Department of Experimental Psychology, University of Oxford, Oxford OX1 3SR, United Kingdom.
Laboratory for Neuro- and Psychophysiology, KU Leuven, 3000 Leuven, Belgium.
J Neurosci. 2020 Oct 7;40(41):7887-7901. doi: 10.1523/JNEUROSCI.0364-20.2020. Epub 2020 Sep 8.
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. Frontal neural networks and the temporal lobes contribute to reward-guided learning in mammals. Here, we provide novel insight by showing that specific corticocortical and thalamocortical functional connectivity is altered after rhesus monkeys received extensive training to learn novel visuospatial discriminations. Contiguous white matter fiber pathways linking these gray matter structures, namely, the uncinate fasciculus, fornix, and ventral prefrontal tract, showed structural changes after completing training in the visuospatial task. Additionally, different patterns of functional and structural connectivity are reported after removal of subcortical connections within the extended hippocampal system, via fornix transection. These results highlight the importance of both corticocortical and thalamocortical interactions in reward-guided learning in the normal brain and identify brain structures important for memory capabilities after injury.
前额叶皮层和颞叶共同调节复杂的学习和记忆能力。在这里，我们在雄性恒河猴接受广泛的训练以学习新的视觉空间辨别（奖励引导学习）前后收集了静息状态功能和扩散加权 MRI 数据。我们发现眶额、腹内侧前额叶、下颞叶、内嗅皮质、后扣带回和前扣带回皮质、海马旁回复合体以及背侧、内侧丘脑的功能连接发生了变化。这些功能连接的皮质间和皮质下变化伴随着联合纤维、穹窿和腹侧前额叶束的相关白质结构改变：这些束连接（皮质下）网络，与猴子和人类的学习和记忆过程有关。在经过良好训练的猴子接受穹窿切开术后，它们在学习新的视觉空间辨别方面受损。此外，观察到的训练后功能连接模式发生了改变。这些变化伴随着腹侧前额叶束的白质变化，尽管联合纤维束的完整性保持不变。我们的实验强调了不同的皮质间和皮质下回路之间的通讯对学习新的视觉空间联想（学习学习）和做出奖励引导决策的能力的重要性。前额叶神经网络和颞叶有助于哺乳动物的奖励引导学习。在这里，我们通过显示特定的皮质间和皮质下功能连接在恒河猴接受广泛训练以学习新的视觉空间辨别后发生改变，提供了新的见解。连接这些灰质结构的连续白质纤维通路，即联合纤维束、穹窿和腹侧前额叶束，在完成视觉空间任务的训练后显示出结构变化。此外，在通过穹窿切开术去除扩展海马系统内的皮质下连接后，报告了不同的功能和结构连接模式。这些结果强调了正常大脑中奖励引导学习中皮质间和皮质下相互作用的重要性，并确定了受伤后记忆能力的重要脑结构。
