The otolith organs of the vestibular system signal dynamic translational head acceleration and head orientation with respect to the gravitational vector. The direct measurements of visual acuity during whole-body translation (Chapter 6) provided the first psychophysical demonstration that otolithic inputs are used to stabilize vision during head acceleration. A second role of the otolith organs is to assist in the control of human posture as has been clearly demonstrated from studies in astronauts showing that the altered otolith input (gravitational otolith inputs are reduced by a minimum of a thousand-fold in orbit) is the source of the postural imbalance observed in astronauts upon landing from shuttle flight (Paloski et al. 1993).
Since the otolith organs play a significant role both for vision and postural control, it is important to be able to identify pathophysiology in patients with suspected otolithic disease (e.g. reports of abnormal sensation of tilt) and therefore to find reliable indicators of normal otolith function. Both sensations and reflexes (postural and ocular) associated to head motion can in theory provide such indicators. Since the brain integrates signals provided by the otolith organs with inputs fi-om other sensory modalities yielding an integrated picture of body motion and position, investigations of otolith function have to take into account other sensory inputs such as vision, somatosensory receptors or concurrent semicircular canal stimulation. For perceptual experiments, these extraneous cues have to be minimized to bring out the role of the otolith organs, while studies on reflex responses can utilize them to enhance signs of otohth function.
Perception of motion reUes on sensory inputs, central processing of the afferent signals and also on factors such as mental state of the subjects or habituation to the stimuh. Thus, all these factors have to be taken into account, when one tries to relate perceptual measurements to the known mechanism of a specific sensory organ.
The study reported in Chapter 3 underlined the difilculty in assuring appropriate stimulation of the vestibular system while minimizing motion cues given by other sensory inputs. Visual, auditory, extraneous head movements and differential movements of parts of the body were eliminated but somatosensory and vibration cues were more difficult to control. To reduce somatosensory information, form-fitting molds could be used to spread out tactile cues over a large
contact area, thereby keeping relatively small the peak pressure at any one part of the skin. Elimination of vibrations and frictional contacts will be more difficult to achieve since it will ideally require the construction of a new acceleratoiy device perhaps based on air bearing technology.
The measurements of motion perception reported in Chapter 3 showed a high intra- and inter-subject variability, which was probably partly due to the difficulty in signaling when a sensation begins. A second problem associated with response latency measurements is the difficulty in providing accurate estimates of the subjects’ reaction times, i.e. the delays between perception and indication of motion. Thus, such perceptual measures strongly depend on the subjects’ willingness to guess or to wait before hazarding an opinion. Forced-choice methods in which perceptual indications are given either once the stimulus has been completed or at a specific time during the stimulus can help to reduce the variability of the results. Psychophysical procedures based on signal detection theory have also been developed to try to take into account inter-subject differences in performing well-defined tasks. In a signal detection experiment, the experimenter presents a signal only on some trials, e.g. on 50% of the trials in a given session. If the subjects are very willing to guess, they will often report that they detect the stimulus even when none was presented; the ‘guessing’ strategy adopted by the subject depends upon factors such as rewards/punishments associated with particular responses and knowledge of the probability that a stimulus will be presented. The selected strategy can be estimated from the responses given by the subjects for the trials without stimulus. Procedures from the signal detection theory have not been widely used so far to study the perception of whole-body motion. This is probably partly due to the difficulty in finding an adequate absent’ stimulus since motion usually involves vibration which creates the problem of differentiating between motion perception and perception of vibration inherent to the stimulus. One way to try to get round this obstacle would be to vibrate the motion device even when it is not moving, as a control condition, but the matching of vibration with and without motion will be extremely difficult to achieve. A second reason for the lack of signal detection procedures in vestibular research may originate from the use in this technique of frequent and brief stimuli: motion stimuli are complex in the sense that they are only fully characterized by several related parameters (acceleration, velocity, frequency content) and therefore as discussed in Chapter 3, brief stimuli may create high acceleration gradients which can, for instance, hinder a perception process based on velocity information.
The perceptual experiments presented in this thesis suggested that for low initial gradients of acceleration and acceleration levels higher than >10 cm/s^, motion detection occurs when a velocity threshold is reached. However, as mentioned in Chapter 3, since measurements were based on latency of the subject’s responses, one cannot conclude that response latencies were governed by a true integration of the otolithic signal rather than by the time required for central processing. This latter explanation is based on models proposed to account for the inverse dependence of response time on strength of the stimulus (Laming 1973), as observed for acoustic stimuli (Sanford 1972): some specific feature of the stimulus is integrated over successive temporal intervals until the
Chapter Eight - Conclusion
accumulated value exceeds a critical limit; the point in time at which the subject signals detection is then governed by the decision procedure.
It might be argued that our measurements were influenced by habituation phenomena, i.e. decrease of the feeling of motion due to sustained acceleration. However, such effects which have been reported for angular motion only occurred for stimulus duration exceeding 30 s (Guedry 1974). Since the mean response latencies of our subjects were less than 3 s and since each motion stimulus included an abrupt deceleration followed by a return of the chair at supraliminal acceleration at the centre of the tract, habituation phenomena were probably negligible in our study.
In summary, a well-controlled experiment carried out with a device specially designed for perceptual studies and employing a more elaborate psychophysical procedure may increase the differences in motion perception between normal subjects and patients without loss of vestibular function. However, the need for a very specialized equipment implies that a test of the otolith organs based on perception will be diflicult to use for routine clinical investigations.
The investigations based on eye movement responses to linear acceleration (Chapters 4-7) provided more encouraging results for the development of a reliable test of otolith function as they showed clear differences between normal subjects and patients with vestibular disorders. A second advantage of these studies over perceptual experiments was their short duration.
In normal subjects, it was found that the LVORs evoked during transient inter-aural accelerations are from onset increased with acceleration magnitudes and target distances and could be slightly suppressed with head-fixed targets. It was also shown that simultaneous head rotation enhanced the early eye movement responses to translational head acceleration. The summary findings obtained in three groups of patients investigated in the different experiments are as follows:
1) Patients with complete loss of vestibular function had no short-latency LVORs and no eye movements in the dark; their results proved the vestibular origin of the ocular responses in normal subjects.
2) Patients with bilaterally absent responses to caloric testing presented mild to severe abnormalities of the LVORs.
3) The asymmetrical LVOR responses observed in patients tested shortly after unilateral vestibular neurectomy led us to suggest a functional polarization of the utricule in human subjects.
4) Patients suffering from benign paroxysmal positional vertigo, which is assumed to result from utricular damage, were also tested (Appendix K, Anastasopoulos et al. 1997). No pronounced abnormality was observed in the eye movements evoked during isolated translational acceleration.
These results in patients indicate that incomplete damage of otolith function remains difBcult to detect, probably due to compensation mechanisms; e.g. unilateral damage was only observed in the acute stage.
Data for the LVOR responses to interaural acceleration were obtained for motion in darkness and in the light. The advantage of tests in darkness is that due to the absence of visual following, measurements can be made when strong ocular responses are present. Its drawback is the variability of response magnitudes observed in normal subjects which prevents the detection of mild otolithic impairment.
By providing a strong visual context, thereby reducing the variability of the normative data, tests with target fixation seem likely to yield more precise diagnostics of otolith fimction. However, only the search-coil recording technique produces accurate and reliable measurements of the short latency responses present before visual following contributes to target fixation; alternative recording techniques are not useful, either because they cannot be properly secured on the subject’s head during abrupt acceleration (infra-red detectors) or because they have a low temporal resolution (video-oculography). EOG can be employed, but because of its inherent noise levels, only measurements of severely impaired eye movements are possible. At present, eye search-coils are not widely available. They are also cumbersome to use and not tolerated by every subject. Alternative techniques could be sought, such as the use of a light-weight accelerometer taped over the closed ^ e lid of one eye (Brown and Day, 1997). This approach might provide both convenience of use and accurate measurements.
Chapter 4 presented the first and so far only study on suppression of short-latency LVORs. Future projects in this area could explore the influence of predictability of the relative target motion on the suppression gain; this would be similar to the experiments reported by Gauthier and Vercher (1990) who showed that the early angular VOR suppression is not observed when visual context (earth-fixed vs. head-fixed target) is unpredictable. Also, the LVOR is known to be dependent on other sensory inputs, e.g. acoustic cues (Buizza et al. 1979), so it would be interesting to investigate whether strong tactile cues indicating that the target will remain stationary with respect to the subject can enhance LVOR suppression: to do so, the subjects could hold the visual target which will remain fixed to the acceleratoiy device. Finally, by employing different ^ ^ s of visual targets, the relative importance of peripheral and central vision for LVOR suppression could be e^glored. The main drawbacks for all these studies are that search-coil recordings will be required since eye movements are expected to be small and a proper head stabilization removing any extraneous rotational head movements will have to be assured.
The psychophysical ejq)eriment presented in Chapter 6 has the advantage of being quick to perform and easy to analyze. This technique demonstrated the usefiilness of LVORs in visual stabilization but yielded only rough estimates of otolith function in patients. Thus, it could be used to quickly assessed the severity of otolith impairment but eye movement recordings will have to be employed concurrently to provide more detailed information.
Chapter Eight - Conclusion
From the LVORs in patients who underwent unilateral vestibular nerve section, it was concluded that compensation for the loss of LVORs for acceleration towards the lesioned side might be achieved through the use of the signals provided by the bending in their off-direction of the hair- cells located in the lateral part of the utricular macula. However, the possibility that the medial part of the utricule also plays a role in this recovery process caimot be excluded. To understand better the compensation process for the loss of one utricule, it would be interesting to cany out two tests of otolithic function in a same group of patients. For instance, the comparison of the time courses of recovery for the linear VORs produced by translational acceleration and for ocular torsion evoked during centrifugation may help to clarify the bases of the compensation mechanisms.
Clinical research into the LVORs is just at its begirming. To further our understanding of this reflex which as we have shown does contribute to the complex task of maintaining stable vision during head motion, future studies should involve patients with circumscribed lesions of the central visual and vestibular pathways. At present, the most critical concerns for the establishment of a reliable test of otolith function seem to be the need for accurate and user-friendly eye movement recording techniques and the availability of devices providing well-controlled head acceleration. While linear acceleratory devices are currently not readily available, rotating chairs are widely used for routine clinical investigations of vestibular fimction. Therefore, eccentric rotation with the head placed away from the axis (as employed in Chapter 7) provides at present a more convenient and easier way to carry out clinical evaluation of otolithic ^sfim ction (Barrat et al. 1987, Koizuka et al. 1993). However, eccentric rotation is far from ideal to provide accurate diagnoses, since: 1) translational acceleration is combined with head rotation and centripetal acceleration and is therefore not as pure a stimulus as isolated whole-body translation, 2) proper control of head position and movement is difBcult to achieve, 3) it is not possible to differentiate between abnormally low LVOR and absent interaction between utricular and canalicular afferents.
References specific to the General conclusion:
Laming D (1973) Mathematical psychology. London: Academic Press.
Paloski WH, Black FO, Reschke MF, Calkins DS, Shupert C (1993) Vestibular ataxia following shuttle flights: effects of microgravity on otolith-mediated sensorimotor control of posture. Am. J. Otol. 14:9-17.
Sanford AJ (1972) Loudness and simple reaction time. Sound 6:92-96