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ARTICLE, Behavioral/Systems

Control of Response Selection by Reinforcer Value Requires Interaction of Amygdala and Orbital Prefrontal Cortex

Mark G. Baxter, Amanda Parker, Caroline C. C. Lindner, Alicia D. Izquierdo and Elisabeth A. Murray
Journal of Neuroscience 1 June 2000, 20 (11) 4311-4319; https://doi.org/10.1523/JNEUROSCI.20-11-04311.2000
Mark G. Baxter
1Department of Psychology, Harvard University, Cambridge, Massachusetts 02138,
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Amanda Parker
2School of Psychology, University of Nottingham, Nottingham NG7 2RD, United Kingdom,
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Caroline C. C. Lindner
3Laboratory of Neuropsychology, National Institute of Mental Health, Bethesda, Maryland 20892, and
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Alicia D. Izquierdo
3Laboratory of Neuropsychology, National Institute of Mental Health, Bethesda, Maryland 20892, and
4Department of Psychology, The George Washington University, Washington, DC 20052
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Elisabeth A. Murray
3Laboratory of Neuropsychology, National Institute of Mental Health, Bethesda, Maryland 20892, and
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    Fig. 1.

    Schematic of testing sequence for the reinforcer devaluation study. Control subjects received no surgery and were given a period of rest equivalent to that provided for the operated monkeys. Note that surgery 2 completes the disconnection of amygdala and orbital prefrontal cortex in all operated subjects.

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    Fig. 2.
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    Fig. 2.

    Intended lesion and plots of the orbital prefrontal cortex and amygdala lesions in the four operated cases (Op1–Op4), shown on ventral surface views (top) and coronal sections (bottom) from a standard rhesus monkey brain. The intended lesion is shown in the leftmost column. The thick black line and small rectangle between the hemispheres in this and other ventral views indicates the extent of the section of the corpus callosum and anterior commissure, respectively; positions of the stereotaxic levels illustrated in the coronal sections are also indicated. The ventral views for Op1–Op4 show reconstructions of the extent of the orbital prefrontal cortex lesions, and are reversed to aid in matching to the individual sections (i.e., the left hemisphere is on theleft). The numbers to theleft of the coronal sections indicate the distance in millimeters from the interaural plane. Compare and contrast with Figure3.

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    Fig. 3.

    Photomicrographs of Nissl-stained coronal sections from case Op3. A, Coronal section ∼30 mm rostral to the interaural plane. The extent of the orbital prefrontal cortex lesion in the left hemisphere is marked by the black arrows. The section of the corpus callosum is also apparent at this level and is marked by the white arrowhead.B, Coronal section 16 mm rostral to the interaural plane. Note the marked loss in volume of the amygdala in the right compared with the left hemisphere. The section of the corpus callosum is marked by the white arrowhead. Therectangles over the left and right temporal lobes show the approximate locations of the regions shown at higher power inC and D, respectively. C, Photomicrograph of the intact (left) amygdala. D, Photomicrograph of the right amygdala ∼9 months after injection of ibotenic acid, at the same magnification used in C. The marked neuronal cell loss and gliosis are characteristic of excitotoxic lesions.

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    Fig. 4.

    The effects of reinforcer devaluation performed before (Test 1) and after (Test 2) the surgical disconnection had been completed. Difference scores (devaluation − baseline) for the control and disconnection group means are shown as bars, with the symbols representing scores of individual monkeys. Normal monkeys showed an enhancement of the devaluation effect in the second test, whereas operated monkeys showed a significant reduction of this effect in the second test. Op1,Filled diamonds; Op2, filled squares; Op3, filled inverted triangles; Op4, filled circles; Con1, open diamonds; Con2, open squares; Con3, open inverted triangles; Con4,open circle.

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    Fig. 5.

    Results of the devaluation procedure (selective satiation) on progressive ratio testing. Baseline data shown are the mean, for each subject, of the maximum number of responses emitted (i.e., maximum ratio attained) during all four baseline sessions. Satiation data are scores for the single satiation session. Group means are shown as bars, with the symbols representing scores of individual monkeys. All monkeys, regardless of group membership, decreased responding during the test session in which the reinforcer was devalued by selective satiation. Symbols as in Figure 4.

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    Table 1.

    Percent damage to amygdala and orbital prefrontal cortex in the four operated subjects

    CaseAmygdalaOrbital prefrontal
    HemispherePercent damageHemispherePercent damage
    Op1L (first)42.9R (second)65.5
    Op2L (second)34.9R (first)73.3
    Op3R (first)95.3L (second)57.1
    Op4R (second)28.4L (first)41.1
    Mean50.459.3
    • The hemisphere in which each lesion was placed (left, L; right, R) and the order in which the surgeries were conducted are indicated. For example, case Op1 received a neurotoxic amygdala lesion in the left hemisphere before beginning behavioral testing and a lesion of the orbital prefrontal cortex in the right hemisphere, with forebrain commissurotomy in the same surgery, to complete the disconnection. See Figure 1 for a schematic of the behavioral testing sequence.

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    Table 2.

    Results of reinforcer devaluation testing

    CaseTest 1Test 2Test 2-test 1 difference
    Baseline F1:F2Satiation F1 F1:F2Satiation F2 F1:F2Difference score (sum)Baseline F1:F2Satiation F1 F1:F2Satiation F2 F1:F2Difference score (sum)
    Con122:814 :1626 :41223.5:6.57 :2327 :3208
    Con214:1612 :1822 :81019.5:10.513 :1728 :2155
    Con327.5:2.528:229 :1120:1013 :1719 :1165
    Con421.5:8.57 :2322 :81515.5:14.56 :2424 :6183
    Mean9.514.755.25
    Op118.5:11.516 :1426 :41025:523 :728 :25−5
    Op224.5:5.517 :1326 :4929.5:0.523 :730 :07−2
    Op320.5:9.512 :1825 :51323.5:6.521 :922 :81−12
    Op4 2.5:27.50 :302 :2820:300 :302 :2820
    Mean8.53.75−4.75
    • The number of food 1 (F1) and food 2 (F2) objects chosen in the baseline sessions (mean of two sessions) and each of the two satiation sessions (preceded by satiation with food 1 or food 2), as well as the difference score between the satiation sessions and the baseline sessions (summed for the two satiation sessions), are given for reinforcer devaluation test 1 and test 2 for each of the eight monkeys (Con1–Con4, control monkeys; Op1–Op4, operated monkeys).

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The Journal of Neuroscience: 20 (11)
Journal of Neuroscience
Vol. 20, Issue 11
1 Jun 2000
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Control of Response Selection by Reinforcer Value Requires Interaction of Amygdala and Orbital Prefrontal Cortex
Mark G. Baxter, Amanda Parker, Caroline C. C. Lindner, Alicia D. Izquierdo, Elisabeth A. Murray
Journal of Neuroscience 1 June 2000, 20 (11) 4311-4319; DOI: 10.1523/JNEUROSCI.20-11-04311.2000

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Control of Response Selection by Reinforcer Value Requires Interaction of Amygdala and Orbital Prefrontal Cortex
Mark G. Baxter, Amanda Parker, Caroline C. C. Lindner, Alicia D. Izquierdo, Elisabeth A. Murray
Journal of Neuroscience 1 June 2000, 20 (11) 4311-4319; DOI: 10.1523/JNEUROSCI.20-11-04311.2000
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Keywords

  • amygdala
  • crossed-lesion technique
  • decision-making
  • orbital prefrontal cortex
  • reinforcer devaluation
  • representation
  • rhesus monkey

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