Research group: Maaike de Vrijer, Pieter Medendorp en Jan van Gisbergen
Detecting true object motion during self-motion, although seemingly effortless, has to overcome two nontrivial problems. First, integrate the local motion information derived from an early fine-grain analysis (the motion seen through many ‘peepholes’) into a global motion pattern. Second, distinguish object motion from the effects of self-motion. So far, these problems have been seen as separable and amenable to sequential analysis. Here, we propose that it would be more optimal to solve them in conjunction. To evaluate this idea, we propose novel experiments exploring the conditions for the detection of true object motion during self-motion.
The project has just started.
Research group: Rens Vingerhoets, Pieter Medendorp and Jan Van Gisbergen
Major issues in the study of spatial orientation concern the questions of how the brain detects self movement and how this information is used to maintain a stable percept of external space. In this project, perceptual stability will be tested on a moment to moment basis while the subject is continuously rotated about a tilted (off-vertical) axis. In the absence of visual cues, the brain depends strongly on vestibular information to reconstruct head rotation and head position in space. The semicircular canals signal head rotation but they only detect angular acceleration so that their signal dies out as rotation continues. The otoliths detect linear acceleration forces but they cannot distinguish between the pull of gravity and the effect of translation. Interpretation of their ambiguous signal requires integration of available rotation signals by an internal model in the brain. When these body rotation signals are reliable, as during rotation in the light, percepts of body movement are roughly veridical. However, during fast off-vertical rotation in the dark (i.e., about a tilted axis), subjects have illusory translation and tilt percepts that do not correspond to the actual pure rotation stimulus. This combination of illusory effects has been interpreted in terms of incorrect otolith signal disambiguation in conditions where rotation information from the canals is misleading. To really test this canal-otolith interaction hypothesis, quantitative perceptual data at high temporal resolution are essential. The project is designed to provide such data for the first time. The major objective in collecting these data is to test to what extent current dynamic orientation models, which have been based and tested mainly on oculomotor data, can also be applied to perception.
Human spatial orientation relies on vision, somatosensory cues and signals from the semicircular canals and the otoliths. The canals measure rotation, while the otoliths are linear accelerometers, sensitive to tilt and translation. To disambiguate the otolith signal, two main hypotheses have been proposed: frequency segregation and canal-otolith interaction. So far these models were based mainly on oculomotor behavior. In this study we investigated their applicability to human self-motion perception. Six subjects were rotated in yaw about an off-vertical axis (OVAR) at various speeds and tilt angles, in darkness. During the rotation, subjects indicated at regular intervals whether a briefly presented dot moved faster or slower than their perceived selfmotion.
Based on such responses, we determined the time course of the selfmotion percept and characterized its steady-state by a psychometric function. The psychophysical results were consistent with anecdotal reports. All subjects initially sensed rotation, but then gradually developed a percept of being translated along a cone. The rotation percept could be described by a decaying exponential with a time constant of about 20 s. Translation percept magnitude typically followed a delayed increasing exponential with delays up to 50 s and a time constant of about 15s. The asymptotic magnitude of perceived translation increased with rotation speed and tilt angle, but never exceeded 14 cm/s. These results were most consistent with predictions of the canal-otolith interaction model, but required parameter values that differed from the original proposal. We conclude that canal-otolith interaction is an important governing principle for self-motion perception that can be deployed flexibly, dependent on stimulus conditions.
Rotation about an axis tilted relative to
gravity generates striking illusory motion percepts. As the initial percept
of body rotation gradually subsides, a feeling of being translated along a
cone emerges. The direction of the illusory conical motion is opposite to
the actual rotation.
Rotation about an axis tilted relative to gravity generates striking illusory motion percepts. As the initial percept of body rotation gradually subsides, a feeling of being translated along a cone emerges. The direction of the illusory conical motion is opposite to the actual rotation.
Vingerhoets, R.A.A. , Medendorp, W.P.
and Gisbergen J.A.M. van
Time course and magnitude of illusory translation perception during off-vertical axis rotation
J. Neurophysiol. 95: 1571-1587, 2006 (pdf)
Research group: Ronald Kaptein and Jan Van Gisbergen
The vestibular system is important for the detection of the direction of gravity and for the analysis of body movements, which generally consist of various combinations of rotations and translations. For this purpose, it has specialized sensors (canals and otoliths), but limitations in their coding properties complicate the analysis. The canal afferents are insensitive to low rotation frequencies. The otoliths, for elementary physical reasons, cannot distinguish between the inertial forces caused by translation and those exerted by tilt relative to gravity. Yet, this tilt/translation distinction is vital for survival. The problem how the brain achieves otolith disambiguation, a hot topic surrounded by controversy, is the central theme of this proposal. The project will investigate the consequences of shortcomings in the disambiguation process for spatial orientation and spatial localization.
Using vestibular sensors to maintain visual stability during changes in head tilt, crucial when panoramic cues are not available, presents a computational challenge. Reliance on the otoliths requires a neural strategy for resolving their tilt/translation ambiguity, such as canal-otolith interaction or frequency segregation. The canal signal is subject to bandwidth limitations. In this study, we assessed the relative contribution of canal and otolith signals and investigated how they might be processed and combined. The experimental approach was to explore conditions with and without otolith contributions in a frequency range with various degrees of canal activation.
We tested the perceptual stability of visual line orientation in six human subjects during passive sinusoidal roll tilt in the dark at frequencies from 0.05 to 0.4 Hz (30 deg peak-to-peak). Since subjects were constantly monitoring spatial motion of a visual line in the frontal plane, the paradigm required moment-to-moment updating for ongoing ego motion. Their task was to judge the total spatial sway of the line when it rotated sinusoidally at various amplitudes. From the responses we determined how the line had to be rotated to be perceived as stable in space. Tests were taken both with (subject upright) and without (subject supine) gravity cues.
Analysis of these data showed that the compensation for body rotation in the computation of line orientation in space, while always incomplete, depended on vestibular rotation frequency and on the availability of gravity cues. In the supine condition, the compensation for ego motion showed a steep increase with frequency, compatible with an integrated canal signal. The improvement of performance in upright, afforded by graviceptive cues from the otoliths, showed low-pass characteristics. Simulations showed that a linear combination of an integrated canal signal and a gravity-based signal can account for these results.
Linear summation of graviceptive and rotational cues.
First, separate estimates of the direction of gravity and angular velocity are obtained. These are weighted and added to obtain the estimate of head rotation. Two disambiguation strategies, frequency segregation and canal-otolith interaction, were simulated.
Both versions of the model can mimic the high-pass behavior in both conditions. The filter model, relying on frequency segregation for disambiguating the otolith signal, reproduces the low-pass characteristics of the otolith signal most accurately. To explain the data, both models require strong canal contribution.
Gisbergen, J.A.M. van
Interpretation of a Discontinuity in the Sense of Verticality at Large Body Tilt.
J Neurophysiol 91: 2205-2214, 2004
Kaptein, R.G. and
Gisbergen, J.A.M. van
Nature of the transition between two modes of external space perception in tilted subjects.
J. Neurophysiol. 93: 3356-3369, 2005
Kaptein, R.G. and
Gisbergen, J.A.M. van
Canal and otolith contributions to visual orientation constancy during sinusoidal roll rotation
J. Neurophysiol 95: 1936-1948, 2006 (pdf)
Vestibular Contributions to visual stability
PhD thesis, Radboud University Nijmegen, 2006 (pdf)
Research group: Anton van Beuzekom and Jan van Gisbergen
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 passively and actively-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.
Report We compared the ability of
passively-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 earth-vertical data were collected,
either by adjusting a visual line or by making saccades. In all spatial
orientation tests, whether involving space-perception or body-tilt judgments,
passively-tilted subjects made considerable systematic errors which mostly
betrayed tilt underestimation (Aubert-effect) and peaked near 130 deg tilt.
However, the Aubert-effect was much smaller in body tilt estimates than in
spatial oculomotor pointing, implying that the underlying signal processing
must have been different. Furthermore, in actively-tilted subjects, the body
tilt estimates became much better but space perception performance was
virtually identical to the passive tilt condition.
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.
Beuzekom AD, and Van Gisbergen JAM (1999)
Comparison of tilt estimates based on line settings, saccadic pointing and verbal reports.
Ann N Y Acad Sci 871: 451-454.
Van Beuzekom AD, and Van Gisbergen JAM (2000)
Properties of the internal representation of gravity inferred from spatial direction and body tilt estimates.
J Neurophysiol 84: 11-27.
Van Beuzekom AD, Medendorp WP, and Van Gisbergen JAM (2001)
The subjective vertical and the sense of self orientation during active body tilt.
Vision Research 41: 3229-3242.
Research group: Anton van Beuzekom and Jan Van Gisbergen
Rapid eye movements to different sensory inputs share a common final pathway. There is clear evidence that the pathways for saccades to visual, auditory and tactile targets have already converged at the level of the superior colliculus (SC) where movement vectors are coded spatially in a motor map. It is not clear whether this applies also to vestibularly induced rapid eye movements (quick phases). Neural activity related to quick phases has been demonstrated in the SC but its functional significance remains uncertain. Another possibility to be considered is that quick phase signals enter the saccadic pathway at a more peripheral stage where signals are coded temporally, separately for each component, i.e. at the level of burstcells. Accordingly, there are at least two levels of possible interaction between visual and vestibular signals for the generation of rapid eye movements (vector and component stage). When both visual and vestibular inputs impinge on the system, interesting interactions occur whose precise nature and neural basis have hardly been studied. This project was designed to study these interactions behaviorally and neurophysiologically. Our aim was to elucidate how the SC participates in the control of vestibularly induced rapid eye movements and to clarify to what extent this role and the interaction findings can be reconciled with its role in foveation.
Report To investigate these issues, we have studied in the monkey to what extent saccades induced by electrical microstimulation in the SC (E-saccades) can be modified by concurrent sinusoidal rotation about a vertical axis. We found clear kinematic effects which cannot readily be understood by interactions at this level. Vectorial peak velocity in E-saccades of a given amplitude increased with head velocity for rotations into the half field where the saccade was directed and decreased for rotation in the opposite direction. Interestingly, this effect was due to a specific effect on the horizontal component; the vertical component did not show systematic kinematic changes. We suggest that the kinematic effect may be due to preparatory quick-phase signals, impinging at the burstcell level, that become expressed once the pause cell gate has been opened by collicular signals. If interaction at a collicular level were responsible for the kinematic effects, one would expect comparable effects in both components. To explore the nature of visuo-vestibular interactions further, we have investigated how the human saccadic system copes with the interfering effects of ongoing horizontal nystagmus when attempting to generate oblique prosaccades or antisaccades. The results suggest that voluntary and reflexive rapid eye movements can be programmed in parallel. The outcome of this process shows a degree of independence between horizontal and vertical components which is not readily understandable in terms of interactions at a vectorial coding stage such as in the collicular map.
Beuzekom AD, and Van Gisbergen JAM (2002)
Collicular microstimulation during passive rotation does not generate fixed gaze shifts.
J Neurophysiol , 87, 2946-2963, 2002.
Van Beuzekom AD, and Van Gisbergen JAM (2002)
Interaction between visual and vestibular signals for the control of rapid eye movements.
J Neurophysiol., 88, 306-322, 2002.
Research group: Vivek Chaturvedi and Jan Van Gisbergen
It is generally assumed that, at a peripheral level, two distinct oculomotor control systems are involved in the execution of binocular gaze shifts in three dimensions. When the target movement calls only for a change in gaze direction, the movement is controlled by the fast saccadic system. Target changes in depth elicit slow vergence movements. When both subsystems are called into action by a target step in 3D (direction and depth component) they do not act independently: Their responses show non-additive dynamic behaviour in that the vergence component is now clearly faster. The aim of this project was to investigate various aspects of the coupling between the two systems relying on both behavioural analysis and on neurophysiological studies.
Report We investigated the role of the monkey superior colliculus (SC) in the control of combined saccade-vergence movements by assessing the perturbing effects of microstimulation. We elicited an electrical saccade by stimulation while the monkey was preparing a visually-guided movement to a near visual target. We showed that that artificial intervention in the SC, while a 3D refixation is prepared or is ongoing, can effect the timing (WHEN) and the metric-specification (WHERE) of both saccades and vergence. This effect would be expected if the population of movement cells at each SC site is tuned in 3D, combining the well-known topographical code for direction and amplitude with a nontopographical depth representation. For an eye movement to a near target, stimulation at a rostral site leds to a significant suppression of the pure vergence response during the period of stimulation. When these paradigms were implemented for 3D refixations, the saccade was inactivated, as expected, while the vergence component was often suppressed more than in the case of the pure vergence. We conclude that the rostral SC, presumably indirectly via connections with the pause neurons, can affect vergence control for both pure vergence and combined 3D responses..
V, and Van Gisbergen JAM (1998)
Shared target selection for combined version-vergence eye movements.
J Neurophysiol 80: 849-862
Chaturvedi, V. and Van Gisbergen, J.A.M. (1999)
Perturbation of combined saccade-vergence movements by microstimulation in monkey superior colliculus.
J. Neurophysiol. 81: 2279-2296.
Chaturvedi, V. and Van Gisbergen, J.A.M.
Stimulation in the rostral pole of monkey superior colliculus: effects on vergence eye movements.
Exp. Brain Res. 132:72-78, 2000.
Research group: J.A.M. van Gisbergen, C.C.A.M. Gielen
Fixating a visual target during head movements requires specific eye movements in order to compensate for movements of the eyes relative to the target. Several sensory systems (e.g. semi-circular canals, otolith system, visual system, muscle spindles in neck muscles) contribute to the accurate stabilization of gaze on targets in 3-D space. The aim of this project is 1) to investigate the characteristics of eye movements in gaze stabilization in natural head movements and 2) to determine the role of various sensory systems to gaze stabilization.
We have investigated gain modulation (context compensation) of the vestibulo-ocular reflex (VOR) for binocular gaze stabilization in human subjects during voluntary yaw and pitch head rotations. Movements of each eye were recorded both when attempting to maintain gaze on a small visual target in a darkened room and after its disappearance (remembered target).
Linear regression analysis on the version gain as a function of target distance yielded a slope representing the influence of target proximity and an intercept corresponding to the response at zero vergence (default gain). The slope of the fitted relationship, divided by the geometrically-required slope provided a measure for the quality of version context compensation ('context gain'). In both yaw and pitch experiments, we found default version gains close to one even for the remembered target condition, indicating that the active VOR for far targets is already close to ideal without visual support. In near target experiments, the presence of visual feedback yielded near unity context gains, indicating close to optimal performance. For remembered targets, the context gain deteriorated but was still superior to performance in corresponding passive studies reported in the literature.
We examined how frequency and target distance, estimated from the vergence angle, affected the sensitivity and phase of the version component of the translational VOR (tVOR) and compared the results to the requirements for ideal performance. Linear regression analysis of the version-sensitivity relationship yielded a slope representing the influence of target distance. The ratio of this slope and the slope required for ideal stabilization provided a measure for the degree of 'distance compensation' in the tVOR. The results show that distance compensation behaves according to low-pass characteristics in each target condition. It declined from 1.00 to 0.84 for visual targets and from 0.87 tot0.57 for remembered targets in the frequency range 0.25 - 1.5 Hz. The intercept obtained from the regression yielded the tVOR response at zero vergence and specified the 'default sensitivity' of the tVOR. Default sensitivity increased with frequency from 0.02 to 0.10 deg/cm for visual targets and from 0.04 to 0.16 deg/cm in darkness. The phase delays of version angular eye velocity relative to translational eye velocity increased on average from 2 deg to 7 deg. In comparison with earlier passive studies, the active tVOR in the dark performs much better at all frequencies where comparison was possible. We conclude that an additional nonvestibular signal with low-pass characteristics contributed to the tVOR during self-generated head translations.
Medendorp, J.D. Crawford, D.Y.P. Henriques, J.A.M. van Gisbergen, C.C.A.M.
Kinematic strategies for upper arm-forearm coordination in three dimensions.
J. Neurophysiol. 84, 2302-2316, 2000.
W.P. Medendorp, J.A.M. van Gisbergen, S. van Pelt, C.C.A.M. Gielen
Context compensation in the vestibulo-ocular reflex during active head rotations.
J. Neurophysiol. 84, 2904-2917, 2000.
W.P. Medendorp, J.A.M. van Gisbergen, C.C.A.M. Gielen
Human gaze stabilization during active head translations.
J. Neurophysiol. 87, 295-304, 2002.