Corticocortical and Thalamocortical Changes in Functional Connectivity and White Matter Structural Integrity after Reward-Guided Learning of Visuospatial Discriminations in Rhesus Monkeys.

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.SIGNIFICANCE STATEMENT 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.

Semantic and emotional content of imagined representations in human occipitotemporal cortex.

Mental imagery is a critical cognitive function, clinically important, but poorly understood. When visual objects are perceived, many of their sensory, semantic and emotional properties are represented in occipitotemporal cortex. Visual imagery has been found to activate some of the same brain regions, but it was not known what properties are re-created in these regions during imagery. We therefore examined the representation during imagery for two stimuli in depth, by comparing the pattern of fMRI response to the patterns evoked by the perception of 200 diverse objects chosen to de-correlate their properties. Real-time, adaptive stimulus selection allowed efficient sampling of this broad stimulus space. Our experiments show that occipitotemporal cortex, which encoded sensory, semantic and emotional properties during perception, can robustly represent semantic and emotional properties during imagery, but that these representations depend on the object being imagined and on individual differences in style and reported vividness of imagery.

Concurrent brain responses to separate auditory and visual targets.

In the attentional blink, a target event (T1) strongly interferes with perception of a second target (T2) presented within a few hundred milliseconds. Concurrently, the brain's electromagnetic response to the second target is suppressed, especially a late negative-positive EEG complex including the traditional P3 wave. An influential theory proposes that conscious perception requires access to a distributed, frontoparietal global workspace, explaining the attentional blink by strong mutual inhibition between concurrent workspace representations. Often, however, the attentional blink is reduced or eliminated for targets in different sensory modalities, suggesting a limit to such global inhibition. Using functional magnetic resonance imaging, we confirm that visual and auditory targets produce similar, distributed patterns of frontoparietal activity. In an attentional blink EEG/MEG design, however, an auditory T1 and visual T2 are identified without mutual interference, with largely preserved electromagnetic responses to T2. The results suggest parallel brain responses to target events in different sensory modalities.