Task-dependent visual topographic connectivity in the human cerebellum

The role of the cerebellum has long been thought to be limited to sensorimotor processes. Recently, its involvement in a broader set of cognitive and associative tasks has challenged this view. Recent studies have expanded the cerebellum's functional repertoire into the visual domain, by identifying 3 topographically organized clusters exhibiting visual-spatial responses using the population receptive field (pRF)-model. In this experiment, researchers used a simple retinotopic mapping stimulus during strict fixation. This represents a situation very different from our everyday vision, which is characterized by continual eye movements, and a complex naturalistic visual stimulation. This makes it hard to translate the previous results to natural, active vision. Here, we used topographic connectivity from V1 to investigate the visual topographic organization in the human cerebellum (of either sex), and its dependence on cognitive state (comparing movie watching and resting state experiments). We find that movie watching evokes visual representations with a clear eccentricity gradient in OMV that was not found in a simple retinotopic mapping experiment. We furthermore discovered a novel topographically organized area in the cerebellum, again evoked specifically during movie watching and not in resting state. This latter area is located in the cerebellar Crus II area and falls within regions usually assigned to the cerebellar default mode network. Our results show that we can reveal task-dependent properties of the visual organization when using different cognitive states and how this can provide information about the processing of visual information, also in regions not previously considered to be visually responsive.Significance statement We used the connective field (CF) model to investigate topographic visual organization in the cerebellum and its dependence on cognitive state. Previous work found three clusters with topographic maps of visual space in the cerebellum. The CF model allowed us to first reproduce and then extend these maps, and study task effects on the visual-topographic organization of the human cerebellum. First, we demonstrate previously unseen visual field eccentricity gradient in the oculomotor vermis, present only during naturalistic movie watching. Furthermore, naturalistic movie watching uncovered an additional topographically organized cluster in Crus II. These results show that the topographical organization is flexible across tasks, and underline the importance of using naturalistic stimuli to probe high-level visual-topographic function.