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Selective Bilateral Amygdala Lesions in Rhesus Monkeys Fail to Disrupt Object Reversal Learning
Open accessAbstract
Neuropsychological studies in nonhuman primates have led to the view that the amygdala plays an essential role in stimulus–reward association. The main evidence in support of this idea is that bilateral aspirative or radiofrequency lesions of the amygdala yield severe impairments on object reversal learning, a task that assesses the ability to shift choices of objects based on the presence or absence of food reward (i.e., reward contingency). The behavioral effects of different lesion techniques, however, can vary. The present study therefore evaluated the effects of selective, excitotoxic lesions of the amygdala in rhesus monkeys on object reversal learning. For comparison, we tested the same monkeys on a task known to be sensitive to amygdala damage, the reinforcer devaluation task. Contrary to previous results based on less selective lesion techniques, monkeys with complete excitotoxic amygdala lesions performed object reversal learning as quickly as controls. As predicted, however, the same operated monkeys were impaired in making object choices after devaluation of the associated food reinforcer. The results suggest two conclusions. First, the results demonstrate that the amygdala makes a selective contribution to stimulus–reward association; the amygdala is critical for guiding object choices after changes in reward value but not after changes in reward contingency. Second, the results implicate a critical contribution to object reversal learning of structures nearby the amygdala, perhaps the subjacent rhinal cortex.
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“As illustrated in Figure 3A (pink), monkeys with bilateral amygdala lesions typically fail to show the devaluation effect or show it only in a strongly attenuated form.”
From Localization of Dysfunction in Major Depressive Disorder: Prefrontal Cortex and Amygdala (2011) · cites this paper as [75]
In the citing paper
“Intact, control monkeys tend to avoid choosing objects associated with the devalued food, a finding called the ‘devaluation effect’.”
From Localization of Dysfunction in Major Depressive Disorder: Prefrontal Cortex and Amygdala (2011) · cites this paper as [75]
In the citing paper
“The monkeys chose objects according to their original preferences, with less influence of their selectively satiated state than in intact monkeys.”
From Localization of Dysfunction in Major Depressive Disorder: Prefrontal Cortex and Amygdala (2011) · cites this paper as [75]
In the citing paper
“The same groups of operated monkeys showed little or no change in food preferences and worked for food like control monkeys.”
From Localization of Dysfunction in Major Depressive Disorder: Prefrontal Cortex and Amygdala (2011) · cites this paper as [75]
In the citing paper
“The red curve in Figure 4A illustrates that selective bilateral amygdala lesions have no effect on learning these object-reward reversals (75, 91).”
From Localization of Dysfunction in Major Depressive Disorder: Prefrontal Cortex and Amygdala (2011) · cites this paper as [75]
In the citing paper
“Some monkeys received bilateral PFo ablations (blue) and others received a crossed surgical disconnection (green) of the amygdala and PFo (a unilateral amygdala lesion in one hemisphere along with unilateral PFo lesion in the other hemisphere, combined with section of the forebrain commissures). In all lesion groups, the devaluation effect was markedly attenuated.”
From Localization of Dysfunction in Major Depressive Disorder: Prefrontal Cortex and Amygdala (2011) · cites this paper as [75]
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Citations
Cites
Preliminary analysis of functions of the temporal lobes in monkeys
KLÜVER, H. (1939) · Archives of Neurology And Psychiatry · doi:10.1001/archneurpsyc.1939.02270240017001 · Cited by 1,696 · cited 4×
“Although abnormal food “preferences” follow large, nonselective lesions that include the amygdala (Klüver and Bucy, 1939; Pribram and Bagshaw, 1953; Weiskrantz, 1956) (see also Baylis and Gaffan, 1991), these altered preferences likely reflect the flattening of choices between foods and nonfoods, or between preferred…”
InfluentialNeurons in the orbitofrontal cortex encode economic value
Padoa-Schioppa, C., & Assad, J. A. (2006) · Nature · doi:10.1038/nature04676 · Cited by 1,598
Relative reward preference in primate orbitofrontal cortex
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Multiple Parallel Memory Systems in the Brain of the Rat
White, N. M., & McDonald, R. J. (2002) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2001.4008 · Cited by 933
Limbic lesions and the problem of stimulus--reinforcement associations.
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Behavioral changes associated with ablation of the amygdaloid complex in monkeys.
Weiskrantz, L. (1956) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0088009 · Cited by 837
Wallis, J. D., & Miller, E. K. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02922.x · Cited by 614
Izquierdo, A., Suda, R. K., & Murray, E. A. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.1921-04.2004 · Cited by 588
Self-citationBaxter, M. G., Parker, A., Lindner, C. C. C., Izquierdo, A. D., & Murray, E. A. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-11-04311.2000 · Cited by 582
Self-citation
Research works printed but not linked: 4
- Baxter, 1998, Aspiration lesions of the amygdala interrupt connections between prefrontal cortex and temporal cortex in rhesus monkeys, Soc Neurosci Abstr, 24, 757
- Izquierdo, 2004, Mediodorsal nucleus of the thalamus contributes to reinforcer devaluation effects in rhesus monkeys, Soc Neurosci Abstr, 30, 84
- Munoz, 2001, Medial temporal removals disconnect rostral superior temporal gyrus from frontal cortex, Soc Neurosci Abstr, 27, 535
- Murray EA (1992) in The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction, Medial temporal lobe structures contributing to recognition memory: the amygdaloid complex versus the rhinal cortex, ed Aggleton JP (Wiley, New York), pp 453–470.
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Sorted by citations
The ventral visual pathway: an expanded neural framework for the processing of object quality
Kravitz, D. J., Saleem, K. S., Baker, C. I., Ungerleider, L. G., & Mishkin, M. (2012) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2012.10.011 · Cited by 1,204
What does the amygdala contribute to social cognition
Adolphs, R. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2010.05445.x · Cited by 836
The amygdala, reward and emotion
Murray, E. A. (2007) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2007.08.013 · Cited by 679
Self-citationEmotion, Cognition, and Mental State Representation in Amygdala and Prefrontal Cortex
Salzman, C. D., & Fusi, S. (2010) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135256 · Cited by 628
A new perspective on the role of the orbitofrontal cortex in adaptive behaviour
Schoenbaum, G., Roesch, M. R., Stalnaker, T. A., & Takahashi, Y. K. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2753 · Cited by 585
Metadata
- Authors
- Izquierdo, A., & Murray, E. A.
- Affiliations
- National Institutes of Health (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2007-01-31
- Volume
- 27
- Issue
- 5
- Pages
- 1054-1062
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6673199
- OpenAlex
- W2014284272
- Cited by
- 121
- References
- 49
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 2 · 2023: 1 · 2022: 4 · 2021: 8 · 2020: 4 · 2019: 3 · 2018: 3 · 2017: 5 · 2016: 4 · 2015: 7 · 2014: 3 · 2013: 9 · 2012: 8
- FWCI
- 7.16
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Soochow University
- National Institutes of Health
- National Institute of Mental Health
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- amygdala, excitotoxic lesions, rhesus monkeys, stimulus-reward associations, reinforcer devaluation, reward contingency, rhinal cortex, reward-guided behavior
- MeSH terms
- Amygdala, Animals, Choice Behavior, Functional Laterality, Macaca mulatta, Male, Reinforcement, Psychology, Reversal Learning
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