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PMID: 10818166 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Control of response selection by reinforcer value requires interaction of amygdala and orbital prefrontal cortex.

Baxter MG, Parker A, Lindner CC, Izquierdo AD, Murray EA

Abstract

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.

MeSH Terms
Accommodation, Ocular/physiology Amygdala/physiology Animals Discrimination, Psychological/physiology Food Macaca mulatta Male Motivation Prefrontal Cortex/physiology Prosencephalon/physiology Reinforcement Schedule Reinforcement, Psychology Reward Satiety Response/physiology
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Baxter M G
Department of Psychology, Harvard University, Cambridge, Massachusetts 02138, USA.
Parker A
Lindner C C
Izquierdo A D
Murray E A
References (31)
31 references, click to expand
  1. The frontal cortex-basal ganglia system in primates.
    Crit Rev Neurobiol. 1996;10(3-4):317-56 PMID: 8978985
  2. Effects of aspiration versus neurotoxic lesions of the amygdala on emotional responses in monkeys.
    Eur J Neurosci. 1999 Dec;11(12):4403-18 PMID: 10594668
  3. Specialisation within the prefrontal cortex: the ventral prefrontal cortex and associative learning.
    Exp Brain Res. 2000 Jul;133(1):103-13 PMID: 10933215
  4. Orbitofrontal cortex and representation of incentive value in associative learning.
    J Neurosci. 1999 Aug 1;19(15):6610-4 PMID: 10414988
  5. Anterior rhinal cortex and amygdala: dissociation of their contributions to memory and food preference in rhesus monkeys.
    Behav Neurosci. 1996 Feb;110(1):30-42 PMID: 8652070
  6. Direct and indirect pathways from the amygdala to the frontal lobe in rhesus monkeys.
    J Comp Neurol. 1981 May 1;198(1):121-36 PMID: 6164704
  7. Emotion: clues from the brain.
    Annu Rev Psychol. 1995;46:209-35 PMID: 7872730
  8. Visual discrimination following successive temporal ablations in monkeys.
    Brain. 1959 Jun;82:232-50 PMID: 13820931
  9. Amygdala circuitry in attentional and representational processes.
    Trends Cogn Sci. 1999 Feb;3(2):65-73 PMID: 10234229
  10. Performance norms for a rhesus monkey neuropsychological testing battery: acquisition and long-term performance.
    Brain Res Cogn Brain Res. 1999 Oct 25;8(3):185-201 PMID: 10556598
  11. Syndrome produced by lesions of the amygdala in monkeys (Macaca mulatta).
    J Comp Physiol Psychol. 1981 Dec;95(6):961-77 PMID: 7320283
  12. Relative reward preference in primate orbitofrontal cortex.
    Nature. 1999 Apr 22;398(6729):704-8 PMID: 10227292
  13. The lateral nucleus of the amygdala mediates expression of the amphetamine-produced conditioned place preference.
    J Neurosci. 1991 Jul;11(7):2107-16 PMID: 2066777
  14. Neurotoxic lesions of basolateral, but not central, amygdala interfere with Pavlovian second-order conditioning and reinforcer devaluation effects.
    J Neurosci. 1996 Aug 15;16(16):5256-65 PMID: 8756453
  15. Dissociable deficits in the decision-making cognition of chronic amphetamine abusers, opiate abusers, patients with focal damage to prefrontal cortex, and tryptophan-depleted normal volunteers: evidence for monoaminergic mechanisms.
    Neuropsychopharmacology. 1999 Apr;20(4):322-39 PMID: 10088133
  16. Impairment of social and moral behavior related to early damage in human prefrontal cortex.
    Nat Neurosci. 1999 Nov;2(11):1032-7 PMID: 10526345
  17. Amygdalo-cortical projections in the monkey (Macaca fascicularis).
    J Comp Neurol. 1984 Dec 20;230(4):465-96 PMID: 6520247
  18. Rhinal cortex ablations fail to disrupt reinforcer devaluation effects in rhesus monkeys (Macaca mulatta).
    Behav Neurosci. 1998 Aug;112(4):1020-5 PMID: 9733208
  19. Unity and diversity of frontal lobe functions.
    Acta Neurobiol Exp (Wars). 1972;32(2):615-56 PMID: 4627626
  20. An assessment of the reinforcing properties of foods after amygdaloid lesions in rhesus monkeys.
    J Comp Physiol Psychol. 1982 Feb;96(1):71-7 PMID: 7056901
  21. Behavioral changes associated with ablation of the amygdaloid complex in monkeys.
    J Comp Physiol Psychol. 1956 Aug;49(4):381-91 PMID: 13345917
  22. Neural encoding in orbitofrontal cortex and basolateral amygdala during olfactory discrimination learning.
    J Neurosci. 1999 Mar 1;19(5):1876-84 PMID: 10024371
  23. Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys.
    J Comp Neurol. 1995 Dec 25;363(4):615-641 PMID: 8847421
  24. Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making.
    J Neurosci. 1999 Jul 1;19(13):5473-81 PMID: 10377356
  25. Dissociation Of working memory from decision making within the human prefrontal cortex.
    J Neurosci. 1998 Jan 1;18(1):428-37 PMID: 9412519
  26. Excitotoxic lesions of the amygdala fail to produce impairment in visual learning for auditory secondary reinforcement but interfere with reinforcer devaluation effects in rhesus monkeys.
    J Neurosci. 1997 Aug 1;17(15):6011-20 PMID: 9221797
  27. Choosing between small, likely rewards and large, unlikely rewards activates inferior and orbital prefrontal cortex.
    J Neurosci. 1999 Oct 15;19(20):9029-38 PMID: 10516320
  28. The orbitofrontal cortex.
    Philos Trans R Soc Lond B Biol Sci. 1996 Oct 29;351(1346):1433-43; discussion 1443-4 PMID: 8941955
  29. The human amygdala in social judgment.
    Nature. 1998 Jun 4;393(6684):470-4 PMID: 9624002
  30. Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning.
    Nat Neurosci. 1998 Jun;1(2):155-9 PMID: 10195132
  31. Emotion-related learning in patients with social and emotional changes associated with frontal lobe damage.
    J Neurol Neurosurg Psychiatry. 1994 Dec;57(12):1518-24 PMID: 7798983
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2000-06-01
Pages
4311-9
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6772657
Subset
IM
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