Interaction between visual and vestibular signals for the control of rapid eye movements.

To investigate interactions between voluntary and reflexive eye movements, five subjects were asked to make pro- or anti-saccades to various oblique locations cued by a head-fixed flash while being rotated sinusoidally in yaw (0.17 Hz; 73 degrees /s peak velocity) in complete darkness. Eye movements were recorded with the coil technique. In the pro-saccade task, targeting responses showed clear compensation for the intervening nystagmus, but there was a marked increase in horizontal scatter. Most quick phases directed into the hemifield opposite to the flash (away trials) were suppressed from ~100 ms onward. By contrast, quick phases directed into the hemifield of the flash (toward trials) continued virtually unabated until visually triggered saccades began to appear. From 80 ms onward, these vestibularly triggered movements showed signs of metrical modification by the visual signal. In the anti-saccade experiments, suppression of quick phases away from the flash was just as strong as in the pro-saccade experiments, and error rates in these trials were almost as low as in stationary control conditions. Suppression of quick phases directed toward the flash was a new phenomenon that emerged only in anti-saccade experiments. Since this inhibition had a late onset and was only partial, error rates in anti-saccade toward trials were very high. At short latencies, both components of most rapid eye movements were wrongly directed toward the flash. This was followed by a stage with frequent incongruent responses in which unsuppressed quick phases provoked an incorrect horizontal movement, whereas the vertical component showed a correct anti-saccade response. At still longer latencies, most responses were correct in both components. The visual modification of short-latency responses in both tasks showed that rapid eye movements could not simply be classified as either voluntary or reflexive, but suggested that signals underlying each class could merge into a compromise response. That vestibular rotation during the anti-saccade task may cause a wrongly directed horizontal component resembling a quick phase, combined with a vertical component expressing a correct anti-saccade signal, reveals a remarkable independence at the component level. These observations suggest that voluntary and involuntary movements can be programmed in parallel. This behavior is explained most parsimoniously by assuming that the two signals converge at a component-coding stage of the system, rather than at a vectorial coding stage.

Collicular microstimulation during passive rotation does not generate fixed gaze shifts.

We investigated whether saccades evoked by electrical stimulation (E-saccades) in the superior colliculus can compensate for passive sinusoidal head rotation in yaw so as to keep the rapid gaze shift constant. After accounting for variations in E-saccade onset position, we found significant horizontal metric changes, proportional to head velocity, in 31 of 37 experiments in 2 monkeys. Vertical effects were small. In a substantial fraction of the experiments (14/37), these metric changes represented significant but often insufficient compensatory adjustments in the horizontal component, opposite to the direction of head movement. However, very robust violations of gaze-shift constancy were remarkably common: significant anticompensatory changes in the horizontal component occurred in 17/37 experiments. In these cases, typically involving larger E-saccades, the horizontal component increased in size with rotation into the half field containing the E-saccade and became smaller during opposite rotation. Further analysis showed that, instead of showing a dichotomy, the metric effect actually varied along a continuum from compensatory to strongly anticompensatory. In addition to these metric changes, we found a robust kinematic effect of head rotation in metrically matched E-saccades. In all experiments where the effect was significant (34/37), horizontal peak velocity increased for rotation into the half field where the E-saccade was directed and decreased for opposite rotation. This kinematic effect was again proportional to head velocity and predominant in the horizontal component. Comparison of yaw and pitch rotation at the same stimulation site showed that both expressions of vestibular-saccade interaction (metric and kinematic) tended to align with the direction of rotation. The component-specific nature of the modulation suggests that the effects may have been caused by convergence of saccadic and vestibular signals at a component-coding stage downstream of the colliculus. We suggest that the quick-phase system got access to the common pulse generator as soon as the collicular stimulation had opened the pause-cell gate. Adding such an anticompensatory signal would act to increase the E-saccade horizontal component when the monkey was rotated in the same direction and bring about a decrease in size and peak velocity when it was opposite. In the large majority of experiments the metric changes failed to maintain gaze-shift constancy, either because they were in the wrong direction or because they were too small. Possible reasons for this major departure from the properties of natural gaze shifts are discussed.

The subjective vertical and the sense of self orientation during active body tilt.

Previous testing of the ability to set a luminous line to the direction of gravity in passively-tilted subjects, in darkness, has revealed a remarkable pattern of systematic errors at tilts beyond 60 degrees, as if body tilt is undercompensated or underestimated (Aubert or A-effect). We investigated whether these consistent deviations from orientation constancy can be avoided during active body tilt, where more potential cues about body tilt (e.g. proprioception and efference copy) are available. The effects of active body tilt on the subjective vertical and on the perception of self tilt were studied in six subjects. After adopting a laterally-tilted posture, while standing in a dark room, they indicated the subjective vertical by adjusting a visual line and gave their verbal estimate of head orientation, expressed on a clock scale. Head roll tilts covered the range from -150 degrees to +150 degrees. The subjective vertical results showed no sign of improvement. Actively-tilted subjects still exhibited the same pattern of systematic errors that characterised their performance during passive tilt. Random errors in this task showed a steep monotonic increase with tilt angle, as in earlier passive tilt experiments. By contrast, verbal head-tilt estimates in the active experiments showed a clear improvement and were now almost devoid of systematic errors, but the noise level remained high. Various models are discussed in an attempt to clarify how these task-related differences and the selective improvement of the self-tilt estimates in the active experiments may have come about.

Properties of the internal representation of gravity inferred from spatial-direction and body-tilt estimates.

One of the key questions in spatial perception is whether the brain has a common representation of gravity that is generally accessible for various perceptual orientation tasks. To evaluate this idea, we compared the ability of six tilted subjects to indicate earth-centric directions in the dark with a visual and an oculomotor paradigm and to estimate their body tilt relative to gravity. Subjective earth-horizontal and -vertical data were collected, either by adjusting a visual line or by making saccades, at 37 roll-tilt angles across the entire range. These spatial perception responses and the associated body-tilt estimates were subjected to a principal-component analysis to describe their tilt dependence. This analysis allowed us to separate systematic and random errors in performance, to disentangle the effects of task (horizontal vs. vertical) and paradigm (visual vs. oculomotor) in the space-perception data, and to compare the veridicality of space perception and the sense of self-tilt. In all spatial-orientation tests, whether involving space-perception or body-tilt judgments, subjects made considerable systematic errors which mostly betrayed tilt underestimation [Aubert effect (A effect)] and peaked near 130 degrees tilt. However, the A effect was much smaller in body-tilt estimates than in spatial pointing, implying that the underlying signal processing must have been different. Pointing results obtained with the visual and the oculomotor paradigm were not identical either, but these differences, which were task-related (horizontal vs. vertical), were subtle in comparison. The tilt-dependent pattern of random errors (noisy scatter) was almost identical in visual and oculomotor pointing results, showing a steep monotonic increase with tilt angle, but was again clearly different in the body-tilt estimates. These findings are discussed in the context of a conceptual model in an attempt to explain how the different patterns of systematic and random errors in external-space and self-tilt perception may come about. The scheme proposes that basically similar computational mechanisms, working with different settings, may be responsible.