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Summary: Premotor Neurons Encode Torsional Eye Velocity during
Smooth-Pursuit Eye Movements
Dora E. Angelaki and J. David Dickman
Department of Neurobiology, Washington University School of Medicine, and Hearing Research Department, Central Institute for the Deaf, St. Louis,
Missouri 63110
Responses to horizontal and vertical ocular pursuit and head and body rotation in multiple planes were recorded in eye movement-
sensitiveneuronsintherostralvestibularnuclei(VN)oftworhesusmonkeys.Whentestedduringpursuitthroughprimaryeyeposition,
themajorityofthecellspreferredeitherhorizontalorverticaltargetmotion.Duringpursuitoftargetsthatmovedhorizontallyatdifferent
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,themajorityofwhichwerecharacterizedas"vertical"duringpursuitthroughprimaryposition,exhibitedsignificantchangesin
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 deriv-
ative of eye position, during smooth-pursuit eye movements. Although no clear clustering of pursuit preferred-direction vectors along
thesemicircularcanalaxeswasobserved,thesensitivityofVNneuronstotorsionaleyemovementsmightreflectapreservationofsimilar
premotor coding of visual and vestibular-driven slow eye movements for both lateral-eyed and foveate species.
Key words: eye movement; vestibulo-ocular; vergence; kinematics; torsion; smooth pursuit; coordinate frame; three-dimensional;
sensorimotor
Introduction
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