Spatiotemporal response properties of cerebellar Purkinje cells to neck displacement

The activity of 184 Purkinje cells and 58 unidentified neurons located within the cerebellar anterior vermis was recorded in decerebrate cats during wobble of the body under a fixed head. This stimulus induced a neck displacement of constant amplitude (2.5 degrees) whose direction rotated at the constant velocity of 56.2 degrees/s on the horizontal plane, both in the clockwise and counterclockwise directions. It was then possible to evaluate the spatiotemporal characteristics of unit responses to neck displacement in the vertical planes; 131 of 184 Purkinje cells (71%) and 35 of 58 unidentified cells (60%) responded to clockwise and/or counterclockwise rotations. In particular, among the responsive units, 44% of the Purkinje cells and 37% of the unidentified cells showed an equal amplitude modulation during clockwise and counterclockwise rotations. These units are expected to show a maximal response sensitivity for neck displacement in a preferred direction, a null response for perpendicularly oriented stimuli and a constant temporal phase (narrowly tuned neurons). In 28% of the Purkinje cells and 40% of the unidentified cells, responses of different amplitudes were observed during clockwise and counterclockwise rotations. These neurons should display a preferred direction of response to neck displacement, lack of null response directions and a temporal phase changing with the stimulus direction (broadly tuned neurons). Finally, 27% of the Purkinje cells and 23% of the unidentified cells responded only to wobble in the clockwise or counterclockwise direction (unidirectional units). This behavior predicts equal sensitivities for all the directions of neck displacement and a response phase changing linearly with the direction of neck displacement. A maximal sensitivity vector (Smax), aligned with the preferred direction of the neuron, was evaluated for the bidirectional narrowly tuned and broadly tuned units. Its amplitude and temporal phase corresponded to the response characteristics expected for stimuli in the preferred direction of the cell. Smax directions were distributed over the horizontal plane. Most of them, however, were closer to the pitch than to the roll axis and pointed towards the animal's tail. Among pitch-related Purkinje cells, the temporal phase of Smax was small with a predominance of phase lags; phase leads of rather large amplitude were usually observed for roll-related Purkinje cells. The possibility that the recorded population of units coded the direction of neck displacement was tested by assuming that each cell gave a vectorial contribution related to its response properties and that the vectorial sum of such contributions represented the outcome of the population code. Dynamic body-to-head displacements in four different directions were simulated and for each direction 12 population vectors were evaluated at regular intervals of the stimulus cycle. The direction of the population vector was related to that of the stimulus, but the correspondence was close only for the pitch direction. Moreover, the amplitude of the population vector depended upon the direction of the stimulus, being larger for pitch than for roll displacements. Due to the efferent connections of the explored cerebellar region, the neuronal signals generated by the Purkinje cell population are probably transferred to the spinal cord, where they may differentially affect the amplitude and the spatial properties of the neck reflexes according to the direction of neck displacement.