Although PTSD and cognitive dysfunction are frequent comorbidities of chronic traumatic brain injury (TBI) in Veterans, the neurophysiological basis of how TBI affects these processes remains unknown. In addition, there are currently no effective treatments available for these prevalent, severely disabling comorbidities. The limbic system, including the hippocampus, amygdala, and regions of the prefrontal cortex, underlies fear acquisition and extinction, as well as many aspects of learning and memory. An exaggerated fear response is thought to be essential to the pathophysiology of PTSD, as well as an associated lack of extinction of fear responses. Extinction, rather than a “forgetting” of the trigger and response, has been demonstrated to be a different form of learning, with new circuits over-riding existing fear responses. A number of studies in humans and rodents have demonstrated that TBI can exacerbate fear responses, while also diminishing the ability to extinguish fearful associations. Tremendous advances have recently been made in understanding how the memory of fear and associated aspects such as contextual information is encoded in the amygdala and its associated neural networks, how neuronal activity in this network interacts with oscillations to encode information, and how fear related memories are recalled and extinguished. Surprisingly, however, there have been few reports to date of how the neurophysiological mechanisms of fear encoding, recall, and extinction are affected by chronic TBI. Elucidating the mechanisms by which TBI affects the circuitry encoding fear learning and extinction in the amygdala and associated brain regions will lead to better targeted treatments, including neuromodulation, for PTSD comorbid with TBI and other learning-associated cognitive dysfunction. Treating PTSD with Deep Brain Stimulation (DBS, a form of neuromodulation) is being tested in Veterans, and it is essential to develop animal models of this clinical intervention, including the potential influence of TBI on behavioral outcomes. Therefore, the overall objective of the current application is to determine how the encoding of fear in extended amygdalar circuitry is exacerbated following TBI, and to utilize electrical stimulation to restore normal balance to this system, enhancing extinction and potentially restoring cognition. As the limbic system underlies many forms of cognition, learning and memory, this may have broader implications in chronic TBI as well. Our central hypothesis is that TBI disrupts normal communication between the amygdala and the hippocampus underlying fear associated memory which leads to overexpression of fear responses, an inability to extinguish learned fear in chronic TBI, and that this network imbalance can be rectified with neuromodulation. We will test the above hypotheses first by determining the effects of chronic TBI-induced disruption on the circuitry underlying fear responses and cognitive tasks in rats using...