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Behavioral/Systems/Cognitive

Comparison of the Effects of Bilateral Orbital Prefrontal Cortex Lesions and Amygdala Lesions on Emotional Responses in Rhesus Monkeys

Alicia Izquierdo, Robin K. Suda and Elisabeth A. Murray
Journal of Neuroscience 14 September 2005, 25 (37) 8534-8542; DOI: https://doi.org/10.1523/JNEUROSCI.1232-05.2005
Alicia Izquierdo
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Robin K. Suda
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Elisabeth A. Murray
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  •   Figure 1.
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    Figure 1.

    Left column, Coronal sections from a standard rhesus monkey brain showing the location and extent of the intended bilateral amygdala lesion (shaded region). Numerals indicate distance from the interaural plane (0). Middle and right columns, MR images from cases Amyg-1 (largest lesion) and Amyg-4 (smallest lesion) at matching levels. T2-weighted MR images reveal the extent of white hypersignal, which reflects edema consequent to the injections of ibotenate and therefore the approximate site of the amygdala lesions.

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    Figure 2.

    Mean food-retrieval latencies (in seconds) across sessions. A, Operated groups differed significantly from controls in their latencies to reach over the rubber snake. Group Amyg (*) or group PFo (#) differ significantly from controls (post hoc Bonferroni's tests, p < 0.05). B, Group Amyg (*) differs significantly from controls (post hoc Bonferroni's tests, p < 0.05) in latencies to reach over the rubber spider. C, There were no group differences in latencies to reach over neutral objects. Group Con, n = 10; group PFo, n = 4; group Amyg, n = 4. Error bars indicate SEM.

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    Figure 3.

    Group mean cumulative duration of defense and approach behaviors when exposed to the rubber snake. Only group Amyg differed significantly from group Con in both their defensive and approach behaviors. *Significantly different from controls (post hoc Bonferroni's tests, p < 0.05). Group Con, n = 10; group PFo, n = 4; group Amyg, n = 4. Error bars indicate SEM.

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    Figure 4.

    Responses to a human intruder. The mean cumulative duration of categories of behavior during the human intruder task is shown. Error bars indicate SEM. A, Alone condition; B, NEC condition; C, ST condition. Group PFo showed less other behaviors in the Alone condition and more mild aggression in the ST condition. For a more detailed description of behaviors, see Table 2. *Significantly different from both group Con and group Amyg. **Significantly different from group Con. Group Con, n = 10; group PFo, n = 3; group Amyg, n = 4.

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    Table 1.

    Percentage of damage to orbital prefrontal cortex (group PFo) and amygdala (group Amyg)

    Monkey Left Right Mean
    PFo-1 92.5 85.2 88.9
    PFo-2 76.1 62.2 69.2
    PFo-3 85.4 72.9 79.2
    PFo-4 85.0 70.0 77.5
    Amyg-1 100 100 100
    Amyg-2 98.5 98.5
    Amyg-3 94.7 77.3 86.0
    Amyg-4 100 70.4 85.2
    • Numerals indicate percentage of damage to orbital prefrontal cortex and amygdala sustained by each of the operated monkeys. PFo-1 to PFo-4, Monkeys with bilateral removals of the orbital prefrontal cortex by aspiration; Amyg-1 to Amyg-4, monkeys with excitotoxic amygdala lesions; Left, left hemisphere; Right, right hemisphere; Mean, average of the values for the left and right hemispheres.

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    Table 2.

    Behaviors analyzed during experiment 1 (snake task) and experiment 2 (human intruder task)

    Behavior Description
    Mild aggression
        Frown Wrinkles or moves eyebrows up and down
        Ears back Flattens ears against head
        Yawn Opens mouth wide, baring upper teeth
    High aggression
        Head/body lunge Thrusts head or body forward
        Cage shake Shakes cage
        Mouth threat Opens mouth slightly, exposing lower teeth
    Defense
        Freezing Motionless for ≥3 s
        Startle Jerks suddenly
        Eye/head aversion Avoids eye contact, shifts gaze or whole head
        Piloerection Hair stands on end
        Move away Retreats from the stimulus
    Submission
        Lip smack Purses and alternatively closes and opens lips
        Grimace Mouth closed, pulls lips backward exposing teeth
        Presentation Presents its hindquarters with tail up
    Approach
        Look at Makes eye contact
        Move toward Shifts body forward, closer to stimulus
        >Touch Handles with hand or foot
        Take/eat reward Picks up or mouths the food reward
    Other behaviors (not directed toward the stimulus)
        Manual exploration Handles any part of its surrounding
        Oral exploration Licks or mouths any part of its surrounding
        Locomotor stereotypies Activities, such as circling, hopping, repeated three or more times
        Self-directed activities Scratches, grooms, holds, etc. any part of its body
        Look away Looks away while engaged in behavior not directed toward stimulus
        Teeth gnashing Chewing motion without food in mouth
        Miscellaneous Engages in any peculiar activity not described above
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    Table 3.

    Summary of three-by-three-by-five ANOVA on food-retrieval latencies in experiment 1

    Fp value
    Group 10.572 0.001
    Trial type 13.149 <0.001
    Group-by-trial type 4.571 0.005
    Session 26.296 <0.001
    Trial type-by-session 7.031 <0.001
    Session-by-group 1.145 NS
    Trial type-by-session-by-group 0.806 NS
    • Resulting F and p values of a three (Con, Amyg, PFo)-by-three (snake, spider, neutral object)-by-five (session 1-5) ANOVA on food-retrieval latencies in experiment 1. NS, Not significant.

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The Journal of Neuroscience: 25 (37)
Journal of Neuroscience
Vol. 25, Issue 37
14 Sep 2005
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Comparison of the Effects of Bilateral Orbital Prefrontal Cortex Lesions and Amygdala Lesions on Emotional Responses in Rhesus Monkeys
Alicia Izquierdo, Robin K. Suda, Elisabeth A. Murray
Journal of Neuroscience 14 September 2005, 25 (37) 8534-8542; DOI: 10.1523/JNEUROSCI.1232-05.2005

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Comparison of the Effects of Bilateral Orbital Prefrontal Cortex Lesions and Amygdala Lesions on Emotional Responses in Rhesus Monkeys
Alicia Izquierdo, Robin K. Suda, Elisabeth A. Murray
Journal of Neuroscience 14 September 2005, 25 (37) 8534-8542; DOI: 10.1523/JNEUROSCI.1232-05.2005
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