Cerebellar dentate nucleus lesions in monkey reveal both a motor-cognitive dichotomy and within-cognition dichotomy of dorsal vs ventral stream processing.

The dysmetria of thought theory holds that the cerebellum is an integral node in the distributed neural circuits subserving cognition. We tested this theory in four rhesus monkeys with bilateral lesions in cerebellar dentate nuclei (DN), targeting ventral sectors linked with cerebral association cortices engaged in cognitive processing. Lesion localization was confirmed by MRI and histology. DN animals and controls were assessed for motor dexterity (Kuypers' Task), attention, three-choice discrimination, recognition memory (Delayed Non-Matching to Sample task [DNMS]), working memory (Delayed Recognition Span Task [DRST]) and executive function (Conceptual Set Shifting Task [CSST]). Performance by the DN animals was not significantly different than controls on the Kuypers' task and DNMS, but as a group they were impaired on DRST and CSST. DN monkeys achieved shorter spans on DRST. Their responses on CSST were more perseverative, and larger lesions produced greater deficits. This study provides the first empirical support for anatomical and functional MRI evidence of a motor-cognitive dichotomy in the cerebellar dentate nucleus. It highlights a within-cognition dichotomy in which cerebellum modulates dorsal stream cognitive functions (spatial awareness; dynamic actions of where and how) characterized by executive functions including working memory but is not engaged in ventral stream cognitive processes (static actions of object identification) exemplified by recognition memory.