Contribution of the amygdala, but not orbitofrontal or medial prefrontal cortices, to the expression of flavour preferences in marmoset monkeys

European Journal of Neuroscience

Volumn 34, Issue 6, 2011, Pages 1006-1017

  Agustín Pavón, Carmen ^a,b,c   Parkinson, John ^a,d   Man, Mei See ^a,b   Roberts, Angela C ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^d BANGOR UNIVERSITY   (United Kingdom)

Author keywords

Amygdala; Prefrontal cortex; Primate; Relative preference; Sweet tooth

Indexed keywords

CARBOHYDRATE; ESSENTIAL OIL; SUCROSE;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; BRAIN DAMAGE; CALLITRICHINAE; COMPUTER; CONTROLLED STUDY; FLAVOR; FOOD PREFERENCE; FRUIT JUICE; LEARNING; NONHUMAN; ORBITAL CORTEX; PARSIMONY ANALYSIS; PREFRONTAL CORTEX; PRIORITY JOURNAL; STIMULUS RESPONSE; SWEETNESS; TASTE PREFERENCE; TOUCH; TRAINING; VISUAL STIMULATION;

AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; BEVERAGES; CALLITHRIX; CARBOHYDRATES; CUES; DIETARY CARBOHYDRATES; FLAVORING AGENTS; FOOD PREFERENCES; FRONTAL LOBE; INJECTIONS; LEARNING; PHOTIC STIMULATION; PREFRONTAL CORTEX; TASTE;

EID: 80052966860     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2011.07813.x     Document Type: Article

References (54)

1. Aggleton, J.P. & Passingham, R.E. (1981) Syndrome produced by lesions of the amygdala in monkeys (Macaca mulatta). J. Comp. Physiol. Psychol., 95, 961-977.
2. Aggleton, J.P. & Passingham, R.E. (1982) An assessment of the reinforcing properties of foods after amygdaloid lesions in rhesus monkeys. J. Comp. Physiol. Psychol., 96, 71-77.
3. Arana, F.S., Parkinson, J.A., Hinton, E., Holland, A.J., Owen, A.M. & Roberts, A.C. (2003) Dissociable contributions of the human amygdala and orbitofrontal cortex to incentive motivation and goal selection. J. Neurosci., 23, 9632-9638.
4. Balleine, B.W. (2005) Neural bases of food-seeking: affect, arousal and reward in corticostriatolimbic circuits. Physiol. Behav., 86, 717-730.
5. Baxter, M.G., Parker, A., Lindner, C.C., Izquierdo, A.D. & Murray, E.A. (2000) Control of response selection by reinforcer value requires interaction of amygdala and orbital prefrontal cortex. J. Neurosci., 20, 4311-4319.
6. Baylis, L.L. & Gaffan, D. (1991) Amygdalectomy and ventromedial prefrontal ablation produce similar deficits in food choice and in simple object discrimination learning for an unseen reward. Exp. Brain Res., 86, 617-622.
7. Beauchamp, G.K. & Cowart, B.J. (1985) Congenital and experiential factors in the development of human flavor preferences. Appetite, 6, 357-372.
8. Burke, K.A., Franz, T.M., Miller, D.N. & Schoenbaum, G. (2007) Conditioned reinforcement can be mediated by either outcome-specific or general affective representations. Front. Integr. Neurosci., 1, 2.
9. Burke, K.A., Franz, T.M., Miller, D.N. & Schoenbaum, G. (2008) The role of the orbitofrontal cortex in the pursuit of happiness and more specific rewards. Nature, 454, 340-344.
10. Burman, K.J. & Rosa, M.G. (2009) Architectural subdivisions of medial and orbital frontal cortices in the marmoset monkey (Callithrix jacchus). J. Comp. Neurol., 514, 11-29.
11. Burns, L.H., Robbins, T.W. & Everitt, B.J. (1993) Differential effects of excitotoxic lesions of the basolateral amygdala, ventral subiculum and medial prefrontal cortex on responding with conditioned reinforcement and locomotor activity potentiated by intra-accumbens infusions of D-amphetamine. Behav. Brain Res., 55, 167-183.
12. Burns, L.H., Everitt, B.J. & Robbins, T.W. (1999) Effects of excitotoxic lesions of the basolateral amygdala on conditional discrimination learning with primary and conditioned reinforcement. Behav. Brain Res., 100, 123-133.
13. Butter, C.M., McDonald, J.A. & Snyder, D.R. (1969) Orality, preference behavior, and reinforcement value of nonfood object in monkeys with orbital frontal lesions. Science, 164, 1306-1307.
14. Cador, M., Robbins, T.W. & Everitt, B.J. (1989) Involvement of the amygdala in stimulus-reward associations: interaction with the ventral striatum. Neuroscience, 30, 77-86.
15. Cahill, L. & McGaugh, J.L. (1990) Amygdaloid complex lesions differentially affect retention of tasks using appetitive and aversive reinforcement. Behav. Neurosci., 104, 532-543.
16. Capaldi, E.D. (1992) Conditioned food preference. In Melin, D.L. (Ed.), The Psychology of Learning and Motivation. Advances in Research and Theory. Academic Press, New York, pp. 1-33.
17. Fellows, L.K. & Farah, M.J. (2007) The role of ventromedial prefrontal cortex in decision making: judgment under uncertainty or judgment per se? Cereb. Cortex, 17, 2669-2674.
18. Gilbert, P.E., Campbell, A. & Kesner, R.P. (2003) The role of the amygdala in conditioned flavor preference. Neurobiol. Learn. Mem., 79, 118-121.
19. Hatfield, T., Han, J.S., Conley, M., Gallagher, M. & Holland, P. (1996) Neurotoxic lesions of basolateral, but not central, amygdala interfere with Pavlovian second-order conditioning and reinforcer devaluation effects. J. Neurosci., 16, 5256-5265.
20. Howell, D.C. (1997) Statistical Methods for Psychology. Wadsworth Publishing Company, Belmont.
21. Ikeda, M., Brown, J., Holland, A.J., Fukuhara, R. & Hodges, J.R. (2002) Changes in appetite, food preference, and eating habits in frontotemporal dementia and Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry, 73, 371-376.
22. Izquierdo, A. & Murray, E.A. (2004) Combined unilateral lesions of the amygdala and orbital prefrontal cortex impair affective processing in rhesus monkeys. J. Neurophysiol., 91, 2023-2039.
23. Izquierdo, A. & Murray, E.A. (2005) Opposing effects of amygdala and orbital prefrontal cortex lesions on the extinction of instrumental responding in macaque monkeys. Eur. J. Neurosci., 22, 2341-2346.
24. Izquierdo, A. & Murray, E.A. (2007) Selective bilateral amygdala lesions in rhesus monkeys fail to disrupt object reversal learning. J. Neurosci., 27, 1054-1062.
25. Johnson, E.C. (2007) Rhesus macaques (Macaca mulatta) are not neophobic toward novel food with a high sugar content. Am. J. Primatol., 69, 591-596.
26. Kelley, A.E., Baldo, B.A., Pratt, W.E. & Will, M.J. (2005) Corticostriatal-hypothalamic circuitry and food motivation: integration of energy, action and reward. Physiol. Behav., 86, 773-795.
27. Keskitalo, K., Knaapila, A., Kallela, M., Palotie, A., Wessman, M., Sammalisto, S., Peltonen, L., Tuorila, H. & Perola, M. (2007) Sweet taste preferences are partly genetically determined: identification of a trait locus on chromosome 16. Am. J. Clin. Nutr., 86, 55-63.
28. Kobayakawa, K., Kobayakawa, R., Matsumoto, H., Oka, Y., Imai, T., Ikawa, M., Okabe, M., Ikeda, T., Itohara, S., Kikusui, T., Mori, K. & Sakano, H. (2007) Innate versus learned odour processing in the mouse olfactory bulb. Nature, 450, 503-508.
29. Lanuza, E., Novejarque, A., Martinez-Ricos, J., Martinez-Hernandez, J., Agustin-Pavon, C. & Martinez-Garcia, F. (2008) Sexual pheromones and the evolution of the reward system of the brain: the chemosensory function of the amygdala. Brain Res. Bull., 75, 460-466.
30. Machado, C.J. & Bachevalier, J. (2007a) The effects of selective amygdala, orbital frontal cortex or hippocampal formation lesions on reward assessment in nonhuman primates. Eur. J. Neurosci., 25, 2885-2904.
31. Machado, C.J. & Bachevalier, J. (2007b) Measuring reward assessment in a semi-naturalistic context: the effects of selective amygdala, orbital frontal or hippocampal lesions. Neuroscience, 148, 599-611.
32. Morris, J.S. & Dolan, R.J. (2001) Involvement of human amygdala and orbitofrontal cortex in hunger-enhanced memory for food stimuli. J. Neurosci., 21, 5304-5310.
33. Mullen, R.J., Buck, C.R. & Smith, A.M. (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development, 116, 201-211.
34. Murray, E.A., Gaffan, E.A. & Flint, R.W. Jr (1996) Anterior rhinal cortex and amygdala: dissociation of their contributions to memory and food preference in rhesus monkeys. Behav. Neurosci., 110, 30-42.
35. Parkinson, J.A., Crofts, H.S., McGuigan, M., Tomic, D.L., Everitt, B.J. & Roberts, A.C. (2001) The role of the primate amygdala in conditioned reinforcement. J. Neurosci., 21, 7770-7780.
36. Parkinson, J.A., Roberts, A.C., Everitt, B.J. & Di Ciano, P. (2005) Acquisition of instrumental conditioned reinforcement is resistant to the devaluation of the unconditioned stimulus. Q. J. Exp. Psychol. B, 58, 19-30.
37. Pears, A., Parkinson, J.A., Hopewell, L., Everitt, B.J. & Roberts, A.C. (2003) Lesions of the orbitofrontal but not medial prefrontal cortex disrupt conditioned reinforcement in primates. J. Neurosci., 23, 11189-11201.
38. Petrovich, G.D. & Gallagher, M. (2007) Control of food consumption by learned cues: a forebrain-hypothalamic network. Physiol. Behav., 91, 397-403.
39. Roberts, A.C. & Wallis, J.D. (2000) Inhibitory control and affective processing in the prefrontal cortex: neuropsychological studies in the common marmoset. Cereb. Cortex, 10, 252-262.
40. Roberts, A.C., Robbins, T.W., Everitt, B.J. & Muir, J.L. (1992) A specific form of cognitive rigidity following excitotoxic lesions of the basal forebrain in marmosets. Neuroscience, 47, 251-264.
41. Roberts, A.C., Tomic, D.L., Parkinson, C.H., Roeling, T.A., Cutter, D.J., Robbins, T.W. & Everitt, B.J. (2007) Forebrain connectivity of the prefrontal cortex in the marmoset monkey (Callithrix jacchus): an anterograde and retrograde tract-tracing study. J. Comp. Neurol., 502, 86-112.
42. Roesch, M.R. & Olson, C.R. (2004) Neuronal activity related to reward value and motivation in primate frontal cortex. Science, 304, 307-310.
43. Rudebeck, P.H. & Murray, E.A. (2008) Amygdala and orbitofrontal cortex lesions differentially influence choices during object reversal learning. J. Neurosci., 28, 8338-8343.
44. Rudebeck, P.H., Behrens, T.E., Kennerley, S.W., Baxter, M.G., Buckley, M.J., Walton, M.E. & Rushworth, M.F. (2008) Frontal cortex subregions play distinct roles in choices between actions and stimuli. J. Neurosci., 28, 13775-13785.
45. Sakai, N. & Yamamoto, T. (2001) Effects of excitotoxic brain lesions on taste-mediated odor learning in the rat. Neurobiol. Learn. Mem., 75, 128-139.
46. Schoenbaum, G., Setlow, B., Nugent, S.L., Saddoris, M.P. & Gallagher, M. (2003) Lesions of orbitofrontal cortex and basolateral amygdala complex disrupt acquisition of odor-guided discriminations and reversals. Learn Mem., 10, 129-140.
47. Schoenbaum, G., Roesch, M.R., Stalnaker, T.A. & Takahashi, Y.K. (2009) A new perspective on the role of the orbitofrontal cortex in adaptive behaviour. Nat. Rev. Neurosci., 10, 885-892.
48. 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.
49. Stoeckel, L.E., Weller, R.E., Cook, E.W. 3rd, Twieg, D.B., Knowlton, R.C. & Cox, J.E. (2008) Widespread reward-system activation in obese women in response to pictures of high-calorie foods. Neuroimage, 41, 636-647.
50. Swanson, L.W. & Petrovich, G.D. (1998) What is the amygdala? Trends Neurosci., 21, 323-331.
51. Touzani, K. & Sclafani, A. (2005) Critical role of amygdala in flavor but not taste preference learning in rats. Eur. J. Neurosci., 22, 1767-1774.
52. Ursin, H., Rosvold, H.E. & Vest, B. (1969) Food preference in brain lesioned monkeys. Physiol. Behav., 4, 609-612.
53. Watanabe, M., Cromwell, H.C., Tremblay, L., Hollerman, J.R., Hikosaka, K. & Schultz, W. (2001) Behavioral reactions reflecting differential reward expectations in monkeys. Exp. Brain Res., 140, 511-518.
54. Weiskrantz, L. (1956) Behavioral changes associated with ablation of the amygdaloid complex in monkeys. J. Comp. Physiol. Psychol., 49, 381-391.