Neural circuit mechanisms to transform cerebellar population dynamics for motor control in monkeys

We exploit identification of neuron types during extracellular recording to demonstrate how the cerebellar cortexs well-established architecture transforms inputs into outputs. During smooth pursuit eye movements, the floccular complex performs distinct input-output transformations of temporal dynamics and directional response properties. The responses of different interneuron types localize the circuit mechanisms of each transformation. Mossy fibers and unipolar brush cells emphasize eye position dynamics uniformly across the cardinal axes; Purkinje cells and molecular layer interneurons code eye velocity along directionally biased axes; Golgi cells show unmodulated firing. Differential directional response properties of different neuron types localize the directional input-output transformation to the last-order inputs to Purkinje cells. Differential temporal dynamics pinpoint the site of the temporal input-output transformation to granule cells. Specific granule cell population dynamics allow the temporal transformations required in the area we study and generalize to many temporal transformations, providing a complete framework to understand cerebellar circuit computation. Impact statementWe dissect the circuit computations performed by the floccular complex of the cerebellum during an exemplar sensory-motor behavior, taking advantage of knowledge of the circuit architecture, existence of discrete neuron types, and a newfound ability to identify neuron types from extracellular recordings. Our results describe the contributions of the major neuron types to the cerebellar input-output computations, identify the population dynamics needed in granule cells to support those computations, and to create a basis set to enable temporally-specific motor behavior and motor learning.