Bechara BP, Gandhi NJ. Matching the oculomotor drive during head-restrained and head-unrestrained gaze shifts in monkey. J Neurophysiol 104: 811-828, 2010. First published May 26, 2010 doi:10.1152/jn.01114.2009. High-frequency burst neurons in the pons provide the eye velocity command (equivalently, the primary oculomotor drive) to the abducens nucleus for generation of the horizontal component of both head-restrained (HR) and head-unrestrained (HU) gaze shifts. We sought to characterize how gaze and its eye-in-head component differ when an "identical" oculomotor drive is used to produce HR and HU movements. To address this objective, the activities of pontine burst neurons were recorded during horizontal HR and HU gaze shifts. The burst profile recorded on each HU trial was compared with the burst waveform of every HR trial obtained for the same neuron. The oculomotor drive was assumed to be comparable for the pair yielding the lowest root-mean-squared error. For matched pairs of HR and HU trials, the peak eye-in-head velocity was substantially smaller in the HU condition, and the reduction was usually greater than the peak head velocity of the HU trial. A time-varying attenuation index, defined as the difference in HR and HU eye velocity waveforms divided by head velocity [␣ ϭ (Ḣ hr Ϫ Ė hu )/Ḣ ] was computed. The index was variable at the onset of the gaze shift, but it settled at values several times greater than 1. The index then decreased gradually during the movement and stabilized at 1 around the end of gaze shift. These results imply that substantial attenuation in eye velocity occurs, at least partially, downstream of the burst neurons. We speculate on the potential roles of burst-tonic neurons in the neural integrator and various cell types in the vestibular nuclei in mediating the attenuation in eye velocity in the presence of head movements.
I N T R O D U C T I O NTo align the visual axis on an object of interest, one must shift the line of sight (gaze) by rapidly moving the eyes in their orbits. For large changes in gaze, a head movement typically accompanies the eye-in-head rotation. Such rapid, coordinated movements of the eyes in the orbits and the head in space are termed head-unrestrained (HU) gaze shifts. For smaller changes in gaze or when the head is immobilized, redirections of the visual axis are executed by eye movements within the orbits. We refer to such high-velocity movements as head-restrained (HR) gaze shifts or saccades.The primary oculomotor drive that produces a saccadic rotation of the eyes in orbits is an eye velocity command from neurons in the saccadic burst generator (Robinson 1975). For horizontal eye movements, the eye velocity command is encoded as a high-frequency volley of action potentials by putative short-lead burst neurons (Van Gisbergen et al. 1981) that reside in the paramedian pontine reticular formation (PPRF) and project directly to the abducens motoneurons (Langer et al. 1986;Strassman et al. 1986a). When the head is restrained, properties of the burst specif...