Flavour exposures after conditioned aversion or preference trigger different brain processes in anaesthetised pigs

European Journal of Neuroscience

Volumn 34, Issue 9, 2011, Pages 1500-1511

  Gaultier, A ^a   Meunier Salaun M C ^a   Malbert, C H ^a   Val Laillet, D ^a  

^a CEMAGREF   (France)

Author keywords

Brain imaging; Dorsal striatum; Food reward; Hedonism; Prefrontal cortex

Indexed keywords

LITHIUM CHLORIDE; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ARTICLE; AVERSION; CINNAMON; CONDITIONING; CONTROLLED STUDY; DIGESTIVE SYSTEM DISEASE; EMOTION; FEEDING; FLAVOR; FOOD PREFERENCE; LEARNING; LIMBIC CORTEX; MALAISE; MEMORY; MOTIVATION; NERVE CELL NETWORK; NEUROIMAGING; NONHUMAN; PRIORITY JOURNAL; REINFORCEMENT; REWARD; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; SWINE; THALAMUS VENTRAL NUCLEUS; THYME;

ANESTHESIA; ANIMALS; ANTIMANIC AGENTS; AVOIDANCE LEARNING; BRAIN; BRAIN MAPPING; CHOICE BEHAVIOR; CONDITIONING (PSYCHOLOGY); DUODENOGASTRIC REFLUX; FEEDING BEHAVIOR; FLAVORING AGENTS; FOOD PREFERENCES; LITHIUM CHLORIDE; POSTURE; REWARD; SWINE; TECHNETIUM TC 99M SESTAMIBI; TOMOGRAPHY, EMISSION-COMPUTED, SINGLE-PHOTON;

EID: 80055028557     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2011.07848.x     Document Type: Article

References (96)

1. Addessi, E., Galloway, A.T., Birch, L. & Visalberghi, E. (2004) Taste perception and food choices in capuchin monkeys and human children. Primatologie, 6, 101-128.
2. de Araujo, I.E., Rolls, E.T., Velazco, M.I., Margot, C. & Cayeux, I. (2005) Cognitive modulation of olfactory processing. Neuron, 46, 671-679.
3. Aston-Jones, G., Smith, R.J., Moorman, D.E. & Richardson, K.A. (2009) Role of lateral hypothalamic orexin neurons in reward processing and addiction. Neuropharmacology, 56, 112-121.
4. Avena, N.M., Rada, P. & Hoebel, B.G. (2008) Evidence for sugar addiction: behavioral and neurochemical effects of intermittent, excessive sugar intake. Neurosci. Biobehav. Rev., 32, 20-39.
5. Barnett, S.A. (1958) Experiments on 'neophobia' in wild and laboratory rats. Br. J. Psychol., 49, 195-201.
6. Baumont, R. (1996) Palatability and feeding behaviour in ruminants - a review. Annales de zootechnie, 45, 385-400.
7. Bellisle, F. (1989) Quantifying palatability in humans. Ann. NY Acad. Sci., 575, 363-374.
8. Bernstein, I.L. (1985) Learned food aversions in the progression of cancer and its treatment. Ann. NY Acad. Sci., 443, 365-380.
9. Bernstein, I.L. (1994) Development of food aversions during illness. Proc. Nutr. Soc., 53, 131-137.
10. Boissy, A., Manteuffel, G., Jensen, M.B., Oppermann Moe, R., Spruijt, B., Keeling, L.J., Winckler, C., Forkman, B., Dimitrov, I., Langbein, J., Bakken, M., Veissier, I. & Aubert, A. (2007) Assessment of positive emotions in animals to improve their welfare. Physiol. Behav., 92, 375-397.
11. Boudry, G. & Perrier, C. (2008) Thyme and cinnamon extracts induce anion secretion in piglet small intestine via cholinergic pathways. J. Physiol. Pharmacol., 59, 543-552.
12. Bragulat, V., Dzemidzic, M., Bruno, C., Cox, C.A., Talavage, T., Considine, R.V. & Kareken, D.A. (2010) Food-related odor probes of brain reward circuits during hunger: a pilot FMRI study. Obesity (Silver Spring), 18, 1566-1571.
13. Bures, J., Bermudez-Rattoni, F. & Yamamoto, T. (1998) Conditioned Taste Aversion: Memory of a Special Kind. University Press, Oxford.
14. Burritt, E.A. & Provenza, F.D. (1990) Food aversion learning in sheep: persistence of conditioned taste aversions to palatable shrubs (Cercocarpus montanus and Amelanchier alnifolia). J. Anim. Sci., 68, 1003-1007.
15. Burritt, E.A. & Provenza, F.D. (1992) Lambs form preferences for nonnutritive flavors paired with glucose. J. Anim. Sci., 70, 1133-1136.
16. Capaldi, E.D. (1999) Conditioned food preferences. In Medin, D. (Ed), The Psychology of Learning and Motivation. Academic Press, NY, pp. 1-33.
17. Carlezon, W.A.J. & Thomas, M.J. (2009) Biological substrates of reward and aversion: a nucleus accumbens activity hypothesis. Neuropharmacology, 56, 122-132.
18. Clouard, C., Meunier-Salaün, M.C. & Val-Laillet, D. (2011) Food preferences and aversions in human health and nutrition: how can pigs help the biomedical research? Animal, in press.
19. Cocores, J.A. & Gold, M.S. (2009) The salted food addiction hypothesis may explain overeating and the obesity epidemic. Med. Hypotheses, 73, 892-899.
20. Corey, D.T. (1978) The determinants of exploration and neophobia. Neurosci. Biobehav. Rev., 2, 235-253.
21. Danilova, V., Danilov, Y., Roberts, T., Elmer, D. & Hellekant, G. (2002) Electrophysiological recordings of mammalian taste nerves. In Simon, S.A. & Nicolelis, M.A.L. (Eds), Methods in Chemosensory Research. CRC Press, Boca Raton, London, NY, Washington DC, pp. 239-364.
22. Dovey, T.M., Staples, P.A., Gibson, E.L. & Halford, J.C. (2008) Food neophobia and 'picky/fussy' eating in children: a review. Appetite, 50, 181-193.
23. Drewnowski, A., Pierce, B. & Halmi, K.A. (1988) Fat aversion in eating disorders. Appetite, 10, 119-131.
24. Ettle, T. & Roth, F.X. (2004) Specific dietary selection for tryptophan by the piglet. J. Anim. Sci., 82, 1115-1121.
25. Felix, B., Leger, M.E., Albe-Fessard, D., Marcilloux, J.C., Rampin, O. & Laplace, J.P. (1999) Stereotaxic atlas of the pig brain. Brain Res. Bull., 49, 1-137.
26. Ferreira, G., Miranda, M.I., De la Cruz, V., Rodriguez-Ortiz, C.J. & Bermudez-Rattoni, F. (2005) Basolateral amygdala glutamatergic activation enhances taste aversion through NMDA receptor activation in the insular cortex. Eur. J. Neurosci., 22, 2596-2604.
27. Ferreira, G., Ferry, B., Meurisse, M. & Levy, F. (2006) Forebrain structures specifically activated by conditioned taste aversion. Behav. Neurosci., 120, 952-962.
28. Fishbein, M., Cox, S., Swenny, C., Mogren, C., Walbert, L. & Fraker, C. (2006) Food chaining: a systematic approach for the treatment of children with feeding aversion. Nutr. Clin. Pract., 21, 182-184.
29. Fontanini, A., Grossman, S.E., Figueroa, J.A. & Katz, D.B. (2009) Distinct subtypes of basolateral amygdala taste neurons reflect palatability and reward. J. Neurosci., 29, 2486-2495.
30. Gilbert, P.E., Campbell, A. & Kesner, R.P. (2003) The role of the amygdala in conditioned flavor preference. Neurobiol. Learn. Mem., 79, 118-121.
31. Gold, B.D., Bhoopalam, P.S., Reifen, R.M., Harvey, E. & Marcon, M.A. (1992) Gastrointestinal complications of gastrocystoplasty. Arch. Dis. Child., 67, 1272-1276.
32. Gottfried, J.A. (2007) What can an orbitofrontal cortex-endowed animal do with smells? Ann. NY Acad. Sci., 121, 102-120.
33. Grabenhorst, F., Rolls, E.T., Parris, B.A. & d'Souza, A.A. (2009) How the brain represents the reward value of fat in the mouth. Cereb. Cortex, 20, 1082-1091.
34. Haber, S.N. & Knutson, B. (2010) The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology, 35, 4-26.
35. Hassani, O.K., Cromwell, H.C. & Schultz, W. (2001) Influence of expectation of different rewards on behavior-related neuronal activity in the striatum. J. Neurophysiol., 85, 2477-2489.
36. Hellekant, G., Danilova, V. & Ninomiya, Y. (1997) Primate sense of taste: behavioral and single chorda tympani and glossopharyngeal nerve fiber recordings in the Rhesus monkey, Macaca mulatta. J. Neurophysiol., 77, 978-993.
37. Houpt, K.A., Zahorik, D.M., Anika, S.M. & Houpt, T.R. (1979) Taste aversion learning in suckling and weanling pigs. Vet. Res. Commun., 3, 165-169.
38. Ishii, Y., Blundell, J.E., Halford, J.C. & Rodgers, R.J. (2003) Palatability, food intake and the behavioural satiety sequence in male rats. Physiol. Behav., 80, 37-47.
39. Ito, R., Robbins, T.W., Pennartz, C.M. & Everitt, B.J. (2008) Functional interaction between the hippocampus and nucleus accumbens shell is necessary for the acquisition of appetitive spatial context conditioning. J. Neurosci., 28, 6950-6959.
40. Jacobsen, P.B., Bovbjerg, D.H., Schwartz, M.D., Andrykowski, M.A., Futterman, A.D., Gilewski, T., Norton, L. & Redd, W.H. (1993) Formation of food aversions in cancer patients receiving repeated infusions of chemotherapy. Behav. Res. Ther., 31, 739-748.
41. Kobayashi, M., Sasabe, T., Takeda, M., Kondo, Y., Yoshikubo, S., Imamura, K., Onoe, H., Sawada, T. & Watanabe, Y. (2002) Functional anatomy of chemical senses in the alert monkey revealed by positron emission tomography. Eur. J. Neurosci., 16, 975-980.
42. Kober, H., Mende-Siedlecki, P., Kross, E.F., Weber, J., Mischel, W., Hart, C.L. & Ochsner, K.N. (2010) Prefrontal-striatal pathway underlies cognitive regulation of craving. Proc. Natl. Acad. Sci. USA, 107, 14811-14816.
43. Kompus, K., Hugdahl, K., Ohman, A., Marklund, P. & Nyberg, L. (2009) Distinct control networks for cognition and emotion in the prefrontal cortex. Neurosci. Lett., 467, 76-80.
44. Kondoh, T., Yamada, S., Shioda, S. & Torii, K. (2005) Central olfactory pathway in response to olfactory stimulation in rats detected by magnetic resonance imaging. Chem. Senses, 30, i172-i173.
45. Langendijk, P., Bolhuis, J.E. & Laurenssen, B.F.A. (2007) Effects of pre- and postnatal exposure to garlic and aniseed flavour on pre- and postweaning feed intake in pigs. Livestock Sci., 108, 284-287.
46. Lewis, N.J. (1999) Frustration of goal-directed behaviour in swine. Appl. Anim. Behav. Sci., 64, 19-29.
47. Lind, N.M., Moustgaard, A., Jelsing, J., Vajta, G., Cumming, P. & Hansen, A.K. (2007) The use of pigs in neuroscience: modeling brain disorders. Neurosci. Biobehav. Rev., 31, 728-751.
48. Marcontell, D.K., Laster, A.E. & Johnson, J. (2003) 17) Cognitive-behavioral treatment of food neophobia in adults. J. Anxiety Disord., 17, 243-251.
49. Martin, C., Grenier, D., Thévenet, M., Vigouroux, M., Bertrand, B., Janier, M., Ravel, N. & Litaudon, P. (2007) fMRI visualization of transient activations in the rat olfactory bulb using short odor stimulations. Neuroimage, 36, 1288-1293.
50. McAlonan, K., Brown, V.J. & Bowman, E.M. (2000) Thalamic reticular nucleus activation reflects attentional gating during classical conditioning. J. Neurosci., 20, 8897-8901.
51. Meunier-Salaün, M.C. & Picard, M. (1996) Les facteurs de choix alimentaires chez les porcs et les volailles. INRA Prod. Anim., 9, 339-348.
52. Meunier-Salaün, M.C., Gaultier, A., Malbert, C.H. & Val-Laillet, D. (2010) What are the prerequisites for the establishment of a pig model to investigate the mechanisms of conditioned food aversion in humans? EAAP Annual Meeting 2010. Wageningen Academic Publishers, Heraklion, Crete Island, Greece, pp. 359.
53. Navarro, M. & Cubero, I. (2003) Lateral parabrachial lesions impair lithium chloride-induced aversive responses but not saccharin-induced flavor preference. Brain Res. Bull., 990, 195-202.
54. Ono, T., Nishino, H., Fukuda, M., Sasaki, K. & Nishijo, H. (1984) Single neuron activity in dorsolateral prefrontal cortex of monkey during operant behavior sustained by food reward. Brain Res. Bull., 311, 323-332.
55. Oostindjer, M., Bolhuis, J.E., van den Brand, H. & Kemp, B. (2009) Prenatal flavor exposure affects flavor recognition and stress-related behavior of piglets. Chem. Senses, 34, 775-787.
56. Pautler, R.G. & Koretsky, A.P. (2002) Tracing odor-induced activation in the olfactory bulbs of mice using manganese-enhanced magnetic resonance imaging. Neuroimage, 16, 441-448.
57. Pinault, D. (2004) The thalamic reticular nucleus: structure, function and concept. Brain Res. Rev., 46, 1-31.
58. Provenza, F.D., Lynch, J.J. & Cheney, C.D. (1995) Effects of a flavor and food restriction on the response of sheep to novel foods. Appl. Anim. Behav. Sci., 43, 83-93.
59. Reilly, S. & Trifunovic, R. (2000) Lateral parabrachial nucleus lesions in the rat: aversive and appetitive gustatory conditioning. Brain Res. Bull., 52, 269-278.
60. Reinhardt, I., Jansen, A., Kellermann, T., Schüppen, A., Kohn, N., Gerlach, A.L. & Kircher, T. (2010) Neural correlates of aversive conditioning: development of a functional imaging paradigm for the investigation of anxiety disorders. Eur. Arch. Psychiatry Clin. Neurosci., 260, 443-453.
61. Roesch, M.R. & Olson, C.R. (2007) Neuronal activity related to anticipated reward in frontal cortex: does it represent value or reflect motivation? Ann. NY Acad. Sci., 121, 431-446.
62. Rolls, E.T. (2004) Smell, taste, texture, and temperature multimodal representations in the brain, and their relevance to the control of appetite. Nutr. Rev., 62, S193-S204.
63. Rolls, E.T. (2005) Taste, olfactory, and food texture processing in the brain, and the control of food intake. Physiol. Behav., 85, 45-56.
64. Rolls, E.T. (2008) Functions of the orbitofrontal and pregenual cingulate cortex in taste, olfaction, appetite and emotion. Acta Physiol. Hung., 95, 131-164.
65. Rolls, E.T., Kringelbach, M.L. & de Araujo, I.E. (2003) Different representations of pleasant and unpleasant odours in the human brain. Eur. J. Neurosci., 18, 695-703.
66. Roman, C., Lin, J.Y. & Reilly, S. (2009) Conditioned taste aversion and latent inhibition following extensive taste preexposure in rats with insular cortex lesions. Brain Res. Bull., 1259, 68-73.
67. Saikali, S., Meurice, P., Sauleau, P., Eliat, P.A., Bellaud, P., Randuineau, G., Vérin, M. & Malbert, C.H. (2010) A three-dimensional digital segmented and deformable brain atlas of the domestic pig. J. Neurosci. Methods, 192, 102-109.
68. Saint-Dizier, H., Lévy, F. & Ferreira, G. (2007) Influence of the mother in the development of flavored-food preference in lambs. Dev. Psychobiol., 49, 98-106.
69. Sauleau, P., Lapouble, E., Val-Laillet, D. & Malbert, C.H. (2009) The pig model in brain imaging and neurosurgery. Animal, 3, 1138-1151.
70. Sclafani, A. (1999) Macronutrient-conditioned flavor preferences. In: Berthoud, H.R. & Seeley, R.J. (Eds), Neural Control of Macronutrient Selection. CRC Press, Boca Raton, FL, pp. 93-106.
71. Sclafani, A., Azzara, A.V., Touzani, K., Grigson, P.S. & Norgren, R. (2001) Parabrachial nucleus lesions block taste and attenuate flavor preference and aversion conditioning in rats. Behav. Neurosci., 115, 920-933.
72. Simons, J.S., Owen, A.M., Fletcher, P.C. & Burgess, P.W. (2005) Anterior prefrontal cortex and the recollection of contextual information. Neuropsychologia, 43, 1774-1783.
73. Small, D.M. & Prescott, J. (2005) Odor/taste integration and the perception of flavor. Exp. Brain Res., 166, 345-357.
74. Smith, D.M., Freeman, J.H.J., Nicholson, D. & Gabriel, M. (2002) Limbic thalamic lesions, appetitively motivated discrimination learning, and training-induced neuronal activity in rabbits. J. Neurosci., 22, 8212-8221.
75. Spurlock, M.E. & Gabler, N.K. (2008) The development of porcine models of obesity and the metabolic syndrome. J. Nutr., 138, 397-402.
76. St-Arnaud-McKenzie, D., Paquet, C., Kergoat, M.J., Ferland, G. & Dubé, L. (2004) Hunger and aversion: drives that influence food intake of hospitalized geriatric patients. J. Gerontol. A Biol. Sci. Med. Sci., 59, 1304-1309.
77. Taber, K.H., Wen, C., Khan, A. & Hurley, R.A. (2004) The limbic thalamus. J. Neuropsychiatry Clin. Neurosci., 16, 127-132.
78. Touzani, K. & Sclafani, A. (2001) Conditioned flavor preference and aversion: role of the lateral hypothalamus. Behav. Neurosci., 115, 84-93.
79. Touzani, K. & Sclafani, A. (2002) Lateral hypothalamic lesions impair flavour-nutrient and flavour-toxin trace learning in rats. Eur. J. Neurosci., 16, 2425-2433.
80. Tracy, A.L. & Davidson, T.L. (2006) Comparison of nutritive and nonnutritive stimuli in intestinal and oral conditioned taste aversion paradigms. Behav. Neurosci., 120, 1268-1278.
81. Tracy, A.L., Jarrard, L.E. & Davidson, T.L. (2001) The hippocampus and motivation revisited: appetite and activity. Behav. Brain Res., 127, 13-23.
82. Val-Laillet, D., Layec, S., Guérin, S., Meurice, P. & Malbert, C.H. (2011) Changes in brain activity after a diet-induced obesity. Obesity (Silver Spring), 19, 749-756.
83. Van Binsbergen, C.J., Hulshof, K.F., Wedel, M., Odink, J. & Coelingh Bennink, H.J. (1988) Food preferences and aversions and dietary pattern in anorexia nervosa patients. Eur. J. Clin. Nutr., 42, 671-678.
84. Vodicka, P., Smetana, K. Jr, Dvorankova, B., Emerick, T., Xu, Y.Z., Ourednik, J., Ourednik, V. & Motlik, J. (2005) The miniature pig as an animal model in biomedical research. Ann. NY Acad. Sci., 1049, 161-171.
85. van de Weerd, H.A. & Day, J.E.L. (2009) A review of environmental enrichment for pigs housed in intensive housing systems. Appl. Anim. Behav. Sci., 116, 1-20.
86. Winston, J.S., Gottfried, J.A., Kilner, J.M. & Dolan, R.J. (2005) Integrated neural representations of odor intensity and affective valence in human amygdala. J. Neurosci., 25, 8903-8907.
87. Wong, R. & McBride, C.B. (1993) Flavour neophobia in gerbils (Meriones unguiculatus) and hamsters (Mesocricetus auratus). Q. J. Exp. Psychol. B, 46, 129-143.
88. Woolley, J.D., Lee, B.S., Taha, S.A. & Fields, H.L. (2007) Nucleus accumbens opioid signaling conditions short-term flavor preferences. Neuroscience, 146, 19-30.
89. Xu, F., Kida, I., Hyder, F. & Shulman, R.G. (2000) Assessment and discrimination of odor stimuli in rat olfactory bulb by dynamic functional MRI. Proc. Natl. Acad. Sci. USA, 97, 10601-10606.
90. Xu, F., Schaefer, M., Kida, I., Schafer, J., Liu, N., Rothman, D.L., Hyder, F., Restrepo, D. & Shepherd, G.M. (2005) Simultaneous activation of mouse main and accessory olfactory bulbs by odors or pheromones. J. Comp. Neurol, 489, 491-500.
91. Yamamoto, T. (2008a) Central mechanisms of roles of taste in reward and eating. Acta Physiol. Hung., 95, 165-186.
92. Yamamoto, T. (2008b) Central mechanisms of taste: cognition, emotion and taste-elicited behaviors. Jpn. Dent. Sci. Rev., 44, 91-99.
93. Young, E.J. & Williams, C.L. (2010) Valence dependent asymmetric release of norepinephrine in the basolateral amygdala. Behav. Neurosci., 124, 633-644.
94. Yuan, Q., Harley, C.W., McLean, J.H. & Knöpfel, T. (2002) Optical imaging of odor preference memory in the rat olfactory bulb. J. Neurophysiol., 87, 3156-3159.
95. Zahorik, D.M. & Houpt, K.A. (1981) Species differences in feeding strategies, food hazards, and the ability to learn food aversions. In Kamil, C. & Sargent, J.D. (Eds), Foraging Behavior. Garland, New York, pp. 289-310.
96. Zeinstra, G.G., Koelen, M.A., Kok, F.J. & de Graaf, C. (2009) Children's hard-wired aversion to pure vegetable tastes. A 'failed' flavour-nutrient learning study. Appetite, 52, 528-530.