Home LiteratureArticle Details
PMID: 14573543 Published · ppublish English Clinical Trial Journal Article Research Support, Non-U.S. Gov't

Dissociable contributions of the human amygdala and orbitofrontal cortex to incentive motivation and goal selection.

Arana FS, Parkinson JA, Hinton E, Holland AJ, Owen AM, Roberts AC

Abstract

Theories of incentive motivation attempt to capture the way in which objects and events in the world can acquire high motivational value and drive behavior, even in the absence of a clear biological need. In addition, for an individual to select the most appropriate goal, the incentive values of competing desirable objects need to be defined and compared. The present study examined the neural substrates by which appetitive incentive value influences prospective goal selection, using positron emission tomographic neuroimaging in humans. Sated subjects were shown a series of restaurant menus that varied in incentive value, specifically tailored for each individual, and in half the trials, were asked to make a selection from the menu. The amygdala was activated by high-incentive menus regardless of whether a choice was required. Indeed, activity in this region varied as a function of individual subjective ratings of incentive value. In contrast, distinct regions of the orbitofrontal cortex were recruited both during incentive judgments and goal selection. Activity in the medial orbital cortex showed a greater response to high-incentive menus and when making a choice, with the latter activity also correlating with subjective ratings of difficulty. Lateral orbitofrontal activity was observed selectively when participants had to suppress responses to alternative desirable items to select their most preferred. Taken together, these data highlight the differential contribution of the amygdala and regions within the orbitofrontal cortex in a neural system underlying the selection of goals based on the prospective incentive value of stimuli, over and above homeostatic influences.

MeSH Terms
Adult Amygdala/anatomy & histology,diagnostic imaging,physiology Behavior/physiology Blood Flow Velocity Cerebrovascular Circulation/physiology Choice Behavior/physiology Food Preferences/physiology Frontal Lobe/anatomy & histology,diagnostic imaging,physiology Goals Humans Male Motivation Reference Values Tomography, Emission-Computed
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Arana F Sergio
Department of Anatomy, University of Cambridge, Cambridge CB2 3DY, United Kingdom.
Parkinson John A
Hinton Elanor
Holland Anthony J
Owen Adrian M
Roberts Angela C
References (43)
43 references, click to expand
  1. Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning.
    Nat Neurosci. 1998 Jun;1(2):155-9 PMID: 10195132
  2. Amygdala activity related to enhanced memory for pleasant and aversive stimuli.
    Nat Neurosci. 1999 Mar;2(3):289-93 PMID: 10195224
  3. Neuroanatomical correlates of hunger and satiation in humans using positron emission tomography.
    Proc Natl Acad Sci U S A. 1999 Apr 13;96(8):4569-74 PMID: 10200303
  4. Relative reward preference in primate orbitofrontal cortex.
    Nature. 1999 Apr 22;398(6729):704-8 PMID: 10227292
  5. The functional neuroanatomy of emotion and affective style.
    Trends Cogn Sci. 1999 Jan;3(1):11-21 PMID: 10234222
  6. Amygdala circuitry in attentional and representational processes.
    Trends Cogn Sci. 1999 Feb;3(2):65-73 PMID: 10234229
  7. The basal ganglia: a vertebrate solution to the selection problem?
    Neuroscience. 1999;89(4):1009-23 PMID: 10362291
  8. Differential neural responses during performance of matching and nonmatching to sample tasks at two delay intervals.
    J Neurosci. 1999 Jun 15;19(12):5066-73 PMID: 10366639
  9. Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making.
    J Neurosci. 1999 Jul 1;19(13):5473-81 PMID: 10377356
  10. Dissociable roles of the central and basolateral amygdala in appetitive emotional learning.
    Eur J Neurosci. 2000 Jan;12(1):405-13 PMID: 10651899
  11. Dissociable functions in the medial and lateral orbitofrontal cortex: evidence from human neuroimaging studies.
    Cereb Cortex. 2000 Mar;10(3):308-17 PMID: 10731225
  12. Sensory-specific satiety-related olfactory activation of the human orbitofrontal cortex.
    Neuroreport. 2000 Mar 20;11(4):893-7 PMID: 10757540
  13. Control of response selection by reinforcer value requires interaction of amygdala and orbital prefrontal cortex.
    J Neurosci. 2000 Jun 1;20(11):4311-9 PMID: 10818166
  14. Changes in functional connectivity in orbitofrontal cortex and basolateral amygdala during learning and reversal training.
    J Neurosci. 2000 Jul 1;20(13):5179-89 PMID: 10864975
  15. Dissociable neural responses in human reward systems.
    J Neurosci. 2000 Aug 15;20(16):6159-65 PMID: 10934265
  16. Event-related activation in the human amygdala associates with later memory for individual emotional experience.
    J Neurosci. 2000 Oct 1;20(19):RC99 PMID: 11000199
  17. Abstract reward and punishment representations in the human orbitofrontal cortex.
    Nat Neurosci. 2001 Jan;4(1):95-102 PMID: 11135651
  18. Neuropsychology of fear and loathing.
    Nat Rev Neurosci. 2001 May;2(5):352-63 PMID: 11331919
  19. Hunger selectively modulates corticolimbic activation to food stimuli in humans.
    Behav Neurosci. 2001 Apr;115(2):493-500 PMID: 11345973
  20. Lesions of the human amygdala impair enhanced perception of emotionally salient events.
    Nature. 2001 May 17;411(6835):305-9 PMID: 11357132
  21. Involvement of human amygdala and orbitofrontal cortex in hunger-enhanced memory for food stimuli.
    J Neurosci. 2001 Jul 15;21(14):5304-10 PMID: 11438606
  22. Anticipation of increasing monetary reward selectively recruits nucleus accumbens.
    J Neurosci. 2001 Aug 15;21(16):RC159 PMID: 11459880
  23. Changes in brain activity related to eating chocolate: from pleasure to aversion.
    Brain. 2001 Sep;124(Pt 9):1720-33 PMID: 11522575
  24. The role of the primate amygdala in conditioned reinforcement.
    J Neurosci. 2001 Oct 1;21(19):7770-80 PMID: 11567067
  25. Stereotaxic display of brain lesions.
    Behav Neurol. 2000;12(4):191-200 PMID: 11568431
  26. Neural responses during anticipation of a primary taste reward.
    Neuron. 2002 Feb 28;33(5):815-26 PMID: 11879657
  27. Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex.
    Neurosci Biobehav Rev. 2002 May;26(3):321-52 PMID: 12034134
  28. Neural economics and the biological substrates of valuation.
    Neuron. 2002 Oct 10;36(2):265-84 PMID: 12383781
  29. The effect of lesions of the basolateral amygdala on instrumental conditioning.
    J Neurosci. 2003 Jan 15;23(2):666-75 PMID: 12533626
  30. Dissociated neural representations of intensity and valence in human olfaction.
    Nat Neurosci. 2003 Feb;6(2):196-202 PMID: 12536208
  31. Lesions of orbitofrontal cortex and basolateral amygdala complex disrupt acquisition of odor-guided discriminations and reversals.
    Learn Mem. 2003 Mar-Apr;10(2):129-40 PMID: 12663751
  32. A three-dimensional statistical analysis for CBF activation studies in human brain.
    J Cereb Blood Flow Metab. 1992 Nov;12(6):900-18 PMID: 1400644
  33. Lesions of the orbitofrontal but not medial prefrontal cortex disrupt conditioned reinforcement in primates.
    J Neurosci. 2003 Dec 3;23(35):11189-201 PMID: 14657178
  34. A unified statistical approach for determining significant signals in images of cerebral activation.
    Hum Brain Mapp. 1996;4(1):58-73 PMID: 20408186
  35. Sexual motivation: a neural and behavioural analysis of the mechanisms underlying appetitive and copulatory responses of male rats.
    Neurosci Biobehav Rev. 1990 Summer;14(2):217-32 PMID: 2190121
  36. Parallel organization of functionally segregated circuits linking basal ganglia and cortex.
    Annu Rev Neurosci. 1986;9:357-81 PMID: 3085570
  37. A motivational view of learning, performance, and behavior modification.
    Psychol Rev. 1974 May;81(3):199-213 PMID: 4424766
  38. Perseverative interference in monkeys following selective lesions of the inferior prefrontal convexity.
    Exp Brain Res. 1970 Nov 26;11(4):376-86 PMID: 4993199
  39. Reward-related activity in the monkey striatum and substantia nigra.
    Prog Brain Res. 1993;99:227-35 PMID: 8108550
  40. Differential effects of excitotoxic lesions of the basolateral amygdala, ventral subiculum and medial prefrontal cortex on responding with conditioned reinforcement and locomotor activity potentiated by intra-accumbens infusions of D-amphetamine.
    Behav Brain Res. 1993 Jun 30;55(2):167-83 PMID: 8357526
  41. Modulation of memory storage.
    Curr Opin Neurobiol. 1996 Apr;6(2):237-42 PMID: 8725966
  42. Different types of fear-conditioned behaviour mediated by separate nuclei within amygdala.
    Nature. 1997 Jul 24;388(6640):377-80 PMID: 9237754
  43. Limbic activation during cue-induced cocaine craving.
    Am J Psychiatry. 1999 Jan;156(1):11-8 PMID: 9892292
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2003-10-22
Pages
9632-8
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6740473
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]