Ocular Counterroll Modulates the Preferred Direction of Saccade-Related Pontine Burst Neurons in the Monkey

Abstract

Saccade-related burst neurons in the paramedian pontine reticular formation (PPRF) of the head-restrained monkey provide a phasic velocity signal to extraocular motoneurons for the generation of rapid eye movements. In the superior colliculus (SC), which directly projects to the PPRF, the motor command for conjugate saccades with the head restrained in a roll position is represented in a reference frame in between oculocentric and space-fixed coordinates with a clear bias toward gravity. Here we studied the preferred direction of premotor burst neurons in the PPRF during static head roll to characterize their frame of reference with respect to head and eye position. In 59 neurons (short-lead, burst-tonic, and long-lead burst neurons), we found that the preferred direction of eye displacement of these neurons changed, relative to head-fixed landmarks, in the horizontal-vertical plane during static head roll. For the short-lead burst neurons and the burst-tonic group, the change was about one-fourth of the amount of ocular counterroll (OCR) and significantly different from a head-centered representation. In the long-lead burst neurons, the rotation of the preferred direction showed a larger trend of about one-half of OCR. During microelectrical stimulation of the PPRF (9 sites in 2 monkeys), the elicited eye movements rotated with about one-half the amount of OCR. In a simple pulley model of the oculomotor plant, the noncraniocentric reference frame of the PPRF output neurons could be reproduced for recently measured pulley positions, if the pulleys were assumed to rotate as a function of OCR with a gain of 0.5. We conclude that the saccadic displacement signal is transformed from a representation in the SC with a clear bias to gravity to a representation in the PPRF that is closely craniocentric, but rotates with OCR, consistent with current concepts of the oculomotor plant.

Magnetic Resonance Imaging of Human Extraocular Muscles in Convergence

“…Another instance of the VOR is static ocular counter-rolling in response to maintained head tilt relative to gravity. Recordings from burst neurons in monkeys are compatible with torsional shift of rectus pulleys transverse to the EOM axes in the direction of ocular counterroll induced by static head tilt (Scherberger et al 2001), analogous to the coordinated torsional pulley shift observed here in convergence. In monkeys the displacement plane for 3-D eye positions during pursuit and saccades also shifts opposite to changes in head orientation relative to gravity (Hess and Angelaki 2002).…”

Neural Correlates of Forward and Inverse Models for Eye Movements: Evidence from Three-Dimensional Kinematics

“…Previous attempts searched for such neural signals consistent with 3D ocular kinematics in the premotor pathway for generating eye movements (van Opstal et al, 1991(van Opstal et al, , 1996Hepp et al, 1993;Scherberger et al, 2001). However, here, we show that the search should not be aimed at neural pathways that implement the inverse model (i.e., those directly involved in the generation of the movement), but rather at neural pathways that implement the forward model.…”

Current concepts of mechanical and neural factors in ocular motility

“…The central neural signals correlated with all types of eye movement would be expected to reflect effects of torsional reconfiguration of rectus pulleys during the VOR. Recordings from burst neurons in monkeys appear compatible with torsional shift of rectus pulleys transverse to the EOM axes induced by static head tilt [66]. In monkeys the displacement plane for 3-D eye positions during pursuit and saccades shifts opposite to changes in head orientation [67], and such shifts may be dynamic during semicircular canal stimulation [68,69].…”