 |
Previous Article | Next Article 
Control of Response Selection by Reinforcer Value Requires
Interaction of Amygdala and Orbital Prefrontal Cortex
Mark G.
Baxter1,
Amanda
Parker2,
Caroline C. C.
Lindner3,
Alicia D.
Izquierdo3, 4, and
Elisabeth A.
Murray3
1 Department of Psychology, Harvard University,
Cambridge, Massachusetts 02138, 2 School of Psychology,
University of Nottingham, Nottingham NG7 2RD, United Kingdom,
3 Laboratory of Neuropsychology, National Institute of
Mental Health, Bethesda, Maryland 20892, and 4 Department
of Psychology, The George Washington University, Washington, DC 20052
Goal-directed actions are guided by expected outcomes of those
actions. Humans with bilateral damage to ventromedial prefrontal cortex, or the amygdala, are deficient in their ability to use information about positive and negative outcomes to guide their choice
behavior. Similarly, rats and monkeys with orbital prefrontal or
amygdala damage have been found to be impaired in their responses to
changing values of outcomes. In the present study, we tested whether
direct, functional interaction between the amygdala and the orbital
prefrontal cortex is necessary for guiding behavior based on expected
outcomes. Unlike control monkeys, rhesus monkeys with surgical
disconnection of these two structures, achieved by crossed unilateral
lesions of the amygdala in one hemisphere and orbital prefrontal cortex
in the other, combined with forebrain commissurotomy, were unable to
adjust their choice behavior after a change in the outcome (here, a
reduction in the value of a particular reinforcer). The lesions did not
affect motivation to work for a food reinforcer, or food preferences,
per se. Hence, the amygdala and orbital prefrontal cortex act as part
of an integrated neural system guiding decision-making and adaptive
response selection.
Key words:
amygdala; crossed-lesion technique; decision-making; orbital prefrontal cortex; reinforcer devaluation; representation; rhesus monkey
Copyright © 2000 Society for Neuroscience 0270-6474/00/20114311-09$05.00/0
This article has been cited by other articles:

|
 |

|
 |
 
J. Li, E. Xiao, D. Houser, and P. R. Montague
Neural responses to sanction threats in two-party economic exchange
PNAS,
September 29, 2009;
106(39):
16835 - 16840.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. E. Morrison and C. D. Salzman
The Convergence of Information about Rewarding and Aversive Stimuli in Single Neurons
J. Neurosci.,
September 16, 2009;
29(37):
11471 - 11483.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. McDannald and G. Schoenbaum
Toward a Model of Impaired Reality Testing in Rats
Schizophr Bull,
July 1, 2009;
35(4):
664 - 667.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Grossberg
Cortical and subcortical predictive dynamics and learning during perception, cognition, emotion and action
Phil Trans R Soc B,
May 12, 2009;
364(1521):
1223 - 1234.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Kazama and J. Bachevalier
Selective Aspiration or Neurotoxic Lesions of Orbital Frontal Areas 11 and 13 Spared Monkeys' Performance on the Object Discrimination Reversal Task
J. Neurosci.,
March 4, 2009;
29(9):
2794 - 2804.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. H. Rudebeck, T. E. Behrens, S. W. Kennerley, M. G. Baxter, M. J. Buckley, M. E. Walton, and M. F. S. Rushworth
Frontal Cortex Subregions Play Distinct Roles in Choices between Actions and Stimuli
J. Neurosci.,
December 17, 2008;
28(51):
13775 - 13785.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. B. Floresco, J. R. St. Onge, S. Ghods-Sharifi, and C. A. Winstanley
Cortico-limbic-striatal circuits subserving different forms of cost-benefit decision making
Cogn Affect Behav Neurosci,
December 1, 2008;
8(4):
375 - 389.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Shea, K. Krug, and P. N. Tobler
Conceptual representations in goal-directed decision making
Cogn Affect Behav Neurosci,
December 1, 2008;
8(4):
418 - 428.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
P. H. Rudebeck, D. M. Bannerman, and M. F. S. Rushworth
The contribution of distinct subregions of the ventromedial frontal cortex to emotion, social behavior, and decision making
Cogn Affect Behav Neurosci,
December 1, 2008;
8(4):
485 - 497.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Todorov and A. D. Engell
The role of the amygdala in implicit evaluation of emotionally neutral faces
Soc Cogn Affect Neurosci,
December 1, 2008;
3(4):
303 - 312.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. E. Guyer, J. Y. F. Lau, E. B. McClure-Tone, J. Parrish, N. D. Shiffrin, R. C. Reynolds, G. Chen, R. J. R. Blair, E. Leibenluft, N. A. Fox, et al.
Amygdala and Ventrolateral Prefrontal Cortex Function During Anticipated Peer Evaluation in Pediatric Social Anxiety
Arch Gen Psychiatry,
November 1, 2008;
65(11):
1303 - 1312.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. van Duuren, J. Lankelma, and C. M. A. Pennartz
Population Coding of Reward Magnitude in the Orbitofrontal Cortex of the Rat
J. Neurosci.,
August 20, 2008;
28(34):
8590 - 8603.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. H. Rudebeck and E. A. Murray
Amygdala and Orbitofrontal Cortex Lesions Differentially Influence Choices during Object Reversal Learning
J. Neurosci.,
August 13, 2008;
28(33):
8338 - 8343.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Ito, T. W. Robbins, C. M. Pennartz, and B. J. Everitt
Functional Interaction between the Hippocampus and Nucleus Accumbens Shell Is Necessary for the Acquisition of Appetitive Spatial Context Conditioning
J. Neurosci.,
July 2, 2008;
28(27):
6950 - 6959.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. S. Monk, E. H. Telzer, K. Mogg, B. P. Bradley, X. Mai, H. M. C. Louro, G. Chen, E. B. McClure-Tone, M. Ernst, and D. S. Pine
Amygdala and Ventrolateral Prefrontal Cortex Activation to Masked Angry Faces in Children and Adolescents With Generalized Anxiety Disorder
Arch Gen Psychiatry,
May 1, 2008;
65(5):
568 - 576.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C.-W. Ng, M. I. Noblejas, J. S. Rodefer, C. B. Smith, and A. Poremba
Double Dissociation of Attentional Resources: Prefrontal Versus Cingulate Cortices
J. Neurosci.,
November 7, 2007;
27(45):
12123 - 12131.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. S. Mitchell, P. G. F. Browning, and M. G. Baxter
Neurotoxic Lesions of the Medial Mediodorsal Nucleus of the Thalamus Disrupt Reinforcer Devaluation Effects in Rhesus Monkeys
J. Neurosci.,
October 17, 2007;
27(42):
11289 - 11295.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. van Duuren, F. A. N. Escamez, R. N.J.M.A. Joosten, R. Visser, A. B. Mulder, and C. M.A. Pennartz
Neural coding of reward magnitude in the orbitofrontal cortex of the rat during a five-odor olfactory discrimination task
Learn. Mem.,
June 11, 2007;
14(6):
446 - 456.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R.J Dolan
The human amygdala and orbital prefrontal cortex in behavioural regulation
Phil Trans R Soc B,
May 29, 2007;
362(1481):
787 - 799.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. M. Tye and P. H. Janak
Amygdala Neurons Differentially Encode Motivation and Reinforcement
J. Neurosci.,
April 11, 2007;
27(15):
3937 - 3945.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. V. Valentin, A. Dickinson, and J. P. O'Doherty
Determining the Neural Substrates of Goal-Directed Learning in the Human Brain
J. Neurosci.,
April 11, 2007;
27(15):
4019 - 4026.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Izquierdo and E. A. Murray
Selective Bilateral Amygdala Lesions in Rhesus Monkeys Fail to Disrupt Object Reversal Learning
J. Neurosci.,
January 31, 2007;
27(5):
1054 - 1062.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. E. Guyer, E. E. Nelson, K. Perez-Edgar, M. G. Hardin, R. Roberson-Nay, C. S. Monk, J. M. Bjork, H. A. Henderson, D. S. Pine, N. A. Fox, et al.
Striatal functional alteration in adolescents characterized by early childhood behavioral inhibition.
J. Neurosci.,
June 14, 2006;
26(24):
6399 - 6405.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. A. Berlin, E. T. Rolls, and S. D. Iversen
Borderline Personality Disorder, Impulsivity, and the Orbitofrontal Cortex
Am J Psychiatry,
December 1, 2005;
162(12):
2360 - 2373.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Sugase-Miyamoto and B. J. Richmond
Neuronal Signals in the Monkey Basolateral Amygdala during Reward Schedules
J. Neurosci.,
November 30, 2005;
25(48):
11071 - 11083.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
X. Protopopescu, H. Pan, M. Altemus, O. Tuescher, M. Polanecsky, B. McEwen, D. Silbersweig, and E. Stern
Orbitofrontal cortex activity related to emotional processing changes across the menstrual cycle
PNAS,
November 1, 2005;
102(44):
16060 - 16065.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. L. Croxson, H. Johansen-Berg, T. E. J. Behrens, M. D. Robson, M. A. Pinsk, C. G. Gross, W. Richter, M. C. Richter, S. Kastner, and M. F. S. Rushworth
Quantitative Investigation of Connections of the Prefrontal Cortex in the Human and Macaque using Probabilistic Diffusion Tractography
J. Neurosci.,
September 28, 2005;
25(39):
8854 - 8866.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Izquierdo, R. K. Suda, and E. A. Murray
Comparison of the Effects of Bilateral Orbital Prefrontal Cortex Lesions and Amygdala Lesions on Emotional Responses in Rhesus Monkeys
J. Neurosci.,
September 14, 2005;
25(37):
8534 - 8542.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Schoenbaum and B. Setlow
Cocaine Makes Actions Insensitive to Outcomes but not Extinction: Implications for Altered Orbitofrontal-Amygdalar Function
Cereb Cortex,
August 1, 2005;
15(8):
1162 - 1169.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Birbaumer, R. Veit, M. Lotze, M. Erb, C. Hermann, W. Grodd, and H. Flor
Deficient Fear Conditioning in Psychopathy: A Functional Magnetic Resonance Imaging Study
Arch Gen Psychiatry,
July 1, 2005;
62(7):
799 - 805.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. L. Wellman, K. Gale, and L. Malkova
GABAA-Mediated Inhibition of Basolateral Amygdala Blocks Reward Devaluation in Macaques
J. Neurosci.,
May 4, 2005;
25(18):
4577 - 4586.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Hurliman, J. C. Nagode, and J. V. Pardo
Double Dissociation of Exteroceptive and Interoceptive Feedback Systems in the Orbital and Ventromedial Prefrontal Cortex of Humans
J. Neurosci.,
May 4, 2005;
25(18):
4641 - 4648.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. W. Johnson, D. M. Bannerman, N. P. Rawlins, R. Sprengel, and M. A. Good
Impaired Outcome-Specific Devaluation of Instrumental Responding in Mice with a Targeted Deletion of the AMPA Receptor Glutamate Receptor 1 Subunit
J. Neurosci.,
March 2, 2005;
25(9):
2359 - 2365.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. S. Crombag, G. Gorny, Y. Li, B. Kolb, and T. E. Robinson
Opposite Effects of Amphetamine Self-administration Experience on Dendritic Spines in the Medial and Orbital Prefrontal Cortex
Cereb Cortex,
March 1, 2005;
15(3):
341 - 348.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. K. Fellows
The Cognitive Neuroscience of Human Decision Making: A Review and Conceptual Framework
Behav Cogn Neurosci Rev,
September 1, 2004;
3(3):
159 - 172.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Izquierdo, R. K. Suda, and E. A. Murray
Bilateral Orbital Prefrontal Cortex Lesions in Rhesus Monkeys Disrupt Choices Guided by Both Reward Value and Reward Contingency
J. Neurosci.,
August 25, 2004;
24(34):
7540 - 7548.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. J. Kennedy and M. L. Shapiro
Retrieving Memories via Internal Context Requires the Hippocampus
J. Neurosci.,
August 4, 2004;
24(31):
6979 - 6985.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. A. Winstanley, D. E. H. Theobald, R. N. Cardinal, and T. W. Robbins
Contrasting Roles of Basolateral Amygdala and Orbitofrontal Cortex in Impulsive Choice
J. Neurosci.,
May 19, 2004;
24(20):
4718 - 4722.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Izquierdo and E. A. Murray
Combined Unilateral Lesions of the Amygdala and Orbital Prefrontal Cortex Impair Affective Processing in Rhesus Monkeys
J Neurophysiol,
May 1, 2004;
91(5):
2023 - 2039.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. L. Pickens, M. P. Saddoris, B. Setlow, M. Gallagher, P. C. Holland, and G. Schoenbaum
Different Roles for Orbitofrontal Cortex and Basolateral Amygdala in a Reinforcer Devaluation Task
J. Neurosci.,
December 3, 2003;
23(35):
11078 - 11084.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Pears, J. A. Parkinson, L. Hopewell, B. J. Everitt, and A. C. Roberts
Lesions of the Orbitofrontal but not Medial Prefrontal Cortex Disrupt Conditioned Reinforcement in Primates
J. Neurosci.,
December 3, 2003;
23(35):
11189 - 11201.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Schoenbaum and B. Setlow
Lesions of Nucleus Accumbens Disrupt Learning about Aversive Outcomes
J. Neurosci.,
October 29, 2003;
23(30):
9833 - 9841.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. S. Arana, J. A. Parkinson, E. Hinton, A. J. Holland, A. M. Owen, and A. C. Roberts
Dissociable Contributions of the Human Amygdala and Orbitofrontal Cortex to Incentive Motivation and Goal Selection
J. Neurosci.,
October 22, 2003;
23(29):
9632 - 9638.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. A. Gottfried, J. O'Doherty, and R. J. Dolan
Encoding Predictive Reward Value in Human Amygdala and Orbitofrontal Cortex
Science,
August 22, 2003;
301(5636):
1104 - 1107.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. L. Fudge and A. B. Emiliano
The Extended Amygdala and the Dopamine System: Another Piece of the Dopamine Puzzle
J Neuropsychiatry Clin Neurosci,
August 1, 2003;
15(3):
306 - 316.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
J. Hornak, J. Bramham, E. T. Rolls, R. G. Morris, J. O'Doherty, P. R. Bullock, and C. E. Polkey
Changes in emotion after circumscribed surgical lesions of the orbitofrontal and cingulate cortices
Brain,
July 1, 2003;
126(7):
1691 - 1712.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Killcross and E. Coutureau
Coordination of Actions and Habits in the Medial Prefrontal Cortex of Rats
Cereb Cortex,
April 1, 2003;
13(4):
400 - 408.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Schoenbaum, B. Setlow, S. L. Nugent, M. P. Saddoris, and M. Gallagher
Lesions of Orbitofrontal Cortex and Basolateral Amygdala Complex Disrupt Acquisition of Odor-Guided Discriminations and Reversals
Learn. Mem.,
March 1, 2003;
10(2):
129 - 140.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. A. Hadland, M.F.S. Rushworth, D. Gaffan, and R. E. Passingham
The Anterior Cingulate and Reward-Guided Selection of Actions
J Neurophysiol,
February 1, 2003;
89(2):
1161 - 1164.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. N. Mead and D. N. Stephens
Selective Disruption of Stimulus-Reward Learning in Glutamate Receptor gria1 Knock-Out Mice
J. Neurosci.,
February 1, 2003;
23(3):
1041 - 1048.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. W. Balleine, A. S. Killcross, and A. Dickinson
The Effect of Lesions of the Basolateral Amygdala on Instrumental Conditioning
J. Neurosci.,
January 15, 2003;
23(2):
666 - 675.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. E. Kelley and K. C. Berridge
The Neuroscience of Natural Rewards: Relevance to Addictive Drugs
J. Neurosci.,
May 1, 2002;
22(9):
3306 - 3311.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Adolphs
Recognizing emotion from facial expressions: psychological and neurological mechanisms.
Behav Cogn Neurosci Rev,
March 1, 2002;
1(1):
21 - 62.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
W. M. Perlstein, T. Elbert, and V. A. Stenger
Dissociation in human prefrontal cortex of affective influences on working memory-related activity
PNAS,
January 24, 2002;
(2002)
241650598.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. S. Rubinsztein, P. C. Fletcher, R. D. Rogers, L. W. Ho, F. I. Aigbirhio, E. S. Paykel, T. W. Robbins, and B. J. Sahakian
Decision-making in mania: a PET study
Brain,
December 1, 2001;
124(12):
2550 - 2563.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Pierce, R.-A. Muller, J. Ambrose, G. Allen, and E. Courchesne
Face processing occurs outside the fusiform `face area' in autism: evidence from functional MRI
Brain,
October 1, 2001;
124(10):
2059 - 2073.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. A. Parkinson, H. S. Crofts, M. McGuigan, D. L. Tomic, B. J. Everitt, and A. C. Roberts
The Role of the Primate Amygdala in Conditioned Reinforcement
J. Neurosci.,
October 1, 2001;
21(19):
7770 - 7780.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. S. Morris and R. J. Dolan
Involvement of Human Amygdala and Orbitofrontal Cortex in Hunger-Enhanced Memory for Food Stimuli
J. Neurosci.,
July 15, 2001;
21(14):
5304 - 5310.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Schoenbaum and B. Setlow
Integrating Orbitofrontal Cortex into Prefrontal Theory: Common Processing Themes across Species and Subdivisions
Learn. Mem.,
May 1, 2001;
8(3):
134 - 147.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. E. Jackson and B. Moghaddam
Amygdala Regulation of Nucleus Accumbens Dopamine Output is Governed by the Prefrontal Cortex
J. Neurosci.,
January 15, 2001;
21(2):
676 - 681.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. W. Balleine and A. Dickinson
The Effect of Lesions of the Insular Cortex on Instrumental Conditioning: Evidence for a Role in Incentive Memory
J. Neurosci.,
December 1, 2000;
20(23):
8954 - 8964.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. M. Perlstein, T. Elbert, and V. A. Stenger
Dissociation in human prefrontal cortex of affective influences on working memory-related activity
PNAS,
February 5, 2002;
99(3):
1736 - 1741.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|

|