Dataset Information

Fast and accurate edge orientation processing during object manipulation.

ABSTRACT: Quickly and accurately extracting information about a touched object's orientation is a critical aspect of dexterous object manipulation. However, the speed and acuity of tactile edge orientation processing with respect to the fingertips as reported in previous perceptual studies appear inadequate in these respects. Here we directly establish the tactile system's capacity to process edge-orientation information during dexterous manipulation. Participants extracted tactile information about edge orientation very quickly, using it within 200 ms of first touching the object. Participants were also strikingly accurate. With edges spanning the entire fingertip, edge-orientation resolution was better than 3° in our object manipulation task, which is several times better than reported in previous perceptual studies. Performance remained impressive even with edges as short as 2 mm, consistent with our ability to precisely manipulate very small objects. Taken together, our results radically redefine the spatial processing capacity of the tactile system.

SUBMITTER: Pruszynski JA

PROVIDER: S-EPMC5922971 | biostudies-literature | 2018 Apr

REPOSITORIES: biostudies-literature

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Fast and accurate edge orientation processing during object manipulation.

Pruszynski J Andrew JA Flanagan J Randall JR Johansson Roland S RS

eLife 20180403

Quickly and accurately extracting information about a touched object's orientation is a critical aspect of dexterous object manipulation. However, the speed and acuity of tactile edge orientation processing with respect to the fingertips as reported in previous perceptual studies appear inadequate in these respects. Here we directly establish the tactile system's capacity to process edge-orientation information during dexterous manipulation. Participants extracted tactile information about edge ...[more]

PMID: 29611804

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Project description:During manipulation, object slipping is prevented by modulating the grip force (GF) in synchrony with motion-related inertial forces, i.e., load force (LF). However, due to conduction delays of the sensory system, GF must be modulated in advance based on predictions of LF changes. It has been proposed that such predictive force control relies on internal representations, i.e., internal models, of the relation between the dynamic of the environment and movement kinematics. Somatosensory and visual feedback plays a primary role in building these internal representations. For instance, it has been shown that manipulation-dependent somatosensory signals contribute to building internal representations of gravity in normal and altered gravitational contexts. Furthermore, delaying the timing of visual feedback of object displacement has been shown to affect GF. Here, we explored whether and the extent to which spatial features of visual feedback movement, such as motion direction, may contribute to GF control. If this were the case, a spatial mismatch between actual (somatosensory) and visual feedback of object motion would elicit changes in GF modulation. We tested this hypothesis by asking participants to generate vertical object movements while visual feedback of object position was congruent (0° rotation) or incongruent (180° or 90°) with the actual object displacement. The role of vision on GF control was quantified by the temporal shift of GF modulation as a function of visual feedback orientation and actual object motion direction. GF control was affected by visual feedback when this was incongruent in the vertical (180°), but not horizontal dimension. Importantly, 180° visual feedback rotation delayed and anticipated GF modulation during upward and downward actual movements, respectively. Our findings suggest that during manipulation, spatial features of visual feedback motion are used to predict upcoming LF changes. Furthermore, the present study provides evidence that an internal model of gravity contributes to GF control by influencing sensory reweighting processes during object manipulation.

Project description:The activity of frontal motor areas during hand-object interaction is coordinated by dense communication along specific white matter pathways. This architecture allows the continuous shaping of voluntary motor output but, despite extensive investigation in non-human primate studies, remains poorly understood in humans. Disclosure of this system is crucial for predicting and treatment of motor deficits after brain lesions. For this purpose, we investigated the effect of direct electrical stimulation on white matter pathways within the frontal lobe on hand-object manipulation. This was tested in 34 patients (15 left hemisphere, mean age 42 years, 17 male, 15 with tractography) undergoing awake neurosurgery for frontal lobe tumour removal with the aid of the brain mapping technique. The stimulation outcome was quantified based on hand-muscle activity required by task execution. The white matter pathways responsive to stimulation with an interference on muscles were identified by means of probabilistic density estimation of stimulated sites, tract-based lesion-symptom (disconnectome) analysis and diffusion tractography on the single patient level. Finally, we assessed the effect of permanent tract disconnection on motor outcome in the immediate postoperative period using a multivariate lesion-symptom mapping approach. The analysis showed that stimulation disrupted hand-muscle activity during task execution at 66 sites within the white matter below dorsal and ventral premotor regions. Two different EMG interference patterns associated with different structural architectures emerged: (i) an 'arrest' pattern, characterized by complete impairment of muscle activity associated with an abrupt task interruption, occurred when stimulating a white matter area below the dorsal premotor region. Local middle U-shaped fibres, superior fronto-striatal, corticospinal and dorsal fronto-parietal fibres intersected with this region. (ii) a 'clumsy' pattern, characterized by partial disruption of muscle activity associated with movement slowdown and/or uncoordinated finger movements, occurred when stimulating a white matter area below the ventral premotor region. Ventral fronto-parietal and inferior fronto-striatal tracts intersected with this region. Finally, only resections partially including the dorsal white matter region surrounding the supplementary motor area were associated with transient upper-limb deficit (P = 0.05; 5000 permutations). Overall, the results identify two distinct frontal white matter regions possibly mediating different aspects of hand-object interaction via distinct sets of structural connectivity. We suggest the dorsal region, associated with arrest pattern and postoperative immediate motor deficits, to be functionally proximal to motor output implementation, while the ventral region may be involved in sensorimotor integration required for task execution.

Dataset Information

Fast and accurate edge orientation processing during object manipulation.

Publications

Fast and accurate edge orientation processing during object manipulation.

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