Graduation Year


Document Type




Degree Granting Department


Major Professor

David Diamond, Ph.D.

Committee Member

Mark Goldman, Ph.D.

Committee Member

Cheryl Kirstein, Ph.D.

Committee Member

Ken Malmberg, Ph.D.

Committee Member

Keith Pennypacker, Ph.D.


Learning, emotion, hippocampus, amygdala, extinction


This series of experiments developed novel paradigms involving the integration of conventional and ethologically relevant forms of reinforcement in the study of fear conditioning in rats. Experiment 1 compared the effects of foot shock, immobilization and predator exposure, alone and in combination, on the expression of conditioned fear memory and extinction. The combination of all 3 reinforcers produced a significantly stronger fear memory and greater resistance to extinction, compared to when each reinforcer was administered alone. Furthermore, whereas conditioning with foot shock, alone, resulted in rapid extinction of the fear memory, the combination of immobilization and cat exposure, or all 3 reinforcers together, produced a robust extinction resistant fear memory. Experiment 2 explored the effects of giving extinction trials every two versus every seven days. This experiment demonstrated extinction when the trials were given every 2 days, with no evidence of extinction when trials were given every 7 days. Experiment 3 focused on extending predator-based conditioning to enhance the development of cue-based fear conditioning. Rats were administered multiple predator-based conditioning trials in one session to enhance the formation of both contextual and cue-based fear memories. Experiment 4 tested the hypothesis that hippocampal involvement during learning is necessary for predator-based contextual, but not cued, fear memory. This work provided support for this hypothesis with the finding of impaired contextual memory, with no effect on cued memory, in rats that had a pharmacological suppression of hippocampal activity during fear conditioning. Experiment 5 developed an entirely novel form of inhibitory avoidance conditioning. This work demonstrated that rats learned to avoid entering a place which was paired with immobilization and predator exposure. Experiment 6 investigated the effects of sleep deprivation occurring prior to fear conditioning on the expression of fear memory. This experiment showed that pre-training sleep deprivation blocked the development of contextual (hippocampal-dependent), but not cue (hippocampal-independent), fear memory. Overall, this series of experiments established the groundwork to use ethologically relevant stimuli, including predator exposure, in conjunction with conventional reinforcers, such as foot shock and immobilization, to advance our understanding of the neurobiology of emotional memory.