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Wutte, Magdalena (2012): Understanding space by moving through it: neural networks of motion- and space processing in humans. Dissertation, LMU München: Graduate School of Systemic Neurosciences (GSN)
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Abstract

Humans explore the world by moving in it, whether moving their whole body as during walking or driving a car, or moving their arm to explore the immediate environment. During movement, self-motion cues arise from the sensorimotor system comprising vestibular, proprioceptive, visual and motor cues, which provide information about direction and speed of the movement. Such cues allow the body to keep track of its location while it moves through space. Sensorimotor signals providing self-motion information can therefore serve as a source for spatial processing in the brain. This thesis is an inquiry into human brain systems of movement and motion processing in a number of different sensory and motor modalities using functional magnetic resonance imaging (fMRI). By characterizing connections between these systems and the spatial representation system in the brain, this thesis investigated how humans understand space by moving through it. In the first study of this thesis, the recollection networks of whole-body movement were explored. Brain activation was measured during the retrieval of active and passive self-motion and retrieval of observing another person performing these tasks. Primary sensorimotor areas dominated the recollection network of active movement, while higher association areas in parietal and mid-occipital cortex were recruited during the recollection of passive transport. Common to both self-motion conditions were bilateral activations in the posterior medial temporal lobe (MTL). No MTL activations were observed during recollection of movement observation. Considering that on a behavioral level, both active and passive self-motion provide sufficient information for spatial estimations, the common activation in MTL might represent the common physiological substrate for such estimations. The second study investigated processing in the 'parahippocampal place area' (PPA), a region in the posterior MTL, during haptic exploration of spatial layout. The PPA in known to respond strongly to visuo-spatial layout. The study explored if this region is processing visuo-spatial layout specifically or spatial layout in general, independent from the encoding sensory modality. In both a cohort of sighted and blind participants, activation patterns in PPA were measured while participants haptically explored the spatial layout of model scenes or the shape of information-matched objects. Both in sighted and blind individuals, PPA activity was greater during layout exploration than during object-shape exploration. While PPA activity in the sighted could also be caused by a transformation of haptic information into a mental visual image of the layout, two points speak against this: Firstly, no increase in connectivity between the visual cortex and the PPA were observed, which would be expected if visual imagery took place. Secondly, blind participates, who cannot resort to visual imagery, showed the same pattern of PPA activity. Together, these results suggest that the PPA processes spatial layout information independent from the encoding modality. The third and last study addressed error accumulation in motion processing on different levels of the visual system. Using novel analysis methods of fMRI data, possible links between physiological properties in hMT+ and V1 and inter-individual differences in perceptual performance were explored. A correlation between noise characteristics and performance score was found in hMT+ but not V1. Better performance correlated with greater signal variability in hMT+. Though neurophysiological variability is traditionally seen as detrimental for behavioral accuracy, the results of this thesis contribute to the increasing evidence which suggests the opposite: that more efficient processing under certain circumstances can be related to more noise in neurophysiological signals. In summary, the results of this doctoral thesis contribute to our current understanding of motion and movement processing in the brain and its interface with spatial processing networks. The posterior MTL appears to be a key region for both self-motion and spatial processing. The results further indicate that physiological characteristics on the level of category-specific processing but not primary encoding reflect behavioral judgments on motion. This thesis also makes methodological contributions to the field of neuroimaging: it was found that the analysis of signal variability is a good gauge for analysing inter-individual physiological differences, while superior head-movement correction techniques have to be developed before pattern classification can be used to this end.