Although T cells aid in maintaining homeostasis of the normal central nervous system (CNS), the significant trafficking of T cells to the CNS under conditions of pathology, infection, or injury presents a dichotomy. The presence of T cells in the CNS under certain contexts is considered detrimental, where T cells have been shown to cause or exacerbate neuropathology. Under certain experimentally-induced conditions, however, T cells have been shown to confer neuroprotection. In the interest of developing immune-based strategies to treat neurodegenerative disease or CNS injury, it is important to understand the conditions that drive T cells to act in a bi-directional manner in the CNS. To begin to address this issue, we used the well-characterized facial nerve axotomy model to study the interactions between T cells, microglia, and injured neurons. We demonstrated that the level of neuronal death can influence the magnitude and rate of T cell accumulation to the injured CNS. Moreover, T cells that are exposed to neuronal injury in early adulthood possess the ability to exhibit memory and increase their responsiveness to the same form of injury induced later in life. Although we found that the presence of T cell memory in the injured FMN was associated with modest effects on functional recovery, there was no obvious impact on measures of neuronal survival. The lack of effect on neuronal survival may have been due to the inability to detect a population of neurons that have been shown in previous studies to undergo severe atrophy and shrinkage following axotomy. It was also shown in those studies that the atrophic neurons possess the capacity to regenerate (i.e., reverse atrophy as demonstrated by the increase in neuronal cell number and size) following nerve re-injury. Using this nerve re-injury model, we found that immunodeficiency impaired the regenerative response of injured facial motor neurons but that T cells were not associated with the reversal of atrophy in wild-type mice. We propose that T cells respond to the neuronal death induced by injury and aid in promoting the long-term survival of the surrounding neurons by maintaining them in an atrophied state where they can be prompted to regenerate. Our findings provide intriguing information regarding the impact of T cells on the status of injured neurons, which may have important implications for the future development of treatment strategies that could aid in the prolonged survival of the neuron following injury.