Impairments in fear extinction memory and basolateral amygdala plasticity in the TgF344-AD rat model of Alzheimer’s disease are distinct from non-pathological aging

Author:

Hernandez Caesar M.ORCID,Jackson Nateka L.,Hernandez Abbi R.,McMahon Lori L.

Abstract

AbstractFear-based disorders such as posttraumatic stress disorder (PTSD) steepen age-related cognitive decline and doubles the risk for developing Alzheimer’s disease. Due to the seemingly hyperactive properties of fear memories, PTSD symptoms can worsen with age. Perturbations in the synaptic circuitry supporting fear memory extinction are key neural substrates of PTSD. The basolateral amygdala (BLA) is a medial temporal lobe structure critical in the encoding, consolidation, and retrieval of fear memories. As little is known about fear extinction memory and BLA synaptic dysfunction within the context of aging and AD, the goal of this study was to investigate how fear extinction memory deficits and basal amygdaloid nucleus (BA) synaptic dysfunction differentially associate in non-pathological aging and AD in the TgF344AD (TgAD) rat model of AD. Young, middle-aged, and older-aged WT and TgAD rats were trained on a delay fear conditioning and extinction procedure prior to ex vivo extracellular field potential recording experiments in the BA. Relative to young WT rats, long-term extinction memory was impaired, and in general, associated with a hyperexcitable BA and impaired LTP in TgAD rats at all ages. In contrast, long-term extinction memory was impaired in aged WT rats and associated with impaired LTP but not BA hyperexcitability. Interestingly, the middle-aged TgAD rats showed intact short-term extinction and BA LTP, suggestive of a compensatory mechanism, whereas differential neural recruitment in older-aged WT rats may have facilitated short-term extinction. As such, associations between fear extinction memory and amygdala deficits in non-pathological aging and AD are dissociable.SignificanceAdults with fear-based disorders like post-traumatic stress disorder are at an increased risk for developing age-related cognitive decline and Alzheimer’s disease (AD). Moreover, negative emotional affect is an early marker of AD. The link between fear-based disorders and AD creates a disadvantage for achieving positive outcomes later in life. Central to the circuitry underlying fear disorders are medial temporal lobe structures like the basal amygdaloid nucleus (BA). However, the role of the BA in fear-based disorders exacerbated by aging and AD is not well understood. Using the TgF344AD rat model of AD, we investigated how fear extinction memory impairments and BA synaptic function are impacted by aging and AD and whether these processes differentially associate in non-pathological aging and AD.

Publisher

Cold Spring Harbor Laboratory

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