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      Haptically Guided Grasping. fMRI Shows Right-Hemisphere Parietal Stimulus Encoding, and Bilateral Dorso-Ventral Parietal Gradients of Object- and Action-Related Processing during Grasp Execution

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          Abstract

          The neural bases of haptically-guided grasp planning and execution are largely unknown, especially for stimuli having no visual representations. Therefore, we used functional magnetic resonance imaging (fMRI) to monitor brain activity during haptic exploration of novel 3D complex objects, subsequent grasp planning, and the execution of the pre-planned grasps. Haptic object exploration, involving extraction of shape, orientation, and length of the to-be-grasped targets, was associated with the fronto-parietal, temporo-occipital, and insular cortex activity. Yet, only the anterior divisions of the posterior parietal cortex (PPC) of the right hemisphere were significantly more engaged in exploration of complex objects (vs. simple control disks). None of these regions were re-recruited during the planning phase. Even more surprisingly, the left-hemisphere intraparietal, temporal, and occipital areas that were significantly invoked for grasp planning did not show sensitivity to object features. Finally, grasp execution, involving the re-recruitment of the critical right-hemisphere PPC clusters, was also significantly associated with two kinds of bilateral parieto-frontal processes. The first represents transformations of grasp-relevant target features and is linked to the dorso-dorsal (lateral and medial) parieto-frontal networks. The second monitors grasp kinematics and belongs to the ventro-dorsal networks. Indeed, signal modulations associated with these distinct functions follow dorso-ventral gradients, with left aIPS showing significant sensitivity to both target features and the characteristics of the required grasp. Thus, our results from the haptic domain are consistent with the notion that the parietal processing for action guidance reflects primarily transformations from object-related to effector-related coding, and these mechanisms are rather independent of sensory input modality.

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          Separate visual pathways for perception and action.

          Accumulating neuropsychological, electrophysiological and behavioural evidence suggests that the neural substrates of visual perception may be quite distinct from those underlying the visual control of actions. In other words, the set of object descriptions that permit identification and recognition may be computed independently of the set of descriptions that allow an observer to shape the hand appropriately to pick up an object. We propose that the ventral stream of projections from the striate cortex to the inferotemporal cortex plays the major role in the perceptual identification of objects, while the dorsal stream projecting from the striate cortex to the posterior parietal region mediates the required sensorimotor transformations for visually guided actions directed at such objects.
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            Working memory in primate sensory systems.

            Sensory working memory consists of the short-term storage of sensory stimuli to guide behaviour. There is increasing evidence that elemental sensory dimensions - such as object motion in the visual system or the frequency of a sound in the auditory system - are stored by segregated feature-selective systems that include not only the prefrontal and parietal cortex, but also areas of sensory cortex that carry out relatively early stages of processing. These circuits seem to have a dual function: precise sensory encoding and short-term storage of this information. New results provide insights into how activity in these circuits represents the remembered sensory stimuli.
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              A common reference frame for movement plans in the posterior parietal cortex.

              Orchestrating a movement towards a sensory target requires many computational processes, including a transformation between reference frames. This transformation is important because the reference frames in which sensory stimuli are encoded often differ from those of motor effectors. The posterior parietal cortex has an important role in these transformations. Recent work indicates that a significant proportion of parietal neurons in two cortical areas transforms the sensory signals that are used to guide movements into a common reference frame. This common reference frame is an eye-centred representation that is modulated by eye-, head-, body- or limb-position signals. A common reference frame might facilitate communication between different areas that are involved in coordinating the movements of different effectors. It might also be an efficient way to represent the locations of different sensory targets in the world.
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                Author and article information

                Contributors
                Journal
                Front Hum Neurosci
                Front Hum Neurosci
                Front. Hum. Neurosci.
                Frontiers in Human Neuroscience
                Frontiers Media S.A.
                1662-5161
                05 January 2016
                2015
                : 9
                : 691
                Affiliations
                Action and Cognition Laboratory, Department of Social Sciences, Institute of Psychology, Adam Mickiewicz University in Poznań Poznań, Poland
                Author notes

                Edited by: Simona Monaco, University of Trento, Italy

                Reviewed by: Anthony Singhal, University of Alberta, Canada; Robert Leslie Whitwell, The University of Western Ontario, Canada

                *Correspondence: Gregory Króliczak krolgreg@ 123456amu.edu.pl ; krol.greg@ 123456gmail.com
                Article
                10.3389/fnhum.2015.00691
                4700263
                26779002
                6f3dcca9-9594-483e-a1e9-84913d40ad86
                Copyright © 2016 Marangon, Kubiak and Króliczak.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 30 September 2015
                : 07 December 2015
                Page count
                Figures: 5, Tables: 1, Equations: 0, References: 89, Pages: 19, Words: 15997
                Funding
                Funded by: Narodowe Centrum Nauki 10.13039/501100004281
                Award ID: 2011/02/A/HS6/00174
                Funded by: Ministerstwo Nauki i Szkolnictwa Wyższego 10.13039/501100004569
                Award ID: 6168/IA/128/2012
                Funded by: Telemedicine and Advanced Technology Research Center 10.13039/100006965
                Categories
                Neuroscience
                Original Research

                Neurosciences
                haptic exploration,encoding bias,action planning,grasp execution,complex objects,dorsal stream

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