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Oculomotor function and self-motion perception in the elderly

Deliverables

In animal experiments, the role of head position on visual perception was investigated in macaque monkeys. Visual receptive fields were mapped in parietal cortex neurons (VIP, MIP, LIP) using different combinations of head and eye positions for spatially defined visual targets. Our present data suggest the multiple reference frames for the coding of personal and extra-personal space in our population of intra-parietal neurons. These findings are important to assess influences of head position on the perception and spatial placement of straight-ahead or eccentric targets, as well as to contributing mechanisms for spatial disorientation during head movements, as one cause of vehicle accidents.
Psychophysical tests on heading perception in humans were done with a virtual reality set-up. Optic flow stimuli of different strengths simulated forward self-motion into different directions. The results suggest that older subjects are not capable to achieve better performance from higher information content, i.e., older subjects cannot process and/or make use of increased incoming information flow in the way younger subjects do. Adding noise to the visual stimulus did not deteriorate the subjects' performance significantly. In a final set of experiments visual stimuli containing horizontal disparity were presented. Interestingly, this additional information was used only for longer presentation times indicating that stereoscopic information needs an integration time before becoming available for behaviour. Our findings might have implications for the future design e.g. of head-up displays in vehicles to support driving. These displays should present a reduced amount of information at high saliency.
The possibility to train older people and patients with certain movement disorders to avoid effectively unexpected obstacles and stumbling was explored under controlled laboratory conditions. The ability to anticipate potential stumbling situations to visually perceived obstacles was determined, as well as the adaptability to learn appropriate anticipatory responses. The immediate goal was to design and evaluate clinical interventions to train elderly individuals at high risk for falling. To this end, a new Fall Prevention Training program for the elderly was defined, refined and implemented in a long-term study. Effects of a low-intensity exercise program on falls, standing balance, balance confidence, and obstacle avoidance performance were investigated. The program resulted in a clinically meaningful, i.e., 46% reduction in the number of falls. These results can already be obtained after only a 5-week training period. Based on this result, the Nijmegen Fall Prevention Program will make a useful an important addition to previously reported effective interventions. The findings will potentially benefit all the elderly in the European Union and elsewhere.
Movement perception plays a crucial and vital role during vehicle driving. Instead of using projected optic flow patterns, or a classical virtual reality display; we made use of a driving simulator. During this study, a base line problem had to be overcome: the occurrence of stimulator sickness. To that end, we recorded neurovegetative parameters via non-invasive micro-captors to record vital parameters (heart rate, respiratory rate, skin conductance, skin temperature, capillary blood flow, etc.) in order to have an objective measure of possible "motion sickness" (simulator sickness), besides the subjective indications of the experimental subjects. In particular, we investigated autonomic nervous system (ANS) activity associated with developing simulator sickness ("Simulator Sickness Predictor Program"). There were marked changes in the ANS activity in the sick subjects. On average, skin resistance and skin temperature decreased with increasing sickness, while skin potential and heart rate increased. These patterns are typical of increased sympathetic activation, and probably correspond to the stress response that is a known component of kinetosis. These parameters can also serve as indicators for anxiety in elderly drivers. Sickness correlated strongly with anxiety increase during the driving session. Contrary to our expectations and all existing literature, three of six vestibular-loss patients tested in this way developed kinetosis, two of them quite severely. Motion sickness thus does not require the presence of a functional vestibular sense.
Studies on eye movement plasticity showed that effects of aging are rather subtle and require more elaborate analysis tools than previously anticipated. The same is true for certain neurological patients, e.g., cerebellar lesion patients. We investigated also whether the lack of significant changes in eye movement plasticity is an indicator of a corresponding lack of changes of learning in other motor systems. This question was addressed with a paradigm to explore learning processes that ameliorate gait, or more specifically, plasticity that improves the ability to cope with disturbances, imitating gait. We established a treadmill paradigm using rapid decelerations in order to assess the individual ability for compensation which might correlate with the risk of falls.
A computational-mathematical model of self-motion perception, movement detection and movement related sensory-motor transformations, and the consequences of aging were finalized. In this two- layer network, the input layer resembles the function of area MT in primates whereas the output layer has functional properties similar to those recently described for areas MST and VIP. The hypothesis then was that aging could be mimicked by a loss of neural elements in the network. We simulated different loss rates and found a steadily increasing error with an increasing loss of neurons. The modelling data, based on neuropsychological and neuroanatomical data on neuronal loss due to age, fit nicely the behavioural results from psychophysical studies.
Eye movement parameters and self-motion perception were assessed in young, middle-aged and elderly subjects during simulated forward translation. Accuracy of saccades in elderly subjects was about 90% and comparable to that known for children and adults. By contrast, accuracy of convergence and divergence (pure or combined) decreased in elderly subjects (60% or below). Furthermore the speed of all vergence movements (pure or combined) was also markedly decreased. These results indicate that vergence eye movements become particularly fragile with age. Slowness both in initiation and execution, and poor accuracy of vergence could be partially responsible for problems with space perception, in particular regarding correct evaluation and interpretation of the distance to an obstacle, thus leading to falls. As shown with transcranial magnetic stimulation (TMS), there is a left/right asymmetry for the encoding of saccade and vergence eye movement metrics involving the posterior parietal cortex and the frontal eye fields. However, the combined message of these studies is that aging has a definite effect on a number of motor and perceptual functions, but these effects are rather subtle and circumscript, and require targeted and specific measures for remedy. The results will allow to target specific deficiencies in the elderly regarding visual attention.
In animal experiments, the cortical and sub-cortical afferent connectivity of areas involved in the generation of eye movements, orienting and perceptive functions was studied in macaque monkeys. To this end, the polysynaptic connectivities between the parietal cortical motion sensitive areas of the "dorsal stream" (MT, MST, VIP), the vestibular cortices, and the cortical oculomotor areas (frontal eye fields, FEF; supplementary eye fields, SEF) was determined with conventional tracers and a transneuronal tracer. Among the vast data yield of novel findings revealed by these experiments, a particularly striking result is the unexpected demonstration that VIP/MIP receive prominent vestibular input directly from the vestibular end organs, by ascending vestibular pathways. These findings are in keeping with the existence of strong vestibular responses in MIP/VIP. Many neurons in MIP/VIP respond to horizontal rotation, and are strongly influenced by active movements, like second-order vestibular neurons. Until now, it was believed that vestibular input reached MIP/VIP only indirectly, via cortico-cortical (polysynaptic) projections from traditional vestibular cortical areas. On the contrary, our results show unequivocally that vestibular input is also relayed to VIP/MIP directly via an ascending oligosynaptic vestibular pathway, i.e., from the vestibular (Scarpa's) ganglia to the vestibular nuclei, from vestibular nuclei to thalamic relays, and from them to MIP/VIP. These findings have important functional implications, since they signify that the intraparietal sulcus areas MIP/VIP should be truly regarded as vestibular cortical areas, and may play a much more important role in processing of self-motion detection than envisaged to date. These data are also important in light of the known alleviation of the syndrome of spatial hemineglect (following a lesion of the right-side parieto-temporal junction in humans) by vestibular stimuli.