The Interaction of Pre-programmed Eye Movements With the Vestibulo-Ocular Reflex

Abstract

The Vestibulo-Ocular Reflex (VOR) works to stabilize gaze during unexpected head movements. However, even subjects who lack a VOR (e.g., vestibulopathic patients) can achieve gaze stability during planned head movements by using pre-programmed eye movements (PPEM). The extent to which PPEM are used by healthy intact subjects and how they interact with the VOR is still unclear. We propose a model of gaze stabilization which makes several claims: (1) the VOR provides ocular stability during unexpected (i.e., passive) head movements; (2) PPEM are used by both healthy and vestibulopathic subjects during planned (i.e., active) head movements; and (3) when a passive perturbation interrupts an active head movement in intact animals (i.e., combined passive and active head movement) the VOR works with PPEM to provide compensation. First, we show how our model can reconcile some seemingly conflicting findings in earlier literature. We then test the above-mentioned predictions against data we collected from both healthy and vestibular-lesioned guinea pigs. We found that (1) vestibular-lesioned animals showed a dramatic decrease in compensatory eye movements during passive head movements, (2) both populations showed improved ocular compensation during active vs. passive head movements, and (3) during combined active and passive head movements, eye movements compensated for both the active and passive component of head velocity. These results support our hypothesis that while the VOR provides compensation during passive head movements, PPEM are used by both intact and lesioned subjects during active movements and further, that PPEM work together with the VOR to achieve gaze stability.

Keywords: Vestibulo-Ocular Reflex; adaptation; biological; efference copy; gaze stabilization; internal model.

Figure 1

Model of gaze stabilization. Bottom portion represents traditional pathways (i.e., the VOR and Gaze Command). Top portion (in gray, labeled “Active”) includes a pathway that estimates head velocity (“Neck and Head Model”) and necessary pre-programmed eye movements (“PPEM”) and two alternative pathways that interact with the VOR. The Suppression Model, in blue, that turns off the VOR and the Cooperative Model, in orange, that estimates the VOR's response (“VOR Model”) and subtracts it from the total eye movement.

Figure 2

Turn-table velocity and head velocity from each of the approximately 80 passive-only trials during a single test day. The head consistently responds as a underdamped second order system with decaying oscillations.

Figure 3

(Top) Data from Dichgans et al. (1973) and (bottom) model simulations. (A) Gaze (G), head (H), and eye (E) position traces from an intact animal during a voluntary head rotation. (B) Eye position from an intact animal when a voluntary head rotation is unexpectedly stopped via head brake. (C) Eye position from a vestibular-lesion animal, that also underwent cervical deafferentation, when a voluntary head rotation is unexpectedly stopped. (D) Eye position from a vestibular-lesion animal, that also underwent cervical deafferentation, when a voluntary head rotation is unexpectedly stopped.

Figure 4

Exemplary data from healthy guinea pigs during passive (Left), active (Middle), and combined (Right) head movements. Details show difference in gain and latency of eye movements during passive and active head movements. Model predictions are identical for passive- and active-only movements, but can be distinguished during combined movements.

Figure 5

(Top and Middle) Gain and latency of eye movements during passive, active, and combined head movements. Regressions were performed against total head velocity (black bars, Equation 6) and against passive and active components of head velocity independently (gray bars, Equation 7). (Bottom) Goodness of fit for each model.

Figure 6

Exemplary data from lesioned guinea pigs during passive (Left), active (Middle), and combined (Right) head movements. Details show difference in gain and latency of eye movements during passive and active head movements. Model predictions are identical for passive- and active-only movements, but can be distinguished during combined movements.

Figure 7

(Top and Middle) Gain and latency of eye movements during passive, active, and combined head movements. Regressions were performed against total head velocity (black bars, Equation 6) and against passive and active components of head velocity independently (gray bars, Equation 7). (Bottom) Goodness of fit for each model.

Figure 8

Gain of pre-programmed eye movements as a function of time after lesion. On days when more than one animal was tested, the gains of all animals were averaged together.

Figure 9

Simulations of pre-programmed eye movements as a function of $\widehat{p}$. Darker traces are simulations with higher values of $\widehat{p}$ and result in very little compensation whereas lighter traces, with lower values of $\widehat{p}$, show large pre-programmed eye movements.