Reward sensitivity modulates connectivity among reward brain areas during processing of anticipatory reward cues

European Journal of Neuroscience

Volumn 38, Issue 3, 2013, Pages 2399-2407

  Costumero, Victor ^a   Barrós Loscertales, Alfonso ^a   Bustamante, Juan C ^a   Ventura Campos, Noelia ^a   Fuentes, Paola ^a   Ávila, César ^a  

^a UNIVERSITAT JAUME I   (Spain)

Author keywords

Dopamine; fMRI; Nucleus accumbens; Orbitofrontal cortex; Personality

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ANTICIPATION; ARTICLE; ASSOCIATION; BEHAVIOR; BRAIN REGION; CONTROLLED STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; IMAGE PROCESSING; MALE; MESENCEPHALON; MOTIVATION; NORMAL HUMAN; NUCLEUS ACCUMBENS; ORBITAL CORTEX; PERSONALITY; PRIORITY JOURNAL; PSYCHOPHYSIOLOGY; PUNISHMENT; REACTION TIME; REWARD; TASK PERFORMANCE;

EID: 84881301608     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12234     Document Type: Article

References (70)

1. Arnett, P.A. & Newman, J.P. (2000) Gray's three-arousal model: an empirical investigation. Pers. Indiv. Differ., 28, 1171-1189.
2. Ashburner, J. & Friston, K.J. (1999) Nonlinear spatial normalization using basis functions. Hum. Brain Mapp., 7, 254-266.
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(Suppl 1), 112-121.
4. Ávila, C. (2001) Distinguishing BIS-mediated and BAS-mediated disinhibition mechanisms: a comparison of disinhibition models of Gray and Patterson and Newman. J. Pers. Soc. Psychol., 80, 311-324.
5. Ávila, C. & Parcet, M.A. (1997) Impulsivity and anxiety differences in cognitive inhibition. Pers. Indiv. Differ., 23, 1055-1064.
6. Ávila, C. & Parcet, M.A. (2001) Personality and inhibition deficits in the stop-signal task: a mediating role of Gray's anxiety and impulsivity. Pers. Indiv. Differ., 29, 975-986.
7. Ávila, C. & Parcet, M.A. (2002) Individual differences in reward sensitivity and attentional focus. Pers. Indiv. Differ., 33, 979-996.
8. Ávila, C. & Torrubia, R. (2008) Performance and conditioning studies. In Corr, P. (Ed.), Reinforcement Sensitivity Theory of Personality. Cambridge University Press, London, pp. 228-260.
9. Ávila, C., Barrós-Loscertales, A., Ortet, G., Parcet, M.A. & Ibañez, M.I. (2003) Set-shifting and sensitivity to reward: a dopamine mechanism for explaining disinhibitory disorders. Cognition Emotion, 17, 951-959.
10. Ávila, C., Parcet, M.A. & Barrós-Loscertales, A. (2008) A cognitive neuroscience approach to individual differences in sensitivity to reward. Neurotox. Res., 14, 191-203.
11. Barrós-Loscertales, A., Meseguer, V., Sanjuán, A., Belloch, V., Parcet, M.A., Torrubia, R. & Avila, C. (2006) Striatum gray matter reduction in males with an overactive behavioral activation system. Eur. J. Neurosci., 24, 2071-2074.
12. Barrós-Loscertales, A., Ventura-Campos, N., Sanjuán-Tomás, A., Belloch, V., Parcet, M.A. & Avila, C. (2010) Behavioral activation system modulation on brain activation during appetitive and aversive stimulus processing. Soc. Cogn. Affect. Neur., 5, 18-28.
13. Beaver, J.D., Lawrence, A.D., van Ditzhuijzen, J., Davis, M.H., Woods, A. & Calder, A.J. (2006) Individual differences in reward drive predict neural responses to images of food. J. Neurosci., 26, 5160-5166.
14. Bechara, A., Damasio, H., Damasio, A.R. & Lee, G.P. (1999) Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making. J. Neurosci., 19, 5473-5481.
15. Bechara, A., Damasio, H. & Damasio, A.R. (2000) Emotion, decision making and the orbitofrontal cortex. Cereb. Cortex, 10, 295-307.
16. Berridge, K.C. & Robinson, T.E. (1998) What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res. Rev., 28, 309-369.
17. Bijttebier, P., Beck, I., Claes, L. & Vandereycken, W. (2009) Gray's Reinforcement Sensitivity Theory as a framework for research on personality-psychopathology associations. Clin. Psychol. Rev., 29, 421-430.
18. Cámara, E., Rodríguez-Fornells, A. & Münte, T.F. (2010) Microstructural brain differences predict functional hemodynamic responses in a reward processing task. J. Neurosci., 30, 11398-11402.
19. Cardinal, R.N., Parkinson, J.A., Hall, J. & Everitt, B.J. (2002) Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci. Biobehav. R., 26, 321-352.
20. Carter, R., MacInnes, J., Huettel, S. & Adcock, R. (2009) Activation in the VTA and nucleus accumbens increases in anticipation of both gains and losses. Front. Behav. Neurosci., 3, 21.
21. Cohen, M.X., Schoene-Bake, J.C., Elger, C.E. & Weber, B. (2009) Connectivity-based segregation of the human striatum predicts personality characteristics. Nat. Neurosci., 12, 32-34.
22. Cools, R., Clarck, L., Owen, A.M. & Robbins, T. (2002) Defining the neural mechanisms of probabilistic reversal learning using event-related functional magnetic resonance imaging. J. Neurosci., 22, 4563-4567.
23. Cooper, J.C., Hollon, N.G., Wimmer, G.E. & Knutson, B. (2009) Available alternative incentives modulate anticipatory nucleus accumbens activation. Soc. Cogn. Affect. Neur., 4, 409-416.
24. Corr, P.J. (2004) Reinforcement sensitivity theory and personality. Neurosci. Biobehav. R., 28, 317-332.
25. Cremers, H.R., Demenescu, L.R., Aleman, A., Renken, R., van Tol, M.J., van der Wee, N.A.J., Veltman, D.J. & Roelofs, K. (2010) Neuroticism modulates amygdala-prefrontal connectivity in response to negative emotional facial expressions. NeuroImage, 49, 963-970.
26. De Martino, B., Camerer, C.F. & Adolphs, R. (2010) Amygdala damage eliminates monetary loss aversion. Proc. Natl. Acad. Sci. USA, 107, 3788-3792.
27. Depue, R.A. & Collins, P.F. (1999) Neurobiology of the structure of personality: dopamine, facilitation of incentive motivation, and extraversion. Behav. Brain Sci., 22, 491-517.
28. Düzel, E., Bunzeck, N., Guitart-Masip, M., Wittmann, B., Schott, B.H. & Tobler, P.N. (2009) Functional imaging of the human dopaminergic midbrain. Trends Neurosci., 32, 321-328.
29. Everitt, B.J., Cador, M. & Robbins, T.W. (1989) Interactions between the amygdala and ventral striatum in stimulus-reward associations: studies using a second-order schedule of sexual reinforcement. Neuroscience, 30, 63-75.
30. Friedman, D.P., Aggleton, J.P. & Saunders, R.C. (2002) Comparison of hippocampal, amygdala, and perirhinal projections to the nucleus accumbens: combined anterograde and retrograde tracing study in the Macaque brain. J. Comp. Neurol., 450, 345-365.
31. Friston, K.J., Holmes, A.P., Worsley, K.J., Poline, J.P., Frith, C.D. & Frackowiak, R.S.J. (1995) Statistical parametric maps in functional imaging: a general linear approach. Hum. Brain Mapp., 2, 189-210.
32. Friston, K.J., Buechel, C., Fink, G.R., Morris, J., Rolls, E. & Dolan, R.J. (1997) Psychophysiological and modulatory interactions in neuroimaging. NeuroImage, 6, 218-229.
33. Fudge, J.L., Kunishio, K., Walsh, C., Richard, D. & Haber, S.N. (2002) Amygdaloid projections to ventromedial striatal subterritories in the primate. Neuroscience, 110, 257-275.
34. Gitelman, D.R., Penny, W.D., Ashburner, J. & Friston, K.J. (2003) Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution. NeuroImage, 19, 200-207.
35. Gottfried, J.A., O'Doherty, J. & Dolan, R.J. (2003) Encoding predictive reward value in human amygdala and orbitofrontal cortex. Science, 301, 1104-1107.
36. Gray, J.A. (1981) A critique of Eysenck's theory of personality. In Eysenck, H.J. (Ed.), A Model for Personality. Springer, Berlin, pp. 246-276.
37. Gray, J.A. (1991) Neural systems, emotion, and personality. In Madden, J. (Ed.), Neurobiology of Learning, Emotion, and Affect. Raven Press, New York, NY, pp. 273-306.
38. Guitart-Masip, M., Fuentemilla, L., Bach, D.R., Huys, Q.J., Dayan, P., Dolan, R.J. & Duzel, E. (2011) Action dominates valence in anticipatory representations in the human striatum and dopaminergic midbrain. J. Neurosci., 31, 7867-7875.
39. Haas, B.W., Omura, K., Amin, Z., Constable, R.T. & Canli, T. (2006) Functional connectivity with the anterior cingulate is associated with extraversion during the emotional Stroop task. Soc. Neurosci., 1, 16-24.
40. Haber, S.N. & Knutson, B. (2010) The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacol., 35, 4-26.
41. Hahn, T., Dresler, T., Ehlis, A.C., Plichta, M.M., Heinzel, S., Polak, T., Lesch, K.P., Breuer, F., Jakob, P.M. & Fallgatter, A.J. (2009) Neural response to reward anticipation is modulated by Gray's impulsivity. NeuroImage, 46, 1148-1153.
42. Hahn, T., Dresler, T., Ehlis, A.C., Pyka, M., Saathoff, C., Jakob, P.M., Lesch, K.P. & Fallgatter, A.J. (2012) Randomness of resting-state brain oscillations encodes Gray's personality trait. NeuroImage, 59, 1842-1845.
43. Jensen, J., Smith, A.J., Willeit, M., Crawley, A.P., Mikulis, D.J., Vitcu, I. & Kapur, S. (2007) Separate brain regions code for salience vs. valence during reward prediction in humans. Hum. Brain Mapp., 28, 294-302.
44. Knutson, B., Adams, C.M., Fong, G.W. & Hommer, D. (2001) Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J. Neurosci., 21, RC159.
45. Knutson, B., Fong, G.W., Bennett, S.M., Adams, C.M. & Hommer, D. (2003) A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: characterization with rapid event-related FMRI. NeuroImage, 18, 263-272.
46. Knutson, B., Taylor, J., Kaufman, M., Peterson, R. & Glover, G. (2005) Distributed neural representation of expected value. J. Neurosci., 25, 4806-4812.
47. Krebs, R.M., Heipertz, D., Schuetze, H. & Duzel, E. (2011) Novelty increases the mesolimbic functional connectivity of the substantianigra/ventral tegmental area (SN/VTA) during reward anticipation: evidence from high-resolution fMRI. NeuroImage, 58, 647-655.
48. Lodge, D.J. (2011) The medial prefrontal and orbitofrontal cortices differentially regulate dopamine system function. Neuropsychopharmacol., 36, 1227-1236.
49. Luman, M., Van Meel, C.S., Oosterlaan, J. & Geurts, H.M. (2012) Reward and punishment sensitivity in children with ADHD: validating the Sensitivity to Punishment and Sensitivity to Reward Questionnaire for Children (SPSRQ-C). J. Abnorm. Child Psych., 40, 145-157.
50. Maldjian, J.A., Laurienti, P.J. & Burdette, J.H. (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage, 19, 1233-1239.
51. Morrison, S.E. & Salzman, C.D. (2010) Re-valuing the amygdala. Curr. Opin. Neurobiol., 20, 221-230.
52. Murray, E.A. (2007) The amygdala, reward and emotion. Trends Cogn. Sci., 11, 489-497.
53. Overton, P.G., Tong, Z.Y. & Clark, D. (1996) A pharmacological analysis of the burst events induced in midbrain dopaminergic neurons by electrical stimulation of the prefrontal cortex in the rat. J. Neural Transm., 103, 523-540.
54. Patterson, C.M. & Newman, J.P. (1993) Reflectivity and learning from aversive events: toward a psychological mechanism for the syndromes of disinhibition. Psychol. Rev., 100, 716-736.
55. Pauli, W.M., Hazy, T.E. & O'Reilly, R.C. (2012) Expectancy, ambiguity, and behavioral flexibility: separable and complementary roles of the orbital frontal cortex and amygdala in processing reward expectancies. J. Cognitive Neurosci., 24, 351-366.
56. Pickering, A.D. & Gray, J.A. (2001) Dopamine, appetitive reinforcement, and the neuropsychology of human learning: an individual differences approach. In Eliasz, A. & Angleitner, A. (Eds), Advances in Individual Differences Research. PABST Science Publishers, Lengerich, Germany, pp. 113-149.
57. Salomone, J.D., Cousins, M.S. & Snyder, B.J. (1997) Behavioral functions of nucleus accumbens dopamine: empirical and conceptual problems with the anhedonia hypothesis. Neurosci. Biobehav. R., 21, 341-359.
58. Sesack, S.R., Carr, D.B., Omelchenko, N. & Pinto, A. (2003) Anatomical substrates for glutamate-dopamine interactions: evidence for specificity of connections and extrasynaptic actions. Ann. NY Acad. Sci., 1003, 36-52.
59. Seymour, B. & Dolan, R. (2008) Emotion, decision making, and the amygdala. Neuron, 58, 662-671.
60. Smillie, L.D. & Jackson, C.J. (2005) The appetitive motivation scale and other BAS measures in the prediction of approach and active avoidance. Pers. Indiv. Differ., 39, 981-994.
61. Stuber, G.D., Sparta, D.R., Stamatakis, A.M., van Leeuwen, W.A., Hardjoprajitno, J.E., Cho, S., Tye, K.M., Kempadoo, K.A., Zhang, F., Deisseroth, K. & Bonci, A. (2011) Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking. Nature, 475, 377-380.
62. Takahashi, Y., Roesch, M.R., Stalnaker, T.A., Haney, R.Z., Calu, D.J., Taylor, A.R., Burke, K.A. & Schoenbaum, G. (2009) The orbitofrontal cortex and ventral tegmental area are necessary for learning from unexpected outcomes. Neuron, 62, 269-280.
63. Telzer, E.H., Masten, C.L., Berkman, E.T., Lieberman, M.D. & Fuligni, A.J. (2010) Gaining while giving: an fMRI study of the rewards of family assistance among white and Latino youth. Soc. Neurosci., 5, 508-518.
64. Tong, Z.Y., Overton, P.G. & Clark, D. (1996) Stimulation of the prefrontal cortex in the rat induces patterns of activity in midbrain dopaminergic neurons which resemble natural burst events. Synapse, 22, 195-208.
65. Tong, Z.Y., Overton, P.G., Martinez-Cué, C. & Clark, D. (1998) Do non-dopaminergic neurons in the ventral tegmental area play a role in the responses elicited in A10 dopaminergic neurons by electrical stimulation of the prefrontal cortex? Exp. Brain Res., 118, 466-476.
66. Torrubia, R., Avila, C., Molto, J. & Caseras, X. (2001) The Sensitivity to Punishment and Sensitivity to Reward Questionnaire (SPSRQ) as a measure of Gray's anxiety and impulsivity dimensions. Pers. Indiv. Differ., 31, 837-862.
67. Torrubia, R., Avila, C. & Caseras, X. (2008) Reinforcement sensitivity scales. In Corr, P.J. (Ed.), The Reinforcement Sensitivity Theory of Personality. Cambridge University Press, Cambridge, pp. 188-227.
68. Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., Mazoyer, B. & Joliot, M. (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage, 15, 273-289.
69. Weller, J.A., Levin, I.P., Shiv, B. & Bechara, A. (2007) Neural correlates of adaptive decision making for risky gains and losses. Psychol. Sci., 18, 958-964.
70. Winstanley, C.A., Theobald, D.E., Cardinal, R.N. & Robbins, T.W. (2004) Contrasting roles of basolateral amygdala and orbitofrontal cortex in impulsive choice. J. Neurosci., 24, 4718-4722.