Optokinetic and vestibular responsiveness in the macaque rostral vestibular and fastigial nuclei

Abstract

We recorded from rostral vestibular (VN) and rostral fastigial nuclei (FN) neurons that did not respond to eye movements during three-dimensional (3D) vestibular and optokinetic stimulation (OKS). The majority of neurons in both areas (76 and 69% in VN and FN, respectively) responded during both rotational and translational motion. Preferred directions scattered throughout 3D space for translation but showed some preference for pitch/roll over yaw for rotation. VN/FN neurons were also tested during OKS while monkeys suppressed their optokinetic nystagmus by fixating a head-fixed target. Only a handful of cells (VN: 17%, FN: 6%) modulated during 0.5-Hz OKS suppression, but the number of responsive cells increased (VN: 40%, FN: 48%) during 0.02-Hz OKS. Preferred directions for rotation and OKS were not matched on individual neurons, and OKS gains were smaller than the respective gains during rotation. These results were generally similar for VN and FN neurons. We conclude that optokinetic-vestibular convergence might not be as prevalent as earlier studies have suggested.

FIG. 1.

Responses from a rostral vestibular nuclei (VN) neuron during 3-dimensional (3D) vestibular stimulation. Small dots show instantaneous firing rate during (A) translation and (B) rotation at 0.5 Hz (12–16 cycles superimposed). Motion directions are indicated by the cartoon drawings. The solid gray lines show the sinusoidal fits. The stimulus traces (Stim) show linear acceleration (A) or angular velocity (B). Response gains were as follows—A: 209 (P ≪ 0.001, lateral), 55 (P = 0.05, fore-aft), and 74 sp/s/G (P = 0.01, vertical); B: 0.75 (P ≪ 0.001, yaw), 0.43 (P ≪ 0.001, pitch), and 1.19 sp/s/deg/s (P ≪ 0.001, roll).

FIG. 2.

Summary of rotation/translation responses in 3D. A and B: distributions of preferred directions (shown in spherical coordinates as azimuth and elevation) during translation and rotation, respectively. Each data point in the scatter plots corresponds to the preferred azimuth (abscissa) and elevation (ordinate) of a single neuron with significant responses along at least 1 motion direction. The data are plotted on Cartesian axes that represent the Lambert cylindrical equal-area projection of the spherical stimulus space (see Gu et al. 2006 for details). Histograms along the top and right sides of each scatter plot show the marginal distributions. Filled symbols indicate cells with significant modulation along at least 1 direction during both rotation and translation (convergent). Open symbols show nonconvergent cells that only modulate during either translation (A) or rotation (B). Cells that were not tested during both rotation and translation are shown with open triangles. C: definition of azimuth and elevation: Top and side view. Straight arrows depict the direction of translation, whereas curved arrows show the direction of rotation around each of the movement axes (based on the right-hand rule). D: scatter plot comparing preferred azimuths for rotation and translation (shown only for convergent cells). For tilt-aligned rotation/translation preferences, data points should fall along the ±90° diagonals (e.g., forward translation is defined with an azimuth of 0°, but a pitch rotation-tilt has an azimuth of 90/270°). E and F: distribution of neural response gains along the 3D preferred direction for translation and rotation, respectively. Fastigial nuclei (FN) neurons, red symbols/bars; VN neurons, blue symbols/bars.

FIG. 3.

Nystagmus elicited during yaw and pitch optokinetic stimulation (OKS). A and B: examples of horizontal (left) and vertical (right) eye position during yaw and pitch OKS at 0.5 and 0.02 Hz, respectively. C and D: histograms of peak horizontal and peak vertical slow phase eye velocity elicited during yaw and pitch OKS, respectively. Data are shown separately for 0.5 (filled bars) and 0.02 Hz (open bars).

FIG. 4.

A: examples of neural responses from a FN cell during yaw, pitch, and roll OKS at 0.5 (top, ∼15 cycles superimposed) and 0.02 Hz (bottom, ∼3 cycles superimposed). Response gains were as follows—0.5 Hz: 0.20 (P = 0.6, yaw OKS), 0.12 (P = 0.5, pitch OKS), and 0.28 sp/s/deg/s (P = 0.3, roll OKS); 0.02 Hz: 0.07 (P = 0.09, yaw OKS), 0.34 (P ≪ 0.001, pitch OKS), and 0.33 sp/s/deg/s (P = 0.03, roll OKS). B: scatter plot comparing 3D neural response gains during rotation and OKS, shown separately for FN (red symbols) and VN (blue symbols) at 0.5 (filled symbols) and 0.02 Hz (open symbols). Data are only shown for cells with significant modulation during both rotation and OKS. C: distribution of the difference in 3D preferred directions for responses to 0.5-Hz rotation and 0.02-Hz OKS stimulation. A difference of 180° signifies alignment of preferred directions; 0° represents anti-alignment.