Neurological decline associated with non-pathological aging is fast becoming a primary concern of Western societies as we are beginning to feel the social, monetary and emotional pressures of an aging population. It is evident that the aging nervous system, whether invertebrate or vertebrate, suffers from a progressive deterioration of plastic components, most noticeably that of learning and memory. While this process likely has a diverse and multifactorial cellular and molecular foundation, one of the foremost mechanistic explanations is captured within the Free Radical Theory of Aging. The theory postulates that senescence is the result of progressive pro-oxidative shifts in cellular redox states and consequential oxidation-dependent alterations in cell physiology. While we are beginning to quantify these changes, it is often difficult to distinguish the adaptive from the maladaptive when considering how molecular changes within the neuron correspond to whole animal neuronal functionality. Using an invertebrate model with a rich history in neurobiology and aging research, the following thesis attempts to bridge this gap in our understanding by investigating the relationship between age-related changes in metabolism, cellular oxidation states, neuronal (electro) physiology and whole animal cognitive performance. My findings implicate age-related changes in metabolism and concurrent glutathione-dependent pro-oxidative shifts in cellular redox states, to be a foundational mechanism behind age-dependent neuronal hypoexcitability and the concurrent behavioural manifestation of long term memory impairment. Moreover, this work pinpoints oxidation-dependent provocation of phospholipase A2, and the resultant release of free fatty acids, to be the molecular fulcrum through which changing cellular oxidation states are translated into electrophysiological and behavioural consequences for the animal. These findings build on a growing body of evidence describing a central role for oxidative stress and perturbed lipid metabolism in neuronal excitability control and age-associated perturbations in cognitive performance. Taken together, the fundamental molecular processes described within this thesis support the optimistic view that the mechanisms of non-pathological aging may suspend rather than irreversibly extinguish the aging brain’s plastic capacity.