Comparison of neuronal activity in external cuneate nucleus, spinocerebellar cortex and interpositus nucleus during passive limb movement

External cuneate nucleus (ECN) conveys an important sensory input to the cerebellum since it relays information about fore-legs, neck and fore-trunk. This information is encoded in the spinocerebellum considered crucial for the production of normal coordinated limb movements. The interpositus nucleus (IN) elaborates the output signals from spinocerebellum to regulate the motor commands. The present experiments were undertaken to study how the sensory representation about limb passive movements is processed in this transcerebellar pathway. We recorded extracellular activity in ECN (180 cells), spinocerebellar cortex (467 Purkinje cells) and IN (97 cells) of anaesthetized rats. Neuronal discharges were monitored while a computer controlled robot arm imposing circular passive movements to the unrestrained forelimb along sagittal plane. We used the Wald-Wolfowitz runs test to identify cellular mean activity significantly modulated over a movement cycle. Among the recorded neurons, 88 ECN, 165 Purkinje and 45 IN cells showed significant modulation along the trajectory. To summarize the variety of waveforms produced by the entire dataset of modulated neurons, we applied the principal component (PC) analysis. The first three PC explained 75% of the total variance. We correlated each PC with every cellular activity histogram, obtaining the weighting coefficients (r). We found that ECN and Purkinje cells had strong positive relationship with the first PC (explaining 43% of the variance) with weighting coefficients centered at r  0.90-0.95. Instead, IN population showed a moderate correlation for the first PC (centered at r  0.60), but a strong correlation with the second PC (explaining 24% of the variance) with weighting coefficients centered at r  0.90-0.95. Lastly, we used linear regression models to relate each PC to the limb kinematics, i.e. shoulder, elbow, wrist angular excursions and the variations of end point coordinates. We observed that the first two PC of the entire dataset fit global limb parameters (end point coordinates) better than individual joint angles. However, the first PC, representing mainly the ECN and spinocerebellar cells activity, was well correlated to the shoulder angle, whereas the second PC, representing IN activity, shows good correlation with elbow and wrist joint excursions. The results of this study suggest that ECN and spinocerebellar cortex represent the sensory signals from limb movement differently respect to the IN encoding. Although all these structures encode information relating the entire limb, ECN and spinocerebellar cortex receive a significant contribution only from the shoulder, whereas IN incorporate information mainly from more distal joints.