Dysfunction in neural circuits underlying emotional processes causes symptoms in a variety of neuropsychiatric disorders, including depression, anxiety disorders, schizophrenia, and drug abuse. Much work in animals and humans has implicated the amygdala in these emotional processes. In primates, however, amygdala neurophysiology has received limited attention, especially with regard to emotional learning. We propose using classical conditioning techniques so that monkeys learn the value of novel visual (Aim 1) or auditory (Aim 2) conditioned stimuli (CS). We assign CSs a value by arbitrarily pairing each CS with unconditioned stimuli (US): liquid reward (positive), air-puff (negative), or no reinforcement. Monkeys demonstrate their learning with two responses: anticipatory licking for rewarded CSs, and anticipatory blinking, a defensive behavior, for negative CSs. We will record the activity of individual amygdala neurons in monkeys as they learn the value of the CSs. Theories of reinforcement learning posit that learning depends upon updating a neural representation of CS value, a process that is driven by error signals indicating the difference between expected and actual reinforcement. We hypothesize that amygdala neurons code the value of CSs, and that this representation is rapidly updated during learning. Furthermore, we hypothesize that amygdala neurons will respond differentially to unexpected compared to expected reinforcement, indicating that amygdala activity reflects error signals. Finally, we hypothesize that neurons whose activity reflects error signals are more likely to also encode CS value.
In Aim 3, we seek to determine whether neural signals reflecting CS value during classical conditioning are best interpreted as coding for CS value or for expected reinforcement, which in more complex paradigms is not necessarily aligned with CS value. In classical conditioning studies, it is not possible to disambiguate these interpretations because CS value always predicts trial outcome. We will use an occasion setting paradigm in which expected outcome is manipulated by presenting a cue transiently before CS onset on a subset of probe trials, while maintaining individual CS value with regular conditioning trials. We will then determine if amygdala neurons represent CS value or expected outcome. These studies have direct relevance to public health, since these neural circuits dysfunction in many psychiatric disorders, including addiction, depression, and schizophrenia.
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