Age-related cognitive decline is related to cellular and systems-level disruptions across multiple brain regions. Because age-related cellular changes within different structures do not show the same patterns of dysfunction, interventions aimed at optimizing function of large-scale brain networks may show greater efficacy at improving cognitive outcomes in older adults than traditional pharmacotherapies. The current study aimed to leverage a preclinical rat model of aging to determine whether cognitive training in young and aged male rats with a computerized paired-associates learning (PAL) task resulted in changes in global resting-state functional connectivity. Moreover, seed-based functional connectivity was used to examine resting state connectivity of cortical areas involved in object-location associative memory and vulnerable in old age, namely the medial temporal lobe (hippocampal cortex and perirhinal cortex, or PRC), retrosplenial cortex (RSC), and frontal cortical areas (prelimbic, or PRL, and infralimbic cortices). There was an age-related increase in global functional connectivity between baseline and post-training resting state scans in aged, cognitively trained rats. This change in connectivity following cognitive training was not observed in young animals, or rats that traversed a track for a reward between scan sessions. Relatedly, an increase in connectivity between PRC and PRL, as well as reduced reciprocal connectivity within the RSC, was found in aged rats that underwent cognitive training, but not the other groups. Subnetwork activation was associated with task performance across age groups. Greater global functional connectivity and connectivity between task-relevant brain regions may elucidate compensatory mechanisms that can be engaged by cognitive training.Significance StatementCognitive impairments in advanced age have been linked to reduced resting state functional connectivity in humans and rats. Resting state functional connectivity is typically examined at a single time point. Thus, little is known regarding the robust versus adaptive properties of these networks in old age. The current study reports longitudinal changes in global connectivity as well as connectivity involving the medial temporal, frontal, and retrosplenial cortices in aged rats that were trained on a rodent touchscreen version of the paired associates learning task. This work is significant because it shows that the functional organization of brain networks in aged rats is adaptive, and this could be leveraged to design behavioral therapies for improving cognitive function in old age.