Modulation of the human vestibuloocular reflex during saccades: probing by high-frequency oscillation and torque pulses of the head

Abstract

1. We probed the gain and phase of the vestibuloocular reflex (VOR) during the execution of voluntary gaze saccades, with continuous oscillation or acceleration pulses, applied through a torque helmet. 2. Small-amplitude (< 1 degree), high-frequency (10-14 Hz) head oscillations in the horizontal or vertical plane were superimposed on ongoing horizontal gaze saccades (40-100 degrees). Torque pulses to the head ("with" or "against" gaze) were superimposed on 40 degrees horizontal saccades. Eye and head movements were precisely measured with sensor coils in magnetic fields. 3. Techniques were developed to separate the oscillatory (horizontal or vertical) component from the gaze shift and obtain VOR gain and phase with Fourier techniques from the relation between eye-in-head and head oscillations. These involved either subtraction of exactly matching saccades with and without oscillation (drawback: low yield) or time shifting of successive trials to synchronize the oscillations (drawback: slight time blurring of saccades). 4. The results of these matching and synchronization methods were essentially identical and consistent. Presaccadic gain values of the horizontal VOR (typically about unity) were reduced by, on average, approximately 20 and 50% during horizontal saccades of 40 and 100 degrees, respectively. These percentages may be truncated because of methodological limitations, but even after taking these into account (on the basis of simulation experiments with 2 different, theoretical profiles of suppression) our results do not support a complete saccadic VOR suppression for any substantial fraction of saccadic duration. Qualitatively similar changes were found when the vertical VOR was probed during 100 degrees horizontal saccades. 5. Concomitantly with the reductions in gain, VOR phase was advanced by approximately 20 degrees during the saccade. 6. In the wake of gaze saccades, VOR gain was consistently elevated (to approximately 1.0) above the presaccadic level (approximately 0.9). We submit that this mechanism ensures stable fixation of the newly acquired target at a time when the head is still moving substantially. 7. Although the responses to head torque pulses showed idiosyncratic asymmetries, analysis of the differences in eye and head movements for pulses with and against consistently showed a sharp fall of VOR gain at saccadic onset, following an approximately exponential course with a time constant of approximately 50 ms. This decay may be assumed to reflect VOR gain for a period of approximately 50 ms, after which secondary gaze control mechanisms become dominant. 8. The time course of the gain decay and phase shift of the VOR suggest that suppression of the "integrative (position) loop" of the VOR circuit was more complete than suppression of the direct, "velocity" pathway.

Premotor Correlates of Integrated Feedback Control for Eye–Head Gaze Shifts

“…2 A, gray traces). As observed previously, perturbed gaze shifts remained accurate following head perturbations ( p ϭ 0.46; paired t test, matched perturbed vs control trials) (Laurutis and Robinson, 1986;Guitton and Volle, 1987;Tomlinson, 1990;Tabak et al, 1996;Cullen et al, 2004) Importantly, the applied transient head perturbations did not completely interrupt the gaze shift (i.e., gaze velocity was not driven to zero velocity for a sustained time interval). Rather, they modified ongoing gaze shifts in two critical ways: (1) gaze shift durations increased significantly ( p Ͻ 0.05) (Fig.…”

“…Numerous studies have shown that gaze accuracy is unaffected by the passive application of head perturbations during an ongoing gaze shift (Tomlinson and Bahra, 1986;Pelisson et al, 1988;Tabak et al, 1996). Dynamic gaze feedback models incorporate this experimental result using their single feedback loop.…”

Coordination of eye and head components of movements evoked by stimulation of the paramedian pontine reticular formation

“…The gain was near unity for stimulation of the anterior zone but substantially suppressed, even negative, when stimulation was applied in the intermediate zone, which evoked large amplitude gaze shifts. Their results are more in line with the accepted notion that the VOR gain is dynamically attenuated during visually-guided gaze shifts (Laurutis and Robinson 1986;Pélisson and Prablanc 1986;Tomlinson and Bahra 1986;Guitton and Volle 1987;Pélisson et al 1988;Lefèvre et al 1992;Tabak et al 1996;Cullen 1998, 2002;. How can this discrepancy be resolved?…”

Nature of Variability in Saccades

“…1A and added dashed lines as our interpretation: the variations in peak velocity seem proportional to those in amplitude. We observed a similar pattern when plotting a main sequence from our earlier experiments (Tabak et al 1996).…”