Dynamics of Squirrel Monkey Linear Vestibuloocular Reflex and Interactions with Fixation Distance

Abstract

Horizontal, vertical, and torsional eye movements were recorded using the magnetic search-coil technique during linear accelerations along the interaural (IA) and dorsoventral (DV) head axes. Four squirrel monkeys were translated sinusoidally over a range of frequencies (0.5-4.0 Hz) and amplitudes (0.1-0.7 g peak acceleration). The linear vestibuloocular reflex (LVOR) was recorded in darkness after brief presentations of visual targets at various distances from the subject. With subjects positioned upright or nose-up relative to gravity, IA translations generated conjugate horizontal (IA horizontal) eye movements, whereas DV translations with the head nose-up or right-side down generated conjugate vertical (DV vertical) responses. Both were compensatory for linear head motion and are thus translational LVOR responses. In concert with geometric requirements, both IA-horizontal and DV-vertical response sensitivities (in deg eye rotation/cm head translation) were related linearly to reciprocal fixation distance as measured by vergence (in m-1, or meter-angles, MA). The relationship was characterized by linear regressions, yielding sensitivity slopes (in deg.cm-1.MA-1) and intercepts (sensitivity at 0 vergence). Sensitivity slopes were greatest at 4.0 Hz, but were only slightly more than half the ideal required to maintain fixation. Slopes declined with decreasing frequency, becoming negligible at 0.5 Hz. Small responses were observed when vergence was zero (intercept), although no response is required. Like sensitivity slope, the intercept was largest at 4.0 Hz and declined with decreasing frequency. Phase lead was near zero (compensatory) at 4.0 Hz, but increased as frequency declined. Changes in head orientation, motion axis (IA vs. DV), and acceleration amplitude produced slight and sporadic changes in LVOR parameters. Translational LVOR response characteristics are consistent with high-pass filtering within LVOR pathways. Along with horizontal eye movements, IA translation generated small torsional responses. In contrast to the translational LVORs, IA-torsional responses were not systematically modulated by vergence angle. The IA-torsional LVOR is not compensatory for translation because it cannot maintain image stability. Rather, it likely compensates for the effective head tilt simulated by translation. When analyzed in terms of effective head tilt, torsional responses were greatest at the lowest frequency and declined as frequency increased, consistent with low-pass filtering of otolith input. It is unlikely that IA-torsional responses compensate for actual head tilt, however, because they were similar for both upright and nose-up head orientations. The IA-torsional and -horizontal LVORs seem to respond only to linear acceleration along the IA head axis, and the DV-vertical LVOR to acceleration along the head's DV axis, regardless of gravity.

Differential Sensorimotor Processing of Vestibulo-Ocular Signals during Rotation and Translation

“…Several hypotheses have been put forward in the past years to account for the differences in the dynamic processing of sensory signals in the TrVOR as compared with the RVOR (Paige and Tomko, 1991b;Raphan et al, 1996;Telford et al, 1997;Green andGaliana, 1998, 1999;Musallam and Tomlinson, 1999). The goal of this section is two-fold: first, to justify the structure of the model supported here (see Fig.…”

“…The use of sinusoidal stimulation at 0.5 Hz to study stable gaze responses during translation deserves f urther comment because of the fact that this is a low-frequency stimulus for the TrVOR, which is robust in the absence of visual feedback only at relatively high frequencies (Ͼ0.5 Hz) (Paige and Tomko, 1991a;Telford et al, 1997). In other words, the observed eye movements during 0.5 Hz TrVOR stable gaze are presumably primarily visually evoked (i.e., pursuit responses).…”

“…The most widespread hypothesis for the dynamic processing of otolith signals has been based on a proposal by Paige and colleagues that the additional required low-pass filtering of otolith signals in the TrVOR is performed by a preliminary neural processing stage including either an integrator or a low-pass filter cascaded with a high-pass filter (Paige and Tomko, 1991b;Telford et al, 1997). The prefiltered otolith signals are then combined with the angular head velocity signals from the semicircular canals and are commonly processed via the parallel pathways proposed by Skavenski and Robinson (1973), as outlined above.…”

“…Both the eye plant (Green and Galiana, 1998) and the prefiltering hypotheses (Paige and Tomko, 1991b;Telford et al, 1997) can qualitatively predict TrVOR dynamics [although an exact match between experimental data and model predictions is problematic because TrVOR dynamics exhibits nonminimum phase behavior when evaluated in an extended frequency range (Angelaki, 1998)]. This is so because the proposed realizations of these alternative hypotheses are practically identical in terms of the overall input-output characterization of the system.…”

“…Second, the frequency range of effective operation is different for the two reflexes. Although the RVOR elicits compensatory eye movements down to ϳ0.05 Hz, the TrVOR only exhibits a robust response above ϳ0.5 Hz (Paige and Tomko, 1991a;Telford et al, 1997;Angelaki, 1998). Finally, there is increasing evidence that the synaptic organization of the otolith-ocular and canal-ocular pathways is different.…”