There is substantial scientific interest in improving approaches that can enhance cognition through brain stimulation. We implemented a non-invasive focal Transcranial Ultrasound Stimulation (TUS) approach with known longer-lasting post-stimulation effects in two rhesus macaques performing a context-dependent memory-sequencing task implemented on multiple touchscreens within their home units. Consistently in both monkeys, TUS to the anterior - but not posterior - medial temporal lobe enhanced performance under stable memory-sequencing contexts. TUS to the medial prefrontal cortex, on the other hand, selectively improved performance when contexts were unstable and the monkey needed to adapt to both a change in context and temporal sequence. These findings shed new light on fronto-temporal nodes that, when perturbed, can selectively enhance cognitive performance, paving the way for further developing non-invasive approaches to improve cognitive function in humans and to study neural circuits under focal perturbation across species.