The smell of fear: comparing the neural ensembles underlying odor fear memory conditioned by innate, inherent, and learned sources of danger

Carew, Samantha J. (2023) The smell of fear: comparing the neural ensembles underlying odor fear memory conditioned by innate, inherent, and learned sources of danger. Doctoral (PhD) thesis, Memorial University of Newfoundland.

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Abstract

Memories can elicit strong emotions, both positive and aversive. Recognizing danger cues in an unfamiliar environment can make the difference between life and death. However, if aversive memory formation becomes dysregulated, safe cues can be misinterpreted as danger signals and lead to avoidance, fear reactions, and other maladaptive behaviours. Rats are utilized as model organisms in combination with classical conditioning to delineate mechanisms underlying aversive memories, but human memory is diverse and complicated. This thesis utilized two forms of “higher-order” learning, pheromone- and second-order conditioning, to recapitulate the diverse ways that humans employ associative learning. Alarm pheromones released from a stressed rat can act as an unconditioned stimulus when paired with a neutral odor to produce an odor fear memory in a conspecific. The basolateral (BLA) and central amygdala are consistently activated across shock- and pheromone-conditioned odor memory recall, but pheromone-conditioned and shock-conditioned memories elicit activation in the accessory olfactory bulb and main olfactory bulb, respectively. Rats can also learn that an odor signals danger when it is paired with a tone or context that was previously paired with shock. First-order conditioned and both forms of second-order conditioned odor memory recall elicit activation in the BLA, the dorsal and ventral hippocampus, and the olfactory cortex. Interestingly recall of an odor fear memory that was conditioned with a feared tone activates the lateral amygdala and auditory cortex. Overall, the results described in this thesis highlight that odor fear memory traces are present in some areas regardless of how the memory was conditioned, while other areas participate in memory traces differentially, possibly depending on sensory features of the conditioned stimuli. Elucidating the mechanisms underlying higher-order conditioning are crucial and could provide valuable insight for treatment of disorders involving aberrant fear, such as post traumatic stress disorder, which currently focus on exposure to faulty danger cues to rewrite traumatic memories.

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