Pavlovian fear conditioning is a ubiquitous form of learning that may underlie disorders of fear and anxiety (e.g., panic and post-traumatic stress disorder) in humans. Many studies indicate that the amygdala is required for both the acquisition and expression of fear conditioning in mammals, however, it is unclear to what extent the amygdala is involved in learning versus performing conditional fear. This issue must be addressed in order to fully understand the role of the amygdala in both emotional learning and anxiety disorders related to this form of learning. Thus, the present project consists of four specific aims to address this question. Multichannel single-unit recordings will be obtained from either the thalamic medial geniculate nucleus (MG), central amygdaloid nucleus (CE) or lateral amygdaloid nucleus (LA) during fear conditioning in behaving rats. These structures are critical components of the neural circuitry underlying fear conditioning to acoustic stimuli. Fear conditioning will be established by pairing an auditory conditional stimulus (CS) with an aversive footshock unconditional stimulus (US); freezing will serve as the measure of learned fear. The first specific aim examines CS-elicited single-unit activity in CE and LA under conditions in which learning and performance are uncoupled. Rats will receive fear conditioning in one context and latent inhibition or extinction training in a different context. Single unit activity in CE or LA will be recorded during behavioral testing in each of the contexts to assess CS-elicited responses under different levels of behavioral performance. The second specific aim assesses whether the development and expression of conditional unit activity in the MG requires neuronal activity in the CE or LA. During either training or testing, the CE or LA will be inactivated and single-unit activity in the MG will be recorded. The third specific aim examines whether there is behavioral or neuronal savings (i.e., learning that is not reflected in performance) following conditioning under amygdala inactivation. To test for savings, rats will be conditioned under amygdaloid inactivation in one phase of training and then conditioned with an intact amygdala in the following phase of training. The fourth specific aim examines the influence of overtraining on the amygdala s contribution to the learning and performance of conditional fear. Collectively, these experiments represent the first systematic attempt to elucidate the relative contribution of CE and LA amygdaloid neurons to learning versus performing conditional fear. The outcome of these experiments will have an important impact on current conceptions of both amygdaloid function and emotional learning and memory.
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