Behavior of gaze velocity Purkinje (GVP) cells during vestibulo-ocular reflex (VOR) stabilization of head rotation and translation

Lawrence H Snyder1 and W. Michael King2

1McDonnell Center for Higher Brain Research
Washington University School of Medicine
St. Louis, MO

2Dept. Neurology and Anatomy
University of Missippi Medical Center
Jackson, MS

The VOR stabilizes gaze during head rotation and translation. We recorded from GVP cells in the cerebellar flocculus and paraflocculus of the monkey during off-axis rotation, which both rotates and translates the head. We asked whether GVP cells carry feed-forward (sensory) signals or feed-back (efference copy) signals, whether these signals are related specifically to head translation, and whether the signals might play a causal role in driving the VOR. We found that GVP cells had an early and a later response component.

The early component was revealed by comparing rotations about anterior and posterior vertical axes during far viewing. Head rotation and eye movement were identical; only head translation varied. GVP cells reflected the difference in translation within 20-30 ms of head movement onset, with modulation proportional to linear head acceleration and independent of viewing distance and eye velocity. This suggests that GVP cells receive a head translation signal with dynamics similar to that of otolith afferents.

The late component of the GVP response was revealed by comparing identical off-axis rotations during near and far viewing. Only the eye movement response to translation varied; head rotation, head translation and the eye movement response to the rotation were invariant. GVP activity was modulated proportional to the excess eye velocity obtained with near compared to far viewing. The relationship between GVP activity and excess eye velocity was identical to that seen during far target pursuit. However, GVP firing lagged eye velocity by 10 ms. These data suggest that GVP cells receive an efference copy only of that portion of the eye movement signal that compensates for translation.

These results are strikingly different from those obtained using sinusoidal head rotation about a single axis of rotation and a single viewing distance. We saw no clear response to either head rotation or to the eye movement response to head rotation. Our results suggest that translation-related signals reach the cerebellum, but that the required scaling of those signals inversely with viewing distance must occur outside the reciprocal pathways between GVP cells and the vestibular nuclei.

Keywords: Vestibulo-ocular reflex VOR eye movements eye head coordination