Differentiable contributions of human amygdalar subregions in the computations underlying reward and avoidance learning

European Journal of Neuroscience

Volumn 34, Issue 1, 2011, Pages 134-145

  Prévost, Charlotte ^a,b   Mccabe, Jonathan A ^a   Jessup, Ryan K ^b   Bossaerts, Peter ^b   O'Doherty, John P ^a,b  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Basolateral complex; Centromedial complex; High resolution fMRI; Instrumental learning

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ARTICLE; AVOIDANCE BEHAVIOR; BASOLATERAL COMPLEX; BRAIN FUNCTION; BRAIN REGION; CENTROMEDIAL COMPLEX; CONTROLLED STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; INSTRUMENTAL CONDITIONING; MALE; MATHEMATICAL MODEL; NERVE CELL NETWORK; NORMAL HUMAN; PRIORITY JOURNAL; REWARD; SIGNAL PROCESSING; STATE DEPENDENT LEARNING;

ADULT; AMYGDALA; ANIMALS; AVOIDANCE LEARNING; BEHAVIOR; BRAIN MAPPING; COMPUTER SIMULATION; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; NERVE NET; NEUROPSYCHOLOGICAL TESTS; REWARD; YOUNG ADULT;

EID: 79955766151     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2011.07686.x     Document Type: Article

References (67)

1. Adolphs, R. (2008) Fear, faces, and the human amygdala. Curr. Opin. Neurobiol., 18, 166-172.
2. Amunts, K., Kedo, O., Kindler, M., Pieperhoff, P., Mohlberg, H., Shah, N.J., Habel, U., Schneider, F. & Zilles, K. (2005) Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: intersubject variability and probability maps. Anat. Embryol. (Berl), 210, 343-352.
3. Anderton, B.H. (1997) Changes in the ageing brain in health and disease. Philos. Trans. R. Soc. Lond. B. Biol. Sci., 352, 1781-1792.
4. Bechara, A., Damasio, H. & Damasio, A.R. (2003) Role of the amygdala in decision-making. Ann. NY Acad. Sci., 985, 356-369.
5. Belova, M.A., Paton, J.J., Morrison, S.E. & Salzman, C.D. (2007) Expectation modulates neural responses to pleasant and aversive stimuli in primate amygdala. Neuron, 55, 970-984.
6. Blair, H.T., Schafe, G.E., Bauer, E.P., Rodrigues, S.M. & LeDoux, J.E. (2001) Synaptic plasticity in the lateral amygdala: a cellular hypothesis of fear conditioning. Learn. Mem., 8, 229-242.
7. Buchel, C. & Dolan, R.J. (2000) Classical fear conditioning in functional neuroimaging. Curr. Opin. Neurobiol., 10, 219-223.
8. Buchel, C., Morris, J., Dolan, R.J. & Friston, K.J. (1998) Brain systems mediating aversive conditioning: an event-related fMRI study. Neuron, 20, 947-957.
9. 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.
10. 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. Rev., 26, 321-352.
11. Cohen, A., Sanborn, A. & Shiffrin, R. (2008) Model evaluation using grouped or individual data. Psychon. Bull. Rev., 15, 692.
12. Corbit, L.H. & Balleine, B.W. (2005) Double dissociation of basolateral and central amygdala lesions on the general and outcome-specific forms of pavlovian-instrumental transfer. J. Neurosci., 25, 962-970.
13. Davis, M. & Whalen, P.J. (2001) The amygdala: vigilance and emotion. Mol. Psychiatry, 6, 13-34.
14. Davis, F.C., Johnstone, T., Mazzulla, E.C., Oler, J.A. & Whalen, P.J. (2010) Regional response differences across the human amygdaloid complex during social conditioning. Cereb. Cortex, 20, 612-621.
15. Dayan, P., Kakade, S. & Montague, P.R. (2000) Learning and selective attention. Nat. Neurosci., 3 (Suppl), 1218-1223.
16. Delgado, M.R., Li, J., Schiller, D. & Phelps, E.A. (2008) The role of the striatum in aversive learning and aversive prediction errors. Philos. Trans. R. Soc. Lond. B. Biol. Sci., 363, 3787-3800.
17. Elliott, R., Newman, J.L., Longe, O.A. & William Deakin, J.F. (2004) Instrumental responding for rewards is associated with enhanced neuronal response in subcortical reward systems. Neuroimage, 21, 984-990.
18. Erev, I. & Roth, A. (1998) Predicting how people play games: reinforcement learning in experimental games with unique, mixed strategy equilibria. Am. Econ. Rev., 88, 848-881.
19. Everitt, B.J., Parkinson, J.A., Olmstead, M.C., Arroyo, M., Robledo, P. & Robbins, T.W. (1999) Associative processes in addiction and reward. The role of amygdala-ventral striatal subsystems. Ann. NY Acad. Sci., 877, 412-438.
20. Fudenberg, D. & Levine, D. (1998) Learning in games. Eur. Econ. Rev., 42, 631-639.
21. Fudge, J.L., Kunishio, K., Walsh, P., Richard, C. & Haber, S.N. (2002) Amygdaloid projections to ventromedial striatal subterritories in the primate. Neuroscience, 110, 257-275.
22. Gallagher, M., Graham, P.W. & Holland, P.C. (1990) The amygdala central nucleus and appetitive Pavlovian conditioning: lesions impair one class of conditioned behavior. J. Neurosci., 10, 1906-1911.
23. Glascher, J., Hampton, A.N. & O'Doherty, J.P. (2009) Determining a role for ventromedial prefrontal cortex in encoding action-based value signals during reward-related decision making. Cereb. Cortex, 19, 483-495.
24. Glover, G.H., Li, T.Q. & Ress, D. (2000) Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magn. Reson. Med., 44, 162-167.
25. Gluck, M.A. & Bower, G.H. (1988) From conditioning to category learning: an adaptive network model. J. Exp. Psychol. Gen., 117, 227-247.
26. Haber, S.N. & Knutson, B. (2010) The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology, 35, 4-26.
27. Hampton, A.N., Adolphs, R., Tyszka, M.J. & O'Doherty, J.P. (2007) Contributions of the amygdala to reward expectancy and choice signals in human prefrontal cortex. Neuron, 55, 545-555.
28. Holland, P.C. & Gallagher, M. (2003) Double dissociation of the effects of lesions of basolateral and central amygdala on conditioned stimulus-potentiated feeding and Pavlovian-instrumental transfer. Eur. J. Neurosci., 17, 1680-1694.
29. Holland, P.C., Petrovich, G.D. & Gallagher, M. (2002) The effects of amygdala lesions on conditioned stimulus-potentiated eating in rats. Physiol. Behav., 76, 117-129.
30. Hsu, M., Bhatt, M., Adolphs, R., Tranel, D. & Camerer, C.F. (2005) Neural systems responding to degrees of uncertainty in human decision-making. Science, 310, 1680-1683.
31. Insausti, R., Juottonen, K., Soininen, H., Insausti, A.M., Partanen, K., Vainio, P., Laakso, M.P. & Pitkanen, A. (1998) MR volumetric analysis of the human entorhinal, perirhinal, and temporopolar cortices. AJNR Am. J. Neuroradiol., 19, 659-671.
32. Killcross, S., Robbins, T.W. & Everitt, B.J. (1997) Different types of fear-conditioned behaviour mediated by separate nuclei within amygdala. Nature, 388, 377-380.
33. Kim, H., Shimojo, S. & O'Doherty, J.P. (2006) Is avoiding an aversive outcome rewarding? Neural substrates of avoidance learning in the human brain PLoS Biol., 4, e233.
34. LaBar, K.S., Gatenby, J.C., Gore, J.C., LeDoux, J.E. & Phelps, E.A. (1998) Human amygdala activation during conditioned fear acquisition and extinction: a mixed-trial fMRI study. Neuron, 20, 937-945.
35. LeDoux, J. (2003) The emotional brain, fear, and the amygdala. Cell. Mol. Neurobiol., 23, 727-738.
36. LeDoux, J. (2007) The amygdala. Curr. Biol., 17, R868-R874.
37. Luce, R.D. (1959) On the possible psychophysical laws. Psychol. Rev., 66, 81-95.
38. Mai, J.K., Paxinos, G. & Voss, T. (2008) Atlas of the Human Brain. Elsevier, Amsterdam.
39. McClure, S.M., Berns, G.S. & Montague, P.R. (2003) Temporal prediction errors in a passive learning task activate human striatum. Neuron, 38, 339-346.
40. Miller, M.I., Beg, M.F., Ceritoglu, C. & Stark, C. (2005) Increasing the power of functional maps of the medial temporal lobe by using large deformation diffeomorphic metric mapping. Proc. Natl Acad. Sci. USA, 102, 9685-9690.
41. Mobbs, D., Petrovic, P., Marchant, J.L., Hassabis, D., Weiskopf, N., Seymour, B., Dolan, R.J. & Frith, C.D. (2007) When fear is near: threat imminence elicits prefrontal-periaqueductal gray shifts in humans. Science, 317, 1079-1083.
42. Myung, I.J. (2003) Tutorial on maximum likelihood estimation. J. Math. Psychol., 47, 90-100.
43. Myung, I. & Busemeyer, J. (1992) Measurement-free tests of a general state-space model of prototype learning. J. Math. Psychol., 36, 32-67.
44. Nelder, J. & Mead, R. (1965) A simplex method for function minimization. Comput. J., 7, 308.
45. O'Doherty, J.P., Dayan, P., Friston, K., Critchley, H. & Dolan, R.J. (2003) Temporal difference models and reward-related learning in the human brain. Neuron, 38, 329-337.
46. Paton, J.J., Belova, M.A., Morrison, S.E. & Salzman, C.D. (2006) The primate amygdala represents the positive and negative value of visual stimuli during learning. Nature, 439, 865-870.
47. Pearce, J.M. & Hall, G. (1980) A model for Pavlovian learning: variations in the effectiveness of conditioned but not of unconditioned stimuli. Psychol. Rev., 87, 532-552.
48. Petrovich, G.D., Ross, C.A., Mody, P., Holland, P.C. & Gallagher, M. (2009) Central, but not basolateral, amygdala is critical for control of feeding by aversive learned cues. J. Neurosci., 29, 15205-15212.
49. Phelps, E.A. (2006) Emotion and cognition: insights from studies of the human amygdala. Annu. Rev. Psychol., 57, 27-53.
50. Price, J.L. (2003) Comparative aspects of amygdala connectivity. Ann. NY Acad. Sci., 985, 50-58.
51. Price, J.L. & Amaral, D.G. (1981) An autoradiographic study of the projections of the central nucleus of the monkey amygdala. J. Neurosci., 1, 1242-1259.
52. Rescorla, R.A. & Wagner, A.R. (1972) A theory of Pavlovian conditioning: variations in effectiveness of reinforcement and nonreinforcement. In A.H., Black & W.F., Prokasy (Eds), Classical Conditioning II: Current Research and Theory. Appleton Century-Crofts, New York, pp. 64-99.
53. Roesch, M.R., Calu, D.J., Esber, G.R. & Schoenbaum, G. (2010) Neural correlates of variations in event processing during learning in basolateral amygdala. J. Neurosci., 30, 2464-2471.
54. Russchen, F.T., Bakst, I., Amaral, D.G. & Price, J.L. (1985) The amygdalostriatal projections in the monkey. An anterograde tracing study. Brain Res., 329, 241-257.
55. Schiller, D., Levy, I., Niv, Y., LeDoux, J.E. & Phelps, E.A. (2008) From fear to safety and back: reversal of fear in the human brain. J. Neurosci., 28, 11517-11525.
56. Schoenbaum, G., Chiba, A.A. & Gallagher, M. (1998) Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning. Nat. Neurosci., 1, 155-159.
57. Schultz, W. (2002) Getting formal with dopamine and reward. Neuron, 36, 241-263.
58. Schwarz, G. (1978) Estimating the dimension of a model. Ann. Stat., 6, 461-464.
59. Seymour, B. & Dolan, R. (2008) Emotion, decision making, and the amygdala. Neuron, 58, 662-671.
60. Seymour, B., O'Doherty, J.P., Koltzenburg, M., Wiech, K., Frackowiak, R., Friston, K. & Dolan, R. (2005) Opponent appetitive-aversive neural processes underlie predictive learning of pain relief. Nat. Neurosci., 8, 1234-1240.
61. Shabel, S.J. & Janak, P.H. (2009) Substantial similarity in amygdala neuronal activity during conditioned appetitive and aversive emotional arousal. Proc. Natl Acad. Sci. USA, 106, 15031-15036.
62. Solano-Castiella, E., Anwander, A., Lohmann, G., Weiss, M., Docherty, C., Geyer, S., Reimer, E., Friederici, A.D. & Turner, R. (2010) Diffusion tensor imaging segments the human amygdala in vivo. Neuroimage, 49, 2958-2965.
63. Sutton, R. & Barto, A. (1998) Reinforcement Learning. MIT Press, Cambridge, MA.
64. Thirion, J.P. (1998) Image matching as a diffusion process: an analogy with Maxwell's demons. Med. Image Anal., 2, 243-260.
65. Vercauteren, T., Pennec, X., Perchant, A. & Ayache, N. (2007) Non-parametric diffeomorphic image registration with the demons algorithm. Med. Image Comput. Comput. Assist. Interv., 10, 319-326.
66. Yacubian, J., Glascher, J., Schroeder, K., Sommer, T., Braus, D.F. & Buchel, C. (2006) Dissociable systems for gain- and loss-related value predictions and errors of prediction in the human brain. J. Neurosci., 26, 9530-9537.
67. Yassa, M.A. & Stark, C.E. (2009) A quantitative evaluation of cross-participant registration techniques for MRI studies of the medial temporal lobe. Neuroimage, 44, 319-327.