The frontal cortex and temporal lobes together regulate complex learning and memory capabilities. Here, we collected resting-state functional and diffusion-weighted MRI data before and after male rhesus macaque monkeys received extensive training to learn novel visuospatial discriminations (reward-guided learning). We found functional connectivity changes in orbitofrontal, ventromedial prefrontal, inferotemporal, entorhinal, retrosplenial, and anterior cingulate cortices, the subicular complex, and the dorsal, medial thalamus. These corticocortical and thalamocortical changes in functional connectivity were accompanied by related white matter structural alterations in the uncinate fasciculus, fornix, and ventral prefrontal tract: tracts that connect (sub)cortical networks and are implicated in learning and memory processes in monkeys and humans. After the well-trained monkeys received fornix transection, they were impaired in learning new visuospatial discriminations. In addition, the functional connectivity profile that was observed after the training was altered. These changes were accompanied by white matter changes in the ventral prefrontal tract, although the integrity of the uncinate fasciculus remained unchanged. Our experiments highlight the importance of different communication relayed among corticocortical and thalamocortical circuitry for the ability to learn new visuospatial associations (learning-to-learn) and to make reward-guided decisions.
Highlights
Refining training for monkeys in neuroscience is essential to optimise their welfare.
Refinements still produce high quality science.
Pair- or group-training monkeys helps acclimate them quicker to transport devices.
Commencing positive reinforcement training on arrival facilitates acclimation.
Negative reinforcement techniques used effectively are also sometimes necessary.
Human functional magnetic resonance imaging (fMRi) typically employs the blood-oxygen-leveldependent (BoLD) contrast mechanism. in non-human primates (nHp), contrast enhancement is possible using monocrystalline iron-oxide nanoparticles (Mion) contrast agent, which has a more temporally extended response function. However, using BoLD fMRi in nHp is desirable for interspecies comparison, and the BOLD signal's faster response function promises to be beneficial for rapid event-related (reR) designs. Here, we used reR BoLD fMRi in macaque monkeys while viewing realworld images, and found visual responses and category selectivity consistent with previous studies. However, activity estimates were very noisy, suggesting that the lower contrast-to-noise ratio of BoLD, suboptimal behavioural performance, and motion artefacts, in combination, render reR BoLD fMRi challenging in nHp. previous studies have shown that reR fMRi is possible in macaques with Mion, despite Mion's prolonged response function. to understand this, we conducted simulations of the BoLD and Mion response during reR, and found that no matter how fast the design, the greater amplitude of the Mion response outweighs the contrast loss caused by greater temporal smoothing. We conclude that although any two of the three elements (reR, BoLD, nHp) have been shown to work well, the combination of all three is particularly challenging.
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