Dissociable roles of medial orbitofrontal cortex in human operant extinction learning

NeuroImage

Volumn 43, Issue 4, 2008, Pages 748-755

  Finger, Elizabeth C ^a,b   Mitchell, Derek G V ^a,b   Jones, Matthew ^a   Blair, R J R ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Amygdala; Anterior cingulate cortex; Frontopolar; Instrumental

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; APPETITE; ARTICLE; AVERSION; BRAIN REGION; CINGULATE GYRUS; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; INSTRUMENTAL CONDITIONING; LEARNING; MALE; NEUROMODULATION; NORMAL HUMAN; ORBITAL CORTEX; PRIORITY JOURNAL; REINFORCEMENT; STIMULUS RESPONSE;

ADULT; BRAIN MAPPING; CONDITIONING, OPERANT; DISCRIMINATION LEARNING; EXTINCTION, PSYCHOLOGICAL; FEMALE; FRONTAL LOBE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE;

EID: 54849405917     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2008.08.021     Document Type: Article

References (56)

1. Amaral D.G., and Price J.L. Amygdalo-cortical projections in the monkey (Macaca fascicularis). J. Comp. Neurol. 230 (1984) 465-496
2. Barbas H., and Pandya D.N. Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey. J. Comp. Neurol. 286 (1989) 353-375
3. Baxter M.G., and Murray E.A. The amygdala and reward. Nat. Rev. Neurosci. 3 (2002) 563-573
4. Berlin H.A., Rolls E.T., and Kischka U. Impulsivity, time perception, emotion and reinforcement sensitivity in patients with orbitofrontal cortex lesions. Brain 127 (2004) 1108-1126
5. Blair K., Marsh A.A., Morton J., Vythilingam M., Jones M., Mondillo K., Pine D.C., Drevets W.C., and Blair J.R. Choosing the lesser of two evils, the better of two goods: specifying the roles of ventromedial prefrontal cortex and dorsal anterior cingulate in object choice. J. Neurosci. 26 (2006) 11379-11386
6. Blair K.S., Smith B.W., Mitchell D.G., Morton J., Vythilingam M., Pessoa L., Fridberg D., Zametkin A., Sturman D., Nelson E.E., Drevets W.C., Pine D.S., Martin A., and Blair R.J. Modulation of emotion by cognition and cognition by emotion. Neuroimage 35 (2007) 430-440
7. Budhani S., Marsh A.A., Pine D.S., and Blair R.J. Neural correlates of response reversal: considering acquisition. Neuroimage 34 (2007) 1754-1765
8. Butter C.M. Perseveration in extinction and in discrimination reversal tasks following selective frontal ablations in Macaca mulatta. Physiol. Behav. 4 (1969) 163-171
9. Chudasama Y., and Robbins T.W. Dissociable contributions of the orbitofrontal and infralimbic cortex to pavlovian autoshaping and discrimination reversal learning: further evidence for the functional heterogeneity of the rodent frontal cortex. J. Neurosci. 23 (2003) 8771-8780
10. Cools R., Clark L., Owen A.M., and Robbins T.W. Defining the neural mechanisms of probabilistic reversal learning using event-related functional magnetic resonance imaging. J. Neurosci. 22 (2002) 4563-4567
11. Cox R.W., and Hyde J.S. Software tools for analysis and visualization of fMRI data. NMR Biomed. 10 (1997) 171-178
12. Ellson D.G. Quantitative studies of the interaction of simple habits: I. Recovery from specific and generalized effects of extinction. J. Exp. Psychol. 23 (1938) 349-355
13. Gallagher M., McMahan R.W., and Schoenbaum G. Orbitofrontal cortex and representation of incentive value in associative learning. J. Neurosci. 19 (1999) 6610-6614
14. Gottfried J.A., and Dolan R.J. Human orbitofrontal cortex mediates extinction learning while accessing conditioned representations of value. Nat. Neurosci. 7 (2004) 1144-1152
15. Izquierdo A., and Murray E.A. Opposing effects of amygdala and orbital prefrontal cortex lesions on the extinction of instrumental responding in macaque monkeys. Eur. J. Neurosci. 22 (2005) 2341-2346
16. Izquierdo A., and Murray E.A. Selective bilateral amygdala lesions in rhesus monkeys fail to disrupt object reversal learning. J. Neurosci. 27 (2007) 1054-1062
17. Izquierdo A., Suda R.K., and Murray E.A. Bilateral orbital prefrontal cortex lesions in rhesus monkeys disrupt choices guided by both reward value and reward contingency. J. Neurosci. 24 (2004) 7540-7548
18. Kosson D.S., Budhani S., Nakic M., Chen G., Saad Z.S., Vythilingam M., Pine D.S., and Blair R.J. The role of the amygdala and rostral anterior cingulate in encoding expected outcomes during learning. Neuroimage 29 (2006) 1161-1172
19. LaBar K.S., Gatenby J.C., Gore J.C., LeDoux J.E., and Phelps E.A. Human amygdala activation during conditioned fear acquisition and extinction: a mixed-trial fMRI study. Neuron 20 (1998) 937-945
20. Levesque J., Eugene F., Joanette Y., Paquette V., Mensour B., Beaudoin G., Leroux J.M., Bourgouin P., and Beauregard M. Neural circuitry underlying voluntary suppression of sadness. Biol. Psychiatry 53 (2003) 502-510
21. Lykken D.T. A study of anxiety in the sociopathic personality. J. Abnorm. Psychology 55 (1957) 6-10
22. McDannald M.A., Saddoris M.P., Gallagher M., and Holland P.C. Lesions of orbitofrontal cortex impair rats' differential outcome expectancy learning but not conditioned stimulus-potentiated feeding. J. Neurosci. 25 (2005) 4626-4632
23. Milad M.R., and Quirk G.J. Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 420 (2002) 70-74
24. Milad M.R., Quinn B.T., Pitman R.K., Orr S.P., Fischl B., and Rauch S.L. Thickness of ventromedial prefrontal cortex in humans is correlated with extinction memory. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 10706-10711
25. Milad M.R., Wright C.I., Orr S.P., Pitman R.K., Quirk G.J., and Rauch S.L. Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biol. Psychiatry 62 (2007) 446-454
26. Mitchell D.G., Luo Q., Mondillo K., Vythilingam M., Finger E.C., and Blair R.J. The interference of operant task performance by emotional distracters: an antagonistic relationship between the amygdala and frontoparietal cortices. Neuroimage 40 (2008) 859-868
27. Moran M.A., Mufson E.J., and Mesulam M.M. Neural inputs into the temporopolar cortex of the rhesus monkey. J. Comp. Neurol. 256 (1987) 88-103
28. Newman J.P., and Kosson D.S. Passive avoidance learning in psychopathic and nonpsychopathic offenders. J. Abnorm. Psychology 95 (1986) 252-256
29. O'Doherty J.P. Lights, camembert, action! The role of human orbitofrontal cortex in encoding stimuli, rewards, and choices. Ann. N. Y. Acad. Sci. 1121 (2007) 254-272
30. O'Doherty J., Critchley H., Deichmann R., and Dolan R.J. Dissociating valence of outcome from behavioral control in human orbital and ventral prefrontal cortices. J. Neurosci. 23 (2003) 7931-7939
31. Ohira H., Nomura M., Ichikawa N., Isowa T., Iidaka T., Sato A., Fukuyama S., Nakajima T., and Yamada J. Association of neural and physiological responses during voluntary emotion suppression. Neuroimage 29 (2006) 721-733
32. Ostlund S.B., and Balleine B.W. Lesions of medial prefrontal cortex disrupt the acquisition but not the expression of goal-directed learning. J. Neurosci. 25 (2005) 7763-7770
33. Pavlov I.P. Conditioned Reflexes (1927), Oxford University Press, London
34. Phelps E.A., Delgado M.R., Nearing K.I., and LeDoux J.E. Extinction learning in humans: role of the amygdala and vmPFC. Neuron 43 (2004) 897-905
35. Pickens C.L., Saddoris M.P., Gallagher M., and Holland P.C. Orbitofrontal lesions impair use of cue-outcome associations in a devaluation task. Behav. Neurosci. 119 (2005) 317-322
36. Quirk G.J., Russo G.K., Barron J.L., and Lebron K. The role of ventromedial prefrontal cortex in the recovery of extinguished fear. J. Neurosci. 20 (2000) 6225-6231
37. Ragozzino M.E. The contribution of the medial prefrontal cortex, orbitofrontal cortex, and dorsomedial striatum to behavioral flexibility. Ann. N. Y. Acad. Sci. 1121 (2007) 355-375
38. Rauch S.L., Milad M.R., Orr S.P., Quinn B.T., Fischl B., and Pitman R.K. Orbitofrontal thickness, retention of fear extinction, and extraversion. NeuroReport 16 (2005) 1909-1912
39. Rescorla R.A., Wagner A.R.A., and Skucy J.C. The effect of response-independent reinforcers during extinction. J. Comp. Physiol. Psychol. 67 (1969) 381-389
40. Roesch M.R., Stalnaker T.A., and Schoenbaum G. Associative encoding in anterior piriform cortex versus orbitofrontal cortex during odor discrimination and reversal learning. Cereb. Cortex (2006)
41. Saddoris M.P., Gallagher M., and Schoenbaum G. Rapid associative encoding in basolateral amygdala depends on connections with orbitofrontal cortex. Neuron 46 (2005) 321-331
42. Schmahmann J.D., and Pandya D.N. Fiber Pathways of the Brain (2006), Oxford University Press, Oxford ; New York
43. Schoenbaum G., and Eichenbaum H. Information coding in the rodent prefrontal cortex. II. Ensemble activity in orbitofrontal cortex. J. Neurophysiol. 74 (1995) 751-762
44. Schoenbaum G., and Roesch M. Orbitofrontal cortex, associative learning, and expectancies. Neuron 47 (2005) 633-636
45. Schoenbaum G., Chiba A.A., and Gallagher M. Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning. Nat. Neurosci. 1 (1998) 155-159
46. Schoenbaum G., Chiba A.A., and Gallagher M. Neural encoding in orbitofrontal cortex and basolateral amygdala during olfactory discrimination learning. J. Neurosci. 19 (1999) 1876-1884
47. Schoenbaum G., Chiba A.A., and Gallagher M. Changes in functional connectivity in orbitofrontal cortex and basolateral amygdala during learning and reversal training. J. Neurosci. 20 (2000) 5179-5189
48. Schoenbaum G., Nugent S.L., Saddoris M.P., and Setlow B. Orbitofrontal lesions in rats impair reversal but not acquisition of go, no-go odor discriminations. NeuroReport 13 (2002) 885-890
49. Schoenbaum G., Setlow B., Nugent S.L., Saddoris M.P., and Gallagher M. Lesions of orbitofrontal cortex and basolateral amygdala complex disrupt acquisition of odor-guided discriminations and reversals. Learn. Mem. 10 (2003) 129-140
50. Schoenbaum G., Setlow B., Saddoris M.P., and Gallagher M. Encoding predicted outcome and acquired value in orbitofrontal cortex during cue sampling depends upon input from basolateral amygdala. Neuron 39 (2003) 855-867
51. Schoenbaum G., Saddoris M.P., and Stalnaker T.A. Reconciling the roles of orbitofrontal cortex in reversal learning and the encoding of outcome expectancies. Ann. N. Y. Acad. Sci. 1121 (2007) 320-335
52. Setlow B., Schoenbaum G., and Gallagher M. Neural encoding in ventral striatum during olfactory discrimination learning. Neuron 38 (2003) 625-636
53. Skinner B.F. The Behavior of Organisms (1938), Copley Publishing Group, Acton
54. Talairach J., and Tournoux P. Co-planar Stereotaxic Atlas of the Human Brain (1988), Thieme, Stuttgart
55. Tremblay L., and Schultz W. Reward-related neuronal activity during go-nogo task performance in primate orbitofrontal cortex. J. Neurophysiol. 83 (2000) 1864-1876
56. Valentin V.V., Dickinson A., and O'Doherty J.P. Determining the neural substrates of goal-directed learning in the human brain. J. Neurosci. 27 (2007) 4019-4026