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.
Highlights
Maintaining a stable line of sight in the midst of head movement is essential to normal function
It suggests that pre-programmed eye movements (PPEM) are a part of normal gaze stabilization resulting in improved compensation during active head movements, similar to what clinicians have observed. It predicts that if the gain of PPEM and Vestibulo-Ocular Reflex (VOR) are similar, PPEM would not be observed in healthy subjects when planned head movements are prevented, as described by Dichgans et al Our model predicts that while PPEM are the primary means of gaze stability during active head movements, the VOR remains online to compensate for any unexpected passive perturbations
In Dichgans original paper, PPEM were defined as compensatory eye movements seen when a planned head movement was unexpectedly prevented
Summary
Maintaining a stable line of sight in the midst of head movement is essential to normal function. It predicts that if the gain of PPEM and VOR are similar (as is the case for non-human primates and humans), PPEM would not be observed in healthy subjects when planned head movements are prevented, as described by Dichgans et al. Our model predicts that while PPEM are the primary means of gaze stability during active head movements, the VOR remains online to compensate for any unexpected passive perturbations. Our model predicts that while PPEM are the primary means of gaze stability during active head movements, the VOR remains online to compensate for any unexpected passive perturbations This claim, that the VOR remains operational during voluntary movements, harkens back to an older, but still on-going controversy regarding gaze shifts. Our hypothesis is that while the VOR pathway provides gaze stabilization during passive head movements, pre-programmed eye movements (PPEM) are used during active head movements. For animals that underwent cervical deafferentation, and had no VOR or COR, we set the estimated passive gain to 0.0
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