Multiple reference frames for motion in the primate cerebellum

Abstract

Knowledge of body motion through space is necessary for spatial orientation, self-motion perception, and postural control. Yet, sensory afferent signals may not directly provide such information to the brain. Because motion detected by the vestibular end organs is encoded in a head-fixed frame of reference, a coordinate transformation is thus required to encode body motion. In this study, we investigated whether cerebellar motion-sensitive neurons encode the translation of the body through space. We systematically changed both the direction of motion relative to the body and the static orientation of the head relative to the trunk. The activities of motion-sensitive neurons in the most medial of the deep cerebellar nuclei, the rostral fastigial nucleus, were compared with those in the brainstem vestibular nuclei. We found a distributed representation of reference frames for motion in the rostral fastigial nucleus, in contrast to cells in the vestibular nuclei, which primarily encoded motion in a head-fixed reference frame. This differential representation of motion-related information implies potential differences in the functional roles of these areas.

Figure 1.

Instantaneous firing rates of two rostral FN neurons during passive whole-body translation at 0.5 Hz (±0.2 g) along different directions in the horizontal plane. Data are color coded for the three head-on-body positions; blue, red, and green colors are used for straight-ahead (h = 0°) and 30° to the right (h = -30°) or left (h = 30°) head-on-trunk positions. Superimposed solid lines represent best-fit sine functions. A, FN neuron encoding motion in a body reference frame, where the firing rate of the cell is independent of head-on-trunk position. B, FN neuron encoding motion in ahead reference frame. The firing rate of the cell changes for the different head-on-trunk positions. In both panels, the minimum responses are marked with asterisks. The black traces represent the linear acceleration stimulus. Motion stimuli are defined relative to the body and, thus, change direction relative to the head (monkey drawing).

Figure 2.

Neural response gain and phase plotted as a function of the direction of translation for each of the three head-on-body positions. A, FN neuron encoding motion in a body reference frame (same data as in Fig. 1 A). The firing rate of the cell is independent of head-on-trunk position. B, FN neuron encoding motion in a head reference frame (same data as in Fig. 1 B). The firing rate of the cell changes for the different head-on-trunk positions. Different symbols are used for data obtained for the three head-on-trunk positions. The corresponding lines illustrate the fit of the λ-variable spatiotemporal tuning model. sp/sec/g, Spikes/second/gravity.

Figure 3.

Parameters of a spatiotemporal tuning model fitted to gain and phase as a function of motion direction separately for each head-on-trunk position (analysis step I). A, The gain and phase of the cell during motion along the maximum response direction for each of the two rotated head-on-body positions (h =±30°) plotted versus the corresponding values when the head was straight ahead relative to the body (h = 0°). Each pair of open and filled symbols corresponding to the same abscissa illustrates data from a cell for which the spatial tuning was tested in both left and right head-on-trunk positions. A few cells were only tested either with the left (h = 30°) or the right head-on-trunk (h = -30°) positions. Regression equations: y = 0.2 + 0.92 x, r² = 0.85 (gain); y = 0.7 + 1.01 x, r² = 0.96 (phase). B, The average spatial shift in the tuning curves for FN and VN neurons was plotted as a function of head-on-body position. Data were normalized before the calculation of the averages by subtracting from the spatial angle of the maximum response direction for h = ±30° the respective angle with the head centered (h = 0°).

Figure 4.

Coordinate frames for FN and VN neurons. A, Comparison between the goodness-of-fit (VAF) for two λ-fixed spatial shift models (analysis step II): a body-fixed reference frame model with λ = 0 (abscissa) and a head-fixed reference frame model with λ = 1 (ordinate). Open circles, VN neurons; gray squares, FN neurons. The dotted line illustrates the unity-slope line. B, Variable spatial shift model (analysis step III): distributions of λ values for the VN and FN cell populations (black and gray, respectively). Vertical gray and black lines illustrate the medians of the two populations, λ (median for FN neurons) = 0.4 and λ (median for VN neurons) = 0.9.