Body sway responses to pseudorandom support surface translations of vestibular loss subjects resemble those of vestibular able subjects.

Body sway responses evoked by a horizontal acceleration of a level and firm support surface are particular in that the vestibular information on body-space angle BS resembles the proprioceptive information on body-foot angle BF. We compared corresponding eyes-closed responses of vestibular-able (VA) and vestibular-loss (VL) subjects, postulating a close correspondence. In contradistinction to previous studies, we used an unpredictable (pseudorandom) stimulus and found that the eyes-closed and eyes-open responses of the VA closely resembled those of the VL subjects, as expected. We further conclude that the vestibular signals coding head linear translation in VA subjects has in this case too little functional relevance to cause a notable difference between the subject groups.

Targeting head movements in humans: Compensation for disturbance from simultaneous body rotations.

Vestibular information plays an important role in spatially oriented motor control and perception. With regard to reorienting head movements, little is known of (1) how vestibular mechanisms compensate for disturbances from concurrent passive trunk rotations (e.g. in a veering vehicle), and (2) whether and how this disturbance compensation is related to the perception of body orientation in space. We here address these two questions in a single experiment. Six healthy subjects (Ss) seated on a turning chair in darkness performed two tasks. (1) Head pointing: Ss made swift head movements in darkness towards the angular position in space of a previously shown visual target. These movements were disturbed by concurrent rotations of the chair, and hence the trunk, which were driven by scaled down versions of the Ss' own head-on-trunk rotations. Although unaware of the disturbance, Ss adjusted their head movements so as to attenuate its effect on head-in-space (HS) position by about 45%. (2) Visual straight ahead (VSA): Using a light pointer, Ss indicated their VSA before each head-pointing trial and tried to reproduce it after the trial. In all Ss, VSA accounted for the disturbing trunk rotation, although to individually varying degrees. No correlation could be detected between VSA reproduction and motor performance, neither within nor across subjects. A vestibular loss subject who performed the same two tasks made no compensatory movements during head pointing and did not account for the disturbance of his HS position during VSA reproduction. Three concepts of vestibular information processing for head movement control were explored with regard to their compatibility with the head-pointing results: (1) Conventional negative feedback, (2) Interaction with an efference copy, and (3) Interaction with neck proprioceptive information. Theoretical analyses and model simulations indicated that all three concepts can explain the observed disturbance compensation. However, they differ in terms of control stability in the presence of feedback time delays, with (3) being best and (1) worst. The different concepts might correspond to fast simple and slower complex compensation mechanisms, respectively, and possibly complement each other during natural behaviours. VSA reproduction may be based on analogous processing principles, but appears to involve different neural circuitries.

Human stance control beyond steady state response and inverted pendulum simplification.

Systems theory analyses have suggested that human upright stance can be modelled in terms of continuous multi-sensory feedback control. So far, these analyses have considered mainly steady-state responses to periodic stimuli and relied on a simplifying model of the body's mechanics in the form of an inverted pendulum. Therefore, they may have ignored relevant aspects of the postural behaviour. To prove a more general validity of a stance control model that we previously derived from such analyses, we now presented subjects with static-dynamic stimulus combinations and assessed response transients, anterior-posterior (a-p) response asymmetries, and possible deviations from the 'inverted pendulum' simplification (by measuring hip and knee bending). We presented normal subjects (Ns) and vestibular loss patients (Ps) with a-p support surface tilt on a motion platform under the instruction to maintain, with eyes closed, the body upright in space. In addition, subjects were to indicate perceived platform tilt with the help of pointers. We combined a fixed-amplitude sinusoidal tilt (0.1 Hz) with static tilts that were varied in amplitude and direction. We recorded upper body (shoulder) and lower body (hip) excursions in space and centre of pressure (COP) shift, and calculated the centre of mass (COM) angular excursion. We found that: (1) Immediately prior to stimulus onset (which was highly predictable), subjects showed a small anticipatory forward lean. (2) The subsequent transient response consisted of two parts. First, the body was moved along with the platform tilt and then, in the second part, the body excursion was braked by starting tilt compensation. Upon increasing tilt amplitude, the braking point showed a pronounced saturation with for-aft asymmetry. (3) During the following prolonged tilt, the tonic body excursions saturated with increasing static tilt amplitude. This saturation also showed a for-aft asymmetry (backwards saturation more pronounced). In contrast, the dynamic body excursions did not depend on the static tilt stimulus. (4) Tilt compensation occurred mainly in the ankle joints, but also involved small synergistic bendings in hips and knees in fixed register to the ankle rotation. (5) After the end of the stimulus, the body returned towards primary position, followed by a pronounced and slowly decaying tonic overshoot which was mainly related to tilt amplitude and initial tonic body excursion. (6) The responses of Ps qualitatively resembled those of Ns, apart from larger body excursions, less pronounced saturations, and less for-aft asymmetries. (7) Perceived platform tilt of Ns and Ps was correlated with their postural tilt compensations, but unlike the postural responses the perceptual responses overestimated actual static and dynamic tilt by a factor of 3-4. Our findings suggest two, so far undescribed and highly nonlinear mechanisms in human stance control. (a) The braking during the transient response appears to reflect a 'sensory reweighting switch' by which subjects change from a control that is referenced to the support to one that is referenced to space. (b) The saturation of the tonic body excursion also reflects a sensory reweighting mechanism; by this, subjects keep their balancing within a certain excursion limit. The two mechanisms were originally not predicted by our stance control model, but do not invalidate it, because they can simply be added to it. Also the observed for-aft asymmetries can be accounted for (by making thresholds in the two mechanisms asymmetric). In its extended form, the model mimics the previous and the new findings. We also conclude that the 'inverted pendulum' simplification is a legitimate simplification. We demonstrate the utility of the model by implementing it into a humanoid robot that then mimics closely the human experimental data. Finally, we present a hypothetical concept on sensory reweighting mechanisms in human stance control, which is meant to serve as a framework for future research.

A cognitive intersensory interaction mechanism in human postural control.

Human control of upright body posture involves inputs from several senses (visual, vestibular, proprioceptive, somatosensory) and their central interactions. We recently studied visual effects on posture control and their intersensory interactions and found evidence for the existence of an indirect and presumably cognitive mode of interaction, in addition to a direct interaction (we found, e.g., that a 'virtual reality' visual stimulus has a weaker postural effect than a 'real world' scene, because of its illusory character). Here we focus on the presumed cognitive interaction mechanism. We report experiments in healthy subjects and vestibular loss patients. We investigated to what extent a postural response to lateral platform tilt is modulated by tilt of a visual scene in an orthogonal rotational plane (anterior-posterior, a-p, direction). The a-p visual stimulus did not evoke a lateral postural response on its own. But it enhanced the response to the lateral platform tilt (i.e., it increased the evoked body excursion). The effect was related to the velocity of the visual stimulus, showed a threshold at 0.31 degrees /s, and increased monotonically with increasing velocity. These characteristics were similar in normals and patients, but body excursions were larger in patients. In conclusion, the orthogonal stimulus arrangement in our experiments allowed us to selectively assess a cognitive intersensory interaction that upon co-planar stimulation tends to be merged with direct interaction. The observed threshold corresponds to the conscious perceptual detection threshold of the visual motion, which is clearly higher than the visual postural response threshold. This finding is in line with our notion of a cognitive phenomenon. We postulate that the cognitive mechanism in normals interferes with a central visual-vestibular interaction mechanism. This appears to be similar in vestibular loss patients, but patients use less effective somatosensory instead of vestibular anti-gravity mechanisms.

Pronounced overestimation of support surface tilt during stance.

A veridical internal notion of the kinematic state of the foot support is essential for postural control. The means by which this is obtained is still a matter of debate. We therefore measured the conscious perception of support tilt during transient anterior-posterior rotations of a motion platform in six healthy subjects, using a psychophysical matching procedure. Furthermore, we evaluated subjects' postural responses (in terms of displacement of subjects' center of mass, COM, and their ankle torque, as represented by the center of foot pressure, COP). The platform tilts were applied in absence of visual and auditory orientation cues. The platform rotations consisted of smoothed position ramps with different dominant frequencies (0.025, 0.05, 0.1, 0.2, 0.4, and 0.8 Hz) and different amplitudes (0.125 degrees, 0.25 degrees, 0.5 degrees, 1 degree, 2 degrees, 4 degrees, and 8 degrees) for the forward and backward directions, which yielded a 6x14 stimulus matrix. The stimuli were repeated five times in a random order. For the matching procedure, subjects tried to maintain an upright body orientation, while trying to orient a light-weight rod, which was attached to a belt around their waists, parallel to the perceived platform surface. We measured the stimulus-evoked angular excursions of the rod and of the subjects' COM as well as the COP shift. We found that the subjects' rod indications overestimated the platform tilts, particularly with small stimulus amplitudes. To characterize the overestimation, we compared the rod indications obtained while subjects stood on the tilting platform, to rod indications in a situation in which they stood next to the platform and tried to match the rod angle to the now visually perceived platform angle. From this comparison, we inferred that the subjects' kinesthetically derived notion of platform tilt overestimates the actual tilt by a factor of approximately 4. The estimates were linearly related to the angle between body (COM) and platform, i.e., to approximately the angle of the ankle joint, a finding which suggests a proprioceptive source of the overestimation. Further analyses supported this view; they showed that the onset latencies of the rod indications could be approximated by a theoretical indication mechanism with a reaction time of about 0.31 s, a velocity threshold of 0.099 degrees/s, and a displacement threshold of 0.12 degrees. These threshold values are well in line with previous work on the leg proprioceptive detection threshold of conscious perception of body sway. We therefore assume that the phenomenon of support tilt overestimation reflects a still unknown mechanism of leg proprioception in postural control.

Multisensory control of human upright stance.

The interaction of different orientation senses contributing to posture control is not well understood. We therefore performed experiments in which we measured the postural responses of normal subjects and vestibular loss patients during perturbation of their stance. Subjects stood on a motion platform with their eyes closed and auditory cues masked. The perturbing stimuli consisted of either platform tilts or external torque produced by force-controlled pull of the subjects' body on a stationary platform. Furthermore, we presented trials in which these two stimuli were applied when the platform was body-sway referenced (i.e., coupled 1:1 to body position, by which ankle joint proprioceptive feedback is essentially removed). We analyzed subjects' postural responses, i.e., the excursions of their center of mass (COM) and center of pressure (COP), using a systems analysis approach. We found gain and phase of the responses to vary as a function of stimulus frequency and in relation to the absence versus presence of vestibular and proprioceptive cues. In addition, gain depended on stimulus amplitude, reflecting a non-linearity in the control. The experimental results were compared to simulation results obtained from an 'inverted pendulum' model of posture control. In the model, sensor fusion mechanisms yield internal estimates of the external stimuli, i.e., of the external torque (pull), the platform tilt and gravity. These estimates are derived from three sensor systems: ankle proprioceptors, vestibular sensors and plantar pressure sensors (somatosensory graviceptors). They are fed as global set point signals into a local control loop of the ankle joints, which is based on proprioceptive negative feedback. This local loop stabilizes the body-on-foot support, while the set point signals upgrade the loop into a body-in-space control. Amplitude non-linearity was implemented in the model in the form of central threshold mechanisms. In model simulations that combined sensor fusion and thresholds, an automatic context-specific sensory re-weighting across stimulus conditions occurred. Model parameters were identified using an optimization procedure. Results suggested that in the sway-referenced condition normal subjects altered their postural strategy by strongly weighting feedback from plantar somatosensory force sensors. Taking this strategy change into account, the model's simulation results well paralleled all experimental results across all conditions tested.

Human postural responses to motion of real and virtual visual environments under different support base conditions.

The role of visual orientation cues for human control of upright stance is still not well understood. We, therefore, investigated stance control during motion of a visual scene as stimulus, varying the stimulus parameters and the contribution from other senses (vestibular and leg proprioceptive cues present or absent). Eight normal subjects and three patients with chronic bilateral loss of vestibular function participated. They stood on a motion platform inside a cabin with an optokinetic pattern on its interior walls. The cabin was sinusoidally rotated in anterior-posterior (a-p) direction with the horizontal rotation axis through the ankle joints (f=0.05-0.4 Hz; A (max)=0.25 degrees -4 degrees ; v (max)=0.08-10 degrees /s). The subjects' centre of mass (COM) angular position was calculated from opto-electronically measured body sway parameters. The platform was either kept stationary or moved by coupling its position 1:1 to a-p hip position ('body sway referenced', BSR, platform condition), by which proprioceptive feedback of ankle joint angle became inactivated. The visual stimulus evoked in-phase COM excursions (visual responses) in all subjects. (1) In normal subjects on a stationary platform, the visual responses showed saturation with both increasing velocity and displacement of the visual stimulus. The saturation showed up abruptly when visually evoked COM velocity and displacement reached approximately 0.1 degrees /s and 0.1 degrees , respectively. (2) In normal subjects on a BSR platform (proprioceptive feedback disabled), the visual responses showed similar saturation characteristics, but at clearly higher COM velocity and displacement values ( approximately 1 degrees /s and 1 degrees , respectively). (3) In patients on a stationary platform (no vestibular cues), the visual responses were basically similar to those of the normal subjects, apart from somewhat higher gain values and less-pronounced saturation effects. (4) In patients on a BSR platform (no vestibular and proprioceptive cues, presumably only somatosensory graviceptive and visual cues), the visual responses showed an abnormal increase in gain with increasing stimulus frequency in addition to a displacement saturation. On the normal subjects we performed additional experiments in which we varied the gain of the visual response by using a 'virtual reality' visual stimulus or by applying small lateral platform tilts. This did not affect the saturation characteristics of the visual response to a considerable degree. We compared the present results to previous psychophysical findings on motion perception, noting similarities of the saturation characteristics in (1) with leg proprioceptive detection thresholds of approximately 0.1 degrees /s and 0.1 degrees and those in (2) with vestibular detection thresholds of 1 degrees /s and 1 degrees , respectively. From the psychophysical data one might hypothesise that a proprioceptive postural mechanism limits the visually evoked body excursions if these excursions exceed 0.1 degrees /s and 0.1 degrees in condition (1) and that a vestibular mechanism is doing so at 1 degrees /s and 1 degrees in (2). To better understand this, we performed computer simulations using a posture control model with multiple sensory feedbacks. We had recently designed the model to describe postural responses to body pull and platform tilt stimuli. Here, we added a visual input and adjusted its gain to fit the simulated data to the experimental data. The saturation characteristics of the visual responses of the normals were well mimicked by the simulations. They were caused by central thresholds of proprioceptive, vestibular and somatosensory signals in the model, which, however, differed from the psychophysical thresholds. Yet, we demonstrate in a theoretical approach that for condition (1) the model can be made monomodal proprioceptive with the psychophysical 0.1 degrees /s and 0.1 degrees thresholds, and for (2) monomodal vestibular with the psychophysical 1 degrees /s and 1 degrees thresholds, and still shows the corresponding saturation characteristics (whereas our original model covers both conditions without adjustments). The model simulations also predicted the almost normal visual responses of patients on a stationary platform and their clearly abnormal responses on a BSR platform.

Meta level concept versus classic reflex concept for the control of posture and movement.

Postural reflexes are replaced soon after birth by automatic reactions that allow for volition and cognition. It is still an enigma how this change in postural control is achieved. We suggest that the change involves the formation of a sensory processing level (meta level) that becomes interleaved in between the tight sensor-actuator coupling of the classic reflexes. We assume that the brain applies at this level intersensory interactions to reconstruct the physical stimuli which are causing the physiological stimuli and sensory signals. The thus derived estimates of the physical stimuli are then used as feedback signals in the posture control system. We present this concept on the background of the classic reflex concept and earlier attempts in the literature to overcome it. The earlier attempts were often motivated by the question how the brain prevents voluntary movements from being hampered by reflexive stabilisation of posture (so-called posture-movement problem). We compare our new concept with the classic reflex concept in a theoretical approach, by implementing both concepts into simple postural control models. In simulations of the two models we superimpose external perturbations (the physical stimuli) and a voluntary body lean movement. We show that it is possible to achieve successful stimulus compensation and unperturbed lean movement with both, the model derived from the new concept and the one of the classic reflex concept. With both approaches, the posture-movement problem does not arise. Based on preliminary considerations that include experimental findings from the literature, however, we conclude that the new concept provides more explanatory power than the classic reflex concept.

Abnormal resonance behavior of the postural control loop in Parkinson's disease.

Human postural control of upright stance sporadically can show an oscillatory behavior. Based on previous work, we assessed whether an abnormal tendency for such oscillations might contribute to the motor impairments in patients with basal ganglia dysfunction such as Parkinson's disease (PD). We investigated postural control during unperturbed stance in normal control subjects and in PD patients off and under treatment, focusing on stabilogram diffusion analysis (SDA) of the foot center of pressure (COP) excursions and conventional measures of the sway amplitude and velocity. We found abnormal 1 Hz body sway oscillation in the SDA curves of PD patients that differed significantly from the body sway typically observed in control subjects during quiet stance. The 1 Hz body sway oscillation was associated with abnormally large and fast sway in the patients off treatment. Under treatment with levodopa, with 'deep brain stimulation' (subthalamic nucleus) and even more so with combined treatment, the oscillations in the SDA curves vanished and the sway became slower. The loss of oscillation and reduction of sway velocity were highly correlated with the improvements of patients' clinical motor assessment score. However, sway amplitude was not correlated with the patients' motor assessment score and patients reported clinical improvement under therapy even though sway amplitude increased on average. A simple feedback model of the postural control system with abnormally large internal noise could predict experimental measures both on and off treatment. The off treatment condition was consistent with a high motor gain in the feedback loop, and the on treatment condition with a reduced motor gain.

A modeling approach to the human spatial orientation system.

The human spatial orientation system is highly complex and nonlinear. It is difficult, therefore, to arrive at an unequivocal model of the underlying processing by merely combining the known elementary mechanisms ("bottom-up" approach); additional "top-down" concepts are required to narrow the choice between several formally equivalent solutions. We here suggest a concept in which sensorimotor control is based on a meta-level that provides an internal representation of the physical stimuli acting upon a subject (e.g., tilt of the support surface), whereas the classic reflex concept essentially proceeds from a direct coupling between physiological stimuli, sensors and actuators. At the hypothesized meta-level, the axial body segments are represented as a stack of superimposed platforms with the lowermost platform (generally the feet) riding on a support surface that acts as the buttress for the subject's active movements. From the sensory point of view, this stack constitutes a system of nested references. This concept explains data from various experiments dealing with self- and object motion perception and body stabilization in a more exhaustive way than does the classic concept. In our view, it provides a robust, flexible, and modular framework for perception and action in space.

Effect of chronic bilateral subthalamic nucleus (STN) stimulation on postural control in Parkinson's disease.

Postural instability is one of the most incapacitating factors in Parkinson's disease (PD). The underlying deficits and the effects of treatment are still not well understood. The aims of the present study were: (i) to identify abnormalities of postural control in PD patients during unperturbed stance and externally perturbed stance (anterior-posterior tilts of the support surface and of the visual scene); (ii) to assess the effects of L-dopa medication and subthalamic nucleus (STN) stimulation on posture control; and (iii) to characterize potential differential or additive effects of both treatments. Eight PD patients under chronic STN stimulation were investigated and compared with 10 normal controls. The assessment was performed in a crossover design (+/- STN stimulation, +/- L-dopa). During unperturbed stance, we recorded measures of spontaneous sway in terms of displacement, velocity and frequency of the centre of pressure (COP), lower body (LB) and upper body (UB) excursions. In addition, inter-segmental UB-LB coupling was investigated as a measure of axial stiffness. All these measures were abnormally large in patients OFF treatment. Under L-dopa treatment, the velocity, frequency and coupling measures were reduced, whereas sway amplitude increased. Very similar effects were obtained under STN stimulation, and these effects became more pronounced in the combined treatment condition. In these data, reduction of inter-segmental coupling correlated with increase in sway amplitude. The finding suggests that axial stiffness reduction under treatment revealed a treatment- resistant deficit in the sensorimotor postural control loop. However, these two effects did not correlate with the motor subscores of the unified Parkinson's disease rating scale (UPDRS), which indicates that they are of minor functional relevance for posture control. A frequency peak in the COP excursions at 0.7-1.1 Hz, which we take to indicate a resonance behaviour of the postural control loop, became reduced under therapy. The reduction of this peak did correlate with most improvements in the UPDRS under therapy. Support surface tilt revealed that an UB righting on the LB segment, which is present in normal controls, is missing in the patients. The postural responses to visual tilt were abnormally large in patients, independent of whether the support was stable or slightly moving, while the control subjects clearly profited from a stable support. This finding suggests that PD patients lack the ability of normal subjects to use sensory or cognitive information when suppressing the destabilizing effect of visual tilt. These abnormal tilt reactions of the patients were resistant to treatment with L-dopa, STN stimulation and a combination of the two. Overall, the effects of STN stimulation on posture control essentially paralleled those of L-dopa during both unperturbed and externally perturbed stance.

A multisensory posture control model of human upright stance.

We present a multisensory postural control model based on experiments where the balance in normal subjects and vestibular loss patients was perturbed by application of external torque produced by force-controlled pull stimuli. The stimuli were applied while subjects stood on a stationary or body-sway-referenced motion platform with eyes closed and auditory cues masked. Excursions of the center of mass (COM) and the center of pressure (COP) were analyzed using a systems analysis approach. The results were compared to an 'inverted pendulum' model of posture control. The model receives input from four sensors: ankle proprioceptors, semicircular canals, otoliths, and plantar pressure sensors (somatosensory graviceptors). Sensor fusion mechanisms are used to yield separate internal representations of foot support motion, gravity, and external torque (pull). These representations are fed as global set point signals into a local control loop based on ankle proprioceptive negative feedback. This set point control upgrades the proprioceptive body-on-foot (support) stabilization into a body-in-space control which compensates for support tilt, gravity, and contact forces. This compensation occurs even when the stimuli are combined or a voluntary lean is superimposed. Model simulations paralleled our experimental findings.

Combined action of smooth pursuit eye movements, optokinetic reflex and vestibulo-ocular reflex in macaque monkey during transient stimulation.

The interaction of smooth pursuit eye movements, vestibulo-ocular reflex (VOR) and optokinetic reflex (OKR) is still not well understood. We therefore measured in macaque monkeys horizontal eye movements using transient horizontal rotations of a visual target, of monkeys' heads and/or of an optokinetic background pattern (ten combinations; smoothed position ramps of 16 degrees ). With intermediate peak velocity of target motion (v(max)=12.8 degrees /s), pursuit held the eyes rather well on target, almost independent of concurrent vestibular or optokinetic stimuli (pursuit gain, 0.73-0.91). With v(max)=1.6 degrees /s, in contrast, pursuit gain became strongly modified by the optokinetic stimulus. With v(max)=51.2 degrees /s, pursuit gain became modified by vestibular stimulation. Although not intuitive, the experimental data can be explained by linear interaction (summation) of the neural driving signals for pursuit, VOR and OKR, as ascertained by simulations of a dynamic model.

Object motion perception is shaped by the motor control mechanism of ocular pursuit.

It is still a matter of debate whether the control of smooth pursuit eye movements involves an internal drive signal from object motion perception. We measured human target velocity and target position perceptions and compared them with the presumed pursuit control mechanism (model simulations). We presented normal subjects (Ns) and vestibular loss patients (Ps) with visual target motion in space. Concurrently, a visual background was presented, which was kept stationary or was moved with or against the target (five combinations). The motion stimuli consisted of smoothed ramp displacements with different dominant frequencies and peak velocities (0.05, 0.2, 0.8 Hz; 0.2-25.6 degrees /s). Subjects always pursued the target with their eyes. In a first experiment they gave verbal magnitude estimates of perceived target velocity in space and of self-motion in space. The target velocity estimates of both Ns and Ps tended to saturate at 0.8 Hz and with peak velocities >3 degrees /s. Below these ranges the velocity estimates showed a pronounced modulation in relation to the relative target-to-background motion ('background effect'; for example, 'background with'-motion decreased and 'against'-motion increased perceived target velocity). Pronounced only in Ps and not in Ns, there was an additional modulation in relation to the relative head-to-background motion, which co-varied with an illusion of self-motion in space (circular vection, CV) in Ps. In a second experiment, subjects performed retrospective reproduction of perceived target start and end positions with the same stimuli. Perceived end position was essentially veridical in both Ns and Ps (apart from a small constant offset). Reproduced start position showed an almost negligible background effect in Ns. In contrast, it showed a pronounced modulation in Ps, which again was related to CV. The results were compared with simulations of a model that we have recently presented for velocity control of eye pursuit. We found that the main features of target velocity perception (in terms of dynamics and modulation by background) closely correspond to those of the internal drive signal for target pursuit, compatible with the notion of a common source of both the perception and the drive signal. In contrast, the eye pursuit movement is almost free of the background effect. As an explanation, we postulate that the target-to-background component in the target pursuit drive signal largely neutralises the background-to-eye retinal slip signal (optokinetic reflex signal) that feeds into the eye premotor mechanism as a competitor of the target retinal slip signal. An extension of the model allowed us to simulate also the findings of the target position perception. It is assumed to be represented in a perceptual channel that is distinct from the velocity perception, building on an efference copy of the essentially accurate eye position. We hold that other visuomotor behaviour, such as target reaching with the hand, builds mainly on this target position percept and therefore is not contaminated by the background effect in the velocity percept. Generally, the coincidence of an erroneous velocity percept and an almost perfect eye pursuit movement during background motion is discussed as an instructive example of an action-perception dissociation. This dissociation cannot be taken to indicate that the two functions are internally represented in separate brain control systems, but rather reflects the intimate coupling between both functions.

Role of anterior and occipital white matter lesions for smooth eye tracking in myotonic dystrophy.

BACKGROUND: The degradation of smooth pursuit eye movements (SP) in myotonic dystrophy (MD) has been shown to result from lesions in the central nervous system. Imaging and histopathological studies have shown considerable areas of white matter lesions (WMLs) with periventricular emphasis. OBJECTIVE: To discover which of these WMLs are relevant in SP impairment? METHOD: Horizontal sinusoidal SP, the vestibulo-ocular reflex (VOR), and its suppression by fixation (VOR-S) were investigated in 12 patients with MD, and the data obtained were compared with those from a control group. RESULTS: Parallel degradation of SP and VOR-S was found in patients, although the eyes hardly needed to move with VOR-S. VOR in patients was normal. These results indicate a central rather than a peripheral origin for the SP degradation. Magnetic resonance images of the patients' heads were obtained and the WMLs transferred to a standard map. The lesions were mainly located around the occipital and anterior horn of the lateral ventricle. SP performance was then related to lesion site. The largest area of deficit associated lesions appeared to be in the parieto-occipital white matter. The most severe SP impairment, however, was associated with frontal WMLs. CONCLUSION: The study establishes a link between SP deficits and WMLs in patients with MD, in line with previous observations that, not only parieto-occipital regions, but also the frontal cortex has a crucial role in the gain control of SP.

Relationship between saccadic eye movements and cortical activity as measured by fMRI: quantitative and qualitative aspects.

We investigated the quantitative relationship between saccadic activity (as reflected in frequency of occurrence and amplitude of saccades) and blood oxygenation level dependent (BOLD) changes in the cerebral cortex using functional magnetic resonance imaging (fMRI). Furthermore, we investigated quantitative changes in cortical activity associated with qualitative changes in the saccade task for comparable levels of saccadic activity. All experiments required the simultaneous acquisition of eye movement and fMRI data. For this purpose we used a new high-resolution limbus-tracking technique for recording eye movements in the magnetic resonance tomograph. In the first two experimental series we varied both frequency and amplitude of saccade stimuli (target jumps). In the third series we varied task difficulty; subjects performed either pro-saccades or anti-saccades. The brain volume investigated comprised the frontal and supplementary eye fields, parietal as well as striate cortex, and the motion sensitive area of the parieto-occipital cortex. All these regions showed saccade-related BOLD responses. The responses in these regions were highly correlated with saccade frequency, indicating that repeated processing of saccades is integrated over time in the BOLD response. In contrast, there was no comparable BOLD change with variation of saccade amplitude. This finding speaks for a topological rather than activity-dependent coding of saccade amplitudes in most cortical regions. In the experiments comparing pro- vs anti-saccades we found higher BOLD activation in the "anti" task than in the "pro" task. A comparison of saccade parameters revealed that saccade frequency and cumulative amplitude were comparable between the two tasks, whereas reaction times were longer in the "anti" task than the pro task. The latter finding is taken to indicate a more demanding cortical processing in the "anti" task than the "pro" task, which could explain the observed difference in BOLD activation. We hold that a quantitative analysis of saccade parameters (especially saccade frequency and latency) is important for the interpretation of the BOLD changes observed with visual stimuli in fMRI.

Visual object localisation in space. Interaction of retinal, eye position, vestibular and neck proprioceptive information.

Perceptual updating of the location of visual targets in space after intervening eye, head or trunk movements requires an interaction between several afferent signals (visual, oculomotor efference copy, vestibular, proprioceptive). The nature of the interaction is still a matter of debate. To address this problem, we presented subjects (n=6) in the dark with a target (light spot) at various horizontal eccentricities (up to +/-20 degrees ) relative to the initially determined subjective straight-ahead direction (SSA). After a memory period of 12 s in complete darkness, the target reappeared at a random position and subjects were to reproduce its previous location in space using a remote control. For both the presentation and the reproduction of the target's location, subjects either kept their gaze in the SSA (retinal viewing condition) or fixated the eccentric target (visuo-oculomotor). Three experimental series were performed: A, "visual-only series": reproduction of the target's location in space was found to be close to ideal, independently of viewing condition; estimation curves (reproduced vs presented positions) showed intercepts approximately 0 degrees and slopes approximately 1; B, "visual-vestibular series": during the memory period, subjects were horizontally rotated to the right or left by 10 degrees or 18 degrees at 0.8-Hz or 0.1-Hz dominant frequency. Following the 0.8-Hz body rotation, reproduction was close to ideal, while at 0.1 Hz it was partially shifted along with the body, in line with the known vestibular high-pass characteristics. Additionally, eccentricity of target presentation reduced the slopes of the estimation curves (less than 1); C, "visual-vestibular-neck series": a shift toward the trunk also occurred after low-frequency neck stimulation (trunk rotated about stationary head). When vestibular and neck stimuli were combined (independent head and trunk rotations), their effects summed linearly, such that the errors cancelled each other during head rotation on the stationary trunk. Variability of responses was always lowest for targets presented at SSA, irrespective of intervening eye, head or trunk rotations. We conclude that: (1) subjects referenced "space" to pre-rotatory SSA and that the memory trace of the target's location in space was not altered during the memory period; and that (2) they used internal estimates of eye, head and trunk displacements with respect to space to match current target position with the memory trace during reproduction; these estimates would be obtained by inverting the physical coordinate transformations produced by these displacements. We present a model which is able to describe these operations and whose predictions closely parallel the experimental results. In this model the estimate of head rotation in space is not obtained directly from the vestibular head-in-space signal, but from a vestibular estimate of the kinematic state of the body support.

Human balance control during cutaneous stimulation of the plantar soles.

Previous work on human postural control of upright stance, performed in the absence of visual and vestibular orientation cues, suggests that somatosensory cues in the feet enable subjects to maintain equilibrium during low-frequency platform tilts. Here we confirm earlier studies which indicated that stimulation of plantar cutaneous mechanoreceptors can lead to postural responses. Yet, this stimulation did not modify considerably the postural reactions of normal subjects and vestibular loss patients during platform tilts. We therefore suggest that it is necessary to differentiate between (i) cues from plantar cutaneous receptors involved in exteroceptive functions, like the evaluation of the support structure or of relative foot-to-surface motion, and (ii) cues from deep receptors which subserve proprioceptive functions like the control of center of pressure shifts within the limits of the foot support base.

Adaptive changes of saccadic eye-head coordination resulting from altered head posture in torticollis spasmodicus.

We asked whether and how the abnormal head posture in torticollis patients affects saccadic gaze shifts and impairs the associated head movements. We wanted to learn to what extent observed changes directly result from the disease or reflect compensatory mechanisms, secondary to the altered head posture. We compared the results of patients with those of normal subjects. When patients viewed a centric target, their heads were a priori deviated in the direction of the torticollis, with orbital eye position showing a compensatory offset in the opposite direction. These abnormal eye and head positions were re-established when patients returned from an eccentric gaze position by means of a centripetal gaze shift, independently of its direction and magnitude, unlike in normal subjects who always recentred eyes and head. In normal subjects the share of the head in the total gaze shift amounted to about 70%, whereas in patients it contributed only 30%, necessitating correspondingly larger orbital eye displacements and eccentricities. Moreover, patients' head movements were asymmetric; they were larger when gaze was shifted into, or returned from the hemifield contralateral to the torticollis direction compared with gaze shifts in the ipsilateral hemifield. The eyes displayed a reversed asymmetry. Patients showed a significant increase in gaze latency and head versus eye delay as well as in the number of corrective saccades. However, head velocity was normal in four out of seven patients. Moreover, all patients made normal eye saccades (peak velocity, duration, gaze error), except for the increase in latency, which also occurred when gaze was shifted without head movements. Thus, patients' saccadic eye-head coordination showed abnormalities which mainly concerned the involved head movements. We suggest that the observed changes do not reflect a direct involvement of the disease upon the gaze shift mechanism, but can be interpreted as adaptive changes that compensate for the altered head posture. We formalized this view in the form of a dynamic model.

Visual search and visual working memory in patients with chronic focal cortical lesions.

Visually guided behavior is known to involve temporo-parietal, inferotemporal, and prefrontal cortex and each of these areas appears to contribute to visual working memory. We explored the extent to which chronic lesions in one of these cortical areas affect visually guided oculomotor performance. We also explore whether possible impairments become more pronounced with increasing memory load. With this aim we recorded saccadic eye movements in 19 patients with a chronic focal postsurgical lesion in either temporo-parietal, inferior temporal or prefrontal cortex. Their results are compared to those of 19 age-matched volunteers. The subjects performed three different visual search tasks with increasing memory load: Instructed search, cue-guided search and memory-guided search. In addition, the latter task was performed with a short (1 s) and a long (6 s) delay. All tasks required the subjects to make a saccade to a single target presented together with one or three distractors. The results indicate that patients with inferotemporal lesions make the most task-related errors. Saccadic reaction times (SRTs) were significantly prolonged in patients with temporo-parietal and prefrontal lesions, but were unaffected in the patients with lesions in the inferotemporal cortex. The spatial accuracy of saccades was lowest in patients with temporo-parietal lesions. An increase in memory load led to more errors, to longer reaction times and to lower saccadic precision. However, the effect was similar across the three patient groups and the controls. An error analysis indicated that both patients and controls tended to weight global (luminance contrast and form) features higher than local features (line-segment orientation) when making difficult perceptual decisions.