Premotor neurons encode torsional eye velocity during smooth-pursuit eye movements

Abstract

Responses to horizontal and vertical ocular pursuit and head and body rotation in multiple planes were recorded in eye movement-sensitive neurons in the rostral vestibular nuclei (VN) of two rhesus monkeys. When tested during pursuit through primary eye position, the majority of the cells preferred either horizontal or vertical target motion. During pursuit of targets that moved horizontally at different vertical eccentricities or vertically at different horizontal eccentricities, eye angular velocity has been shown to include a torsional component the amplitude of which is proportional to half the gaze angle ("half-angle rule" of Listing's law). Approximately half of the neurons, the majority of which were characterized as "vertical" during pursuit through primary position, exhibited significant changes in their response gain and/or phase as a function of gaze eccentricity during pursuit, as if they were also sensitive to torsional eye velocity. Multiple linear regression analysis revealed a significant contribution of torsional eye movement sensitivity to the responsiveness of the cells. These findings suggest that many VN neurons encode three-dimensional angular velocity, rather than the two-dimensional derivative of eye position, during smooth-pursuit eye movements. Although no clear clustering of pursuit preferred-direction vectors along the semicircular canal axes was observed, the sensitivity of VN neurons to torsional eye movements might reflect a preservation of similar premotor coding of visual and vestibular-driven slow eye movements for both lateral-eyed and foveate species.

Fig. 1.

Responses of an eye-head neuron during vertical and horizontal pursuit (0.5 Hz ±10°) with the target located either straight ahead (top), to the left (for vertical pursuit;bottom left) or up (horizontal pursuit; bottom right). For each panel, the three components of eye position (E_hor, horizontal;E_ver, vertical; andE_tor, torsional) and the three components of the angular velocity (Ω_hor, horizontal; Ω_ver, vertical; and Ω_tor, torsional) of the right eye and IFR of the neuron are shown. Positive directions of eye movements are leftward, downward, and clockwise (relative to the animal). Vertical scale bars, 20° for eye position, 30°/sec for horizontal–vertical, and 10°/sec for torsional eye velocity. Note that, because of the mathematics of rotational kinematics, Ω_tor is not the time derivative of E_tor (Tweed and Vilis, 1987,1990; Haslwanter, 1995).

Fig. 2.

Responses of the same eye-head neuron as in Figure1 during rotation about different axes (0.5 Hz, ±10°). The animal was viewing a head-fixed target located straight ahead during yaw, pitch, roll, or right anterior–left posterior canal plane (RALP) rotation. For each panel, the three components of eye position (E_hor, horizontal;E_ver, vertical; andE_tor, torsional) and the three components of the angular velocity (Ω_hor, horizontal; Ω_ver, vertical; and Ω_tor, torsional) of the right eye, stimulus (head velocity, H), and IFR of the neuron. Positive directions of eye and head movements are leftward, downward, and clockwise (relative to the animal). Vertical scale bars, 30°/sec for horizontal–vertical–torsional eye and head velocity.

Fig. 3.

Spatial distribution of pursuit response vectors for 100 neurons tested during horizontal–vertical pursuit through primary position. Different symbols represent PV (red circles), EH (blue diamonds), and BT (green squares) cells. Dotted circular lines illustrate concentric circles at a constant sensitivity (2, 1, and 0.5 spikes/sec per °/sec). Dotted radial lines represent 30° increments in spatial alignment.

Fig. 4.

Dependence of (A) neural firing rates and (B) torsional eye velocity on horizontal (left) and vertical (right) gaze eccentricity during vertical and horizontal pursuit, respectively. Data from 16 PV (red circles), EH (blue diamonds), and BT (green squares) cells that exhibited a significant dependence of gain and/or phase on eye position are shown. Data in B were recorded simultaneously with the neural responses in A. Torsional eye velocity is shown above the dotted zero-line when positive torsion is elicited simultaneously with positive vertical (downward) or positive horizontal (leftward) eye velocity and below the dotted zero-line otherwise. The small nonzero torsional values at zero eye position (straight-ahead gaze) reflect the small difference between straight ahead and primary position (see Materials and Methods). Neural response phase was expressed relative to downward and ipsilateral eye velocity for vertical and horizontal pursuit, respectively. A phase of 0° (−90°) corresponded to a response in phase with downward eye velocity (position) during vertical pursuit and ipsilateral eye velocity (position) during horizontal pursuit.

Fig. 5.

Quantification of the torsional eye movement sensitivity of neurons. A, Comparison of two goodness-of-fit criteria, the variance-accounted-for (VAF) and the Bayesian information criteria (BIC), obtained for the traditional 2D (horizontal–vertical) versus 3D model fits. VAF and BIC values for the 3D model fall above or below (respectively) the corresponding values obtained from the 2D model. Filled symbols correspond to fits for neurons with significant target position dependence (Fig.4A). Open symbols are used for cells whose regressions were not significant. B, Spatial plots of the computed 3D eye movement sensitivity vector for 31 cells tested during eccentric pursuit. Each line corresponds to a single cell, with its length representing the sensitivity of the cell to pursuit and its orientation corresponding to the absolute value of the elevation angle, β, out of Listing's plane toward the torsional axis (Eq. 3). Filled symbols were used for the same PV (red circles), EH (blue diamonds), and BT (green squares) cells as those plotted in Figure4. Open symbols were used for the remaining cells whose gain and phase dependence on target eccentricity was not rendered significant according to linear regressions similar to those in Figure4.

Fig. 6.

3D spatial distribution of pursuit preferred directions (unit vectors) for 31 cells. The mean vector orientations for the ipsilateral (left) horizontal canal (HC), anterior canal (AC), and posterior canal (PC) afferents have been plotted with heavy, long lines (magenta, green, and cyan lines, respectively) (data from Dickman et al., 2002). As rotations are represented using the right-hand rule, a preferred sensitivity for ipsilateral (leftward) rotation is represented as a vector aligned with the positive z-axis. Similarly, sensitivity to a downward rotation is illustrated as a vector aligned with the positive y-axis. Finally, a clockwise rotation (i.e., rotation toward right ear down from upright) is represented as a vector aligned with the positive x-axis. Red circles illustrate PV; blue diamonds, EH responses; and green squares, BT cells.