Neocortex–Cerebellum Circuits for Cognitive Processing

Classic studies have mainly focused on sensorimotor information transmitted through the two cerebellar input pathways, granule cells and climbing fibers. Recent investigations indicate that the cerebellum receives diverse reward expectation-related information via granule cells, and reward prediction error signals via climbing fibers. The cerebellum may in turn reciprocally influence brain-wide reward circuitry via output pathways from the cerebellar nuclei. Prevailing theories of cerebellar function posit that the granule cell layer generates a dimensionally expanded representation of its mossy fiber inputs. Recent observations in multiple contexts and species indicate that granule cells may perform a richer set of functions, including the faithful transmission of neocortical neuronal dynamics to the cerebellar circuit. Similarly, classical views of climbing fibers as reporting movement errors have broadened to incorporate instructive signals that might drive more flexible and varied types of reinforcement learning. Recent experiments also identified a critical role for cerebellar output in sustaining cortical preparative activity that underlies cognitive and working memory processes. Thus, the neocortex–cerebellum circuit can be conceptualized as a joint dynamic system performing both sensorimotor functions, as traditionally assigned to the cerebellum, and reward-related, cognitive processing. Although classically thought of as a motor circuit, the cerebellum is now understood to contribute to a wide variety of cognitive functions through its dense interconnections with the neocortex, the center of brain cognition. Recent investigations have shed light on the nature of cerebellar cognitive processing and information exchange with the neocortex. We review findings that demonstrate widespread reward-related cognitive input to the cerebellum, as well as new studies that have characterized the codependence of processing in the neocortex and cerebellum. Together, these data support a view of the neocortex–cerebellum circuit as a joint dynamic system both in classical sensorimotor contexts and reward-related, cognitive processing. These studies have also expanded classical theory on the computations performed by the cerebellar circuit. Although classically thought of as a motor circuit, the cerebellum is now understood to contribute to a wide variety of cognitive functions through its dense interconnections with the neocortex, the center of brain cognition. Recent investigations have shed light on the nature of cerebellar cognitive processing and information exchange with the neocortex. We review findings that demonstrate widespread reward-related cognitive input to the cerebellum, as well as new studies that have characterized the codependence of processing in the neocortex and cerebellum. Together, these data support a view of the neocortex–cerebellum circuit as a joint dynamic system both in classical sensorimotor contexts and reward-related, cognitive processing. These studies have also expanded classical theory on the computations performed by the cerebellar circuit.