Spreading depolarizations (SD) are waves of transient neuronal and glial depolarization that propagate across the cortical surface in response to certain stimuli or injury. During ischemia, SD-like peri-infarct depolarizations (PIDs) occur which can impair tissue by increasing disparity between CBF and metabolism. Despite the largest predictor of stroke in patients being advanced age, there are few studies examining PIDs in aged animals. In the current study we describe electrophysiological and hemodynamic changes in young (1-2 months), middle-aged (9 months) and old (24 months) male Wistar rats exposed to mild focal ischemia. A multi-modal imaging strategy allowed for the study of synchronous changes in: membrane potential, cerebral blood volume, local blood oxygen saturation, and cerebral blood flow (CBF). Multi-modal imaging of the rat cerebral cortex was achieved via closed cranial window mounted over the right parietal bone. Images were captured of the cortex illuminated with light-emitting diodes at wavelengths either preferentially absorbed by deoxygenated hemoglobin or isobestic for deoxygenated and oxygenated hemoglobin (representing total hemoglobin). Laser speckle contrast images and florescence images of a voltage sensitive dye (RH-1838) were also captured. The rats were continuously kept under halothane anesthesia and euthanized at the end of the experiments. A similar decrease in CBF was observed immediately following middle cerebral artery occlusion (MCAO) in young (53.8±8.1%), middle-aged (52.2±10.9%) and old rats (51.6±6.4%). Age significantly altered the total number of PIDs during and after MCAO and both middle-aged and old rats had significantly fewer PIDs than young (p<0.05). Depolarizations were categorized as follows: PIDs associated with membrane potential recovery (SD-like PIDs) and those without prompt recovery (terminal PIDs). Young animals had more frequent SD-like PIDs than middle-aged or old rats (p<0.05). Old animals experienced significantly fewer SD-like PIDs but more terminal PIDs than either middle-aged or young (p<0.05). Terminal PIDs were associated with a sustained reduction in local CBF (inverse hemodynamic response) but SD-like PIDs were associated with variable responses in CBF and hyperemia was associated with SD-like PIDs more frequently in young (85%) compared to old rats (58%). Age significantly altered the number, shape and hemodynamic responses of PIDs during mild stroke. Young animals had frequent PIDs, mostly associated with membrane repolarization and increased CBF. Old rats displayed frequent terminal depolarizations coupled with a lasting decrease in local blood flow. The occurrence of such depolarization events likely compromises the cortical tissue of aged animals exposed to even a short duration of focal ischemia.