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Preserved stimulus-reward and reversal learning after selective neonatal orbital frontal areas 11/13 or amygdala lesions in monkeys.

ABSTRACT: Neither lesions of orbital frontal (OFC) areas 11/13 nor selective amygdala lesions alter the ability to learn stimulus-reinforcer association and reversal discriminations in adult monkeys. Here, we investigated whether the same conclusion will hold true when the same lesions occur in infancy. Infant rhesus monkeys received sham-operations, neurotoxic amygdala lesions, or aspiration OFC 11/13 lesions at 8-15 days of age and were trained on object discrimination reversal (ODR) tasks. Performance on a single pair (1-Pair) ODR was assessed at the age of 3 months and 3 years, and then animals were tested in a 5-Pair ODR task in which they had to concurrently learn and reverse five discrimination problems. The results indicated that the ability to solve a single-pair discrimination problem followed by six reversals appears to be late maturing in monkeys but is spared following selective lesions of either OFC areas 11/13 or amygdala, even with the use of the more challenging 5-object ODR task. Finally, performance in the 1 and 5-Pair ODR at 3 years was comparable to that following adult-onset lesions, indicating that neither OFC areas 11/13 nor amygdala are critical for the development of reversal learning.

SUBMITTER: Kazama AM

PROVIDER: S-EPMC3369024 | biostudies-literature | 2012 Jul

REPOSITORIES: biostudies-literature

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Preserved stimulus-reward and reversal learning after selective neonatal orbital frontal areas 11/13 or amygdala lesions in monkeys.

Kazama Andy M AM Bachevalier Jocelyne J

Developmental cognitive neuroscience 20120324 3

Neither lesions of orbital frontal (OFC) areas 11/13 nor selective amygdala lesions alter the ability to learn stimulus-reinforcer association and reversal discriminations in adult monkeys. Here, we investigated whether the same conclusion will hold true when the same lesions occur in infancy. Infant rhesus monkeys received sham-operations, neurotoxic amygdala lesions, or aspiration OFC 11/13 lesions at 8-15 days of age and were trained on object discrimination reversal (ODR) tasks. Performance ...[more]

PMID: 22494813

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Project description:Orbitofrontal cortex (OFC), medial frontal cortex (MFC), and amygdala mediate stimulus-reward learning, but the mechanisms through which they interact are unclear. Here, we investigated how neurons in macaque OFC and MFC signaled rewards and the stimuli that predicted them during learning with and without amygdala input. Macaques performed a task that required them to evaluate two stimuli and then choose one to receive the reward associated with that option. Four main findings emerged. First, amygdala lesions slowed the acquisition and use of stimulus-reward associations. Further analyses indicated that this impairment was due, at least in part, to ineffective use of negative feedback to guide subsequent decisions. Second, the activity of neurons in OFC and MFC rapidly evolved to encode the amount of reward associated with each stimulus. Third, amygdalectomy reduced encoding of stimulus-reward associations during the evaluation of different stimuli. Reward encoding of anticipated and received reward after choices were made was not altered. Fourth, amygdala lesions led to an increase in the proportion of neurons in MFC, but not OFC, that encoded the instrumental response that monkeys made on each trial. These correlated changes in behavior and neural activity after amygdala lesions strongly suggest that the amygdala contributes to the ability to learn stimulus-reward associations rapidly by shaping encoding within OFC and MFC.SIGNIFICANCE STATEMENT Altered functional interactions among orbital frontal cortex (OFC), medial frontal cortex (MFC), and amygdala are thought to underlie several psychiatric conditions, many related to reward learning. Here, we investigated the causal contribution of the amygdala to the development of neuronal activity in macaque OFC and MFC related to rewards and the stimuli that predict them during learning. Without amygdala inputs, neurons in both OFC and MFC showed decreased encoding of stimulus-reward associations. MFC also showed increased encoding of the instrumental responses that monkeys made on each trial. Behaviorally, changes in neural activity were accompanied by slower stimulus-reward learning. The findings suggest that interactions among amygdala, OFC, and MFC contribute to learning about stimuli that predict rewards.

Dataset Information

Preserved stimulus-reward and reversal learning after selective neonatal orbital frontal areas 11/13 or amygdala lesions in monkeys.

Publications

Preserved stimulus-reward and reversal learning after selective neonatal orbital frontal areas 11/13 or amygdala lesions in monkeys.

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