TEMPORAL FEATURES OF DIRECTIONAL TUNING BY SPINOCEREBELLAR NEURONS - RELATION TO LIMB GEOMETRY

1. We showed previously that neurons in the dorsal spinocerebellar tra ct (DSCT) may encode whole-limb parameters of movement and posture rat her than localized proprioceptive information. Neurons were found to r espond to hindlimb movements in the sagittal plane with maximum activi ty for foot placements in one direction and minimum activity for place ments in the opposite direction. In contrast, movement direction is no t specifically encoded by response activity when movements are restric ted to a single joint. 2. We now describe the spatiotemporal character istics of DSCT directional sensitivity for the responses of 267 neuron s to small amplitude (0.5 cm) perturbations of the cat hindlimb. A sma ll platform attached to the left hind foot was perturbed along four or eight directions in the sagittal plane, eliciting significant respons es in 261 (98%) of the cells. The responses typically consisted of a s equence of peaks and troughs in poststimulus spike density lasting 150 ms or more following limb perturbation. 3. Peaks of activity in parti cular poststimulus intervals were broadly tuned for the direction of t he perturbation, as determined by fitting the firing rates recorded in response to each perturbation direction to a cosine model. The parame ters of the cosine model, namely the amplitude of modulation, the dire ction of maximum response, and the goodness of fit to the model, were computed for each 4 ms poststimulus interval. The parameters all showe d the same tendency to wax and wane with respect to poststimulus time. For each period during which the cell activity was highly correlated with the tuning model, the tuning indicated a different best direction . Thus each cell's directional tuning could be characterized by a set of tuning maxima associated with specific poststimulus times, when the amplitude of the tuning reached a local maximum and the fit to the co sine model was highly significant (R(2) > 0.85). 4. Directions of the tuning maxima for the total population of cells were not uniformly dis tributed within particular poststimulus intervals. There was a statist ically significant directional bias for upward directed perturbations in the poststimulus interval between 20 and 40 ms, followed by a perio d of downward bias from 45 to 55 ms. Between 60 and 85 ms, the distrib ution of tuning maxima was significantly skewed backward, whereas a ve ry strong bias for the forward direction was present at about 100 ms. 5. Because the tuning was determined from responses to very small pert urbations of the limb in a given posture, it was not clear whether the responses were related to specific joint angles or muscle lengths, or whether they somehow represented the kinematics of the whole Limb. To address this point, we examined the responses of 95 cells in two anim als that were each tested in two different limb positions. One positio n was an approximation of the normal standing position. The other posi tion consisted of a shortening of the limb axis (with major changes in all joint angles) in one animal, or a rotation of the limb axis backw ard (with little change in joint angles) in the other. 6. We compared each cell's responses to the same perturbations applied in the two lim b positions and found they could be identical, scaled in time or magni tude, or completely different in the two positions. A greater percenta ge of cells with different responses was found in the experiment with the limb axis rotated. In the other experiment, in which there were ma jor differences in joint angles in the two positions, the responses we re mostly the same or scaled in time in the two positions. We also det ermined the population directional biases for the two positions in eac h experi ment, and found that phase differences between the vectors re presenting population biases for the two positions were minimized when they were measured relative to the orientation of the limb axis (limb coordinates) rather than to the extrinsic vertical (lab coordinates). 7. On the basis of this result, which was consistent with the data fr om seven other animals, we propose that DSCT activity may represent mo vement kinematics in a limb-centered reference frame. The directional sensitivity of the cells is defined by the orientation of the limb axi s, which is the axis connecting the hip joint with the point of ground contact. The finding that preferred directions tend to cluster about directions that approximate limb movements along the limb axis (change s in limb length) or normal to it (changes in limb orientation) furthe r suggests a two-dimensional coordinate system defined by limb length and orientation. Because the temporal components of the directional re sponses seem to occur independently, we also suggest that elements of the presynaptic circuitry may provide the basis for this two-dimension al representation and also be responsible for creating and shaping its temporal domain.