioural Brain Research 125, 205213.Google Scholar
Weyant, MJ, Eachempati, SR, Maluccio, MA, Rivadeneira, DE, Grobmyer, SR, Hydo, LJ, Barie, PS 2000. Interpretation of computed tomography does not correlate with laboratory or pathologic findings in surgically confirmed acute appendicitis. Surgery 128, 145152.Google Scholar
Will, MJ, Pratt, WE, Kelley, AE 2006. Pharmacological characterization of high-fat feeding induced by opioid stimulation of the ventral striatum. Physiology & Behavior 89, 226234.Google Scholar
Wood, IS, Trayhurn, P 2003. Glucose transporters (GLUT and SGLT): expanded families of sugar transport proteins. British Journal of Nutrition 89, 39.Google Scholar
Wu, H, Pal, D, Song, TY, Sullivan, JA, Tai, YC 2008. Micro insert: a prototype full-ring PET device for improving the image resolution of a small animal PET scanner. Journal of Nuclear Medicine 49, 16681676.Google Scholar
Xi, S, Yin, W, Wang, Z, Kusunoki, M, Lian, X, Koike, T, Fan, J, Zhang, Q 2004. A minipig model of high-fat/high-sucrose diet-induced diabetes and atherosclerosis. International Journal of Experimental Pathology 85, 223231.Google Scholar
Yanovski, S 2003. Sugar and fat: cravings and aversions. The Journal of Nutrition 133 (suppl. 3), 835S837S.Google Scholar
Yasoshima, Y, Morimoto, T, Yamamoto, T 2000. Different disruptive effects on the acquisition and expression of conditioned taste aversion by blockades of amygdalar ionotropic and metabotropic glutamatergic receptor subtypes in rats. Brain Research 869, 1524.CrossRefGoogle ScholarPubMed
Zeinstra, GG, Koelen, MA, Kok, FJ, de Graaf, C 2009. Children's hard-wired aversion to pure vegetable tastes. A ‘failed’ flavour–nutrient learning study. Appetite 52, 528530.Google Scholar