Visual perceptual stability and the processing of self-motion information: neurophysiology, psychophysics and neuropsychology

While we move through our environment, we constantly have to deal with new sensory input. Especially the visual system has to deal with an ever-changing input signal, since we continuously move our eyes. For example, we change our direction of gaze about three times every second to a new area within...

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1. Verfasser: Dowiasch, Stefan
Beteiligte: Bremmer, Frank (Prof. Dr.) (BetreuerIn (Doktorarbeit))
Format: Dissertation
Veröffentlicht: Philipps-Universität Marburg 2015
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Zusammenfassung:While we move through our environment, we constantly have to deal with new sensory input. Especially the visual system has to deal with an ever-changing input signal, since we continuously move our eyes. For example, we change our direction of gaze about three times every second to a new area within our visual field with a fast, ballistic eye movement called a saccade. As a consequence, the entire projection of the surrounding world on our retina moves. Yet, we do not perceive this shift consciously. Instead, we have the impression of a stable world around us, in which objects have a well-defined location. In my thesis I aimed to investigate the underlying neural mechanisms of the visual perceptual stability of our environment. One hypothesis is that there is a coordinate transformation of the retinocentric input signal to a craniocentric (egocentric) and eventually even to a world centered (allocentric) frame of reference. Such a transformation into a craniocentric reference frame requires information about both the location of a stimulus on the retina and the current eye position within the head. The physicist Hermann von Helmholtz was one of the first who suggested that such an eye-position signal is available in the brain as an internal copy of the motor plan, which is sent to the eye muscles. This so-called efference copy allows the brain to classify actions as self-generated and differentiate them from being externally triggered. If we are the creator of an action, we are able to predict its outcome and can take this prediction into consideration for the further processing. For example, if the projection of the environment moves across the retina due to an eye movement, the shift is registered as self-induced and the brain maintains a stable percept of the world. However, if one gently pushes the eye from the side with a finger, we perceive a moving environment. Along the same lines, it is necessary to correctly attribute the movement of the visual field to our own self-motion, e.g. to perform eye movements accounting for the additional influences of our movements. The first study of my thesis shows that the perceived location of a stimulus might indeed be a combination of two independent neuronal signals, i.e. the position of the stimulus on the retina and information about the current eye-position or eye-movement, respectively. In this experiment, the mislocalization of briefly presented stimuli, which is characteristic for each type of eye-movement, leads to a perceptual localization of stimuli within the area of the blind spot on the retina. Yet, this is the region where the optic nerve leaves the eye, meaning that there are no photoreceptors available to convert light into neuronal signals. Physically, subjects should be blind for stimuli presented in this part of the visual field. In fact, a combination of the actual stimulus position with the specific, error-inducing eye-movement information is able to explain the experimentally measured behavior. The second study in my thesis investigates the underlying neural mechanism of the mislocalization of briefly presented stimuli during eye-movements. Many previous studies using animal models (the rhesus monkey) revealed internal representations of eye-position signals in various brain regions and therefore confirmed the hypothesis of an efference copy signal within the brain. Although these eye-position signals basically reflect the actual eye-position with good accuracy, there are also some spatial and temporal inaccuracies. These erroneous representations have been previously suggested as the source of perceptual mislocalization during saccades. The second study of my thesis extends this hypothesis to the mislocalization during smooth pursuit eye-movements. We usually perform such an eye movement when we want to continuously track a moving object with our eyes. I showed that the activity of neurons in the ventral intraparietal area of the rhesus monkey adequately represents the actual eye-position during smooth pursuit. However, there was a constant lead of the internal eye-position signal as compared to the real eye-position in direction of the ongoing eye-movement. In combination with a distortion of the visual map due to an uneven allocation of attention in direction of the future stimulus position, this results in a mislocalization pattern during smooth pursuit, which almost exactly resembles those typically measured in psychophysical experiments. Hence, on the one hand the efference copy of the eye-position signal provides the required signal to perform a coordinate transformation in order to preserve a stable perception of our environment. On the other hand small inaccuracies within this signal seem to cause perceptual errors when the visual system is experimentally pushed to its limits. The efference copy also plays a role in dysfunctions of the brain in neurological or psychiatric diseases. For example, many symptoms of schizophrenia patients could be explained by an impaired efference copy mechanism and a resulting misattribution of agency to self- and externally-produced actions. Following this hypothesis, the typically observed auditory hallucinations in these patients might be the result of an erroneously assigned agency of their own thoughts. To make a detailed analysis of this potentially impaired efference copy mechanism possible, the third study of my thesis investigated eye movements of schizophrenia patients and tried to step outside the limited capabilities of laboratory setups into the real world. This study showed that results of previous laboratory studies only partly resemble those obtained in the real world. For example, schizophrenia patients, when compared to healthy controls, usually show a more inaccurate smooth pursuit eye-movement in the laboratory. Yet, in the real world when they track a stationary object with their eyes while they are moving towards it, there are no differences between patients and healthy controls, although both types of eye-movements are closely related. This might be due to the fact that patients were able to use additional sources of information in the real world, e.g. self-motion information, to compensate for some of their deficits under certain conditions. Similarly, the fourth study of my thesis showed that typical impairments of eye-movements during healthy aging can be equalized by other sources of information available under natural conditions. At the same time, this work underlined the need of eye-movement measurements in the real world as a complement to laboratory studies to accurately describe the visual system, all mechanisms of perception and their interactions under natural circumstances. For example, experiments in the laboratory usually analyze particularly selected eye-movement parameters within a specific range, such as saccades of a certain amplitude. However, this does not reflect everyday life in which parameters like that are typically continuous and not normally distributed. Furthermore, motion-selective areas in the brain might play a much bigger role in natural environments, since we generally move our head and/or ourselves. To correctly analyze the contribution to and influences on eye-movements, one has to perform eye-movement studies under conditions as realistic as possible. The fifth study of my thesis aimed to investigate a possible application of eye-movement studies in the diagnosis of neuronal diseases. We showed that basic eye-movement parameters like saccade peak-velocity can be used to differentiate patients with Parkinson’s disease from patients with an atypical form of Parkinsonism, progressive supranuclear palsy. This differentiation is of particular importance since both diseases share a similar onset but have a considerably different progression and outcome, requiring different types of therapies. An early differential diagnosis, preferably in a subclinical stage, is needed to ensure the optimal treatment of the patients in order to ease the symptoms and eventually even improve the prognosis. The study showed that mobile eye-trackers are particularly well-suited to investigate eye movements in the daily clinical routine, due to their promising results in differential diagnosis and their easy, fast and reliable handling. In conclusion, my thesis underlines the importance of an interaction of all the different neuroscientific methods such as psychophysics, eye-movement measurements in the real world, electrophysiology and the investigation of neuropsychiatric patients to get a complete picture of how the brain works. The results of my thesis contribute to extent the current knowledge about the processing of information and the perception of our environment in the brain, point towards fields of application of eye-movement measurements and can be used as groundwork for future research.