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      Real-time vision, tactile cues, and visual form agnosia: removing haptic feedback from a “natural” grasping task induces pantomime-like grasps

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          Abstract

          Investigators study the kinematics of grasping movements (prehension) under a variety of conditions to probe visuomotor function in normal and brain-damaged individuals. “Natural” prehensile acts are directed at the goal object and are executed using real-time vision. Typically, they also entail the use of tactile, proprioceptive, and kinesthetic sources of haptic feedback about the object (“haptics-based object information”) once contact with the object has been made. Natural and simulated (pantomimed) forms of prehension are thought to recruit different cortical structures: patient DF, who has visual form agnosia following bilateral damage to her temporal-occipital cortex, loses her ability to scale her grasp aperture to the size of targets (“grip scaling”) when her prehensile movements are based on a memory of a target previewed 2 s before the cue to respond or when her grasps are directed towards a visible virtual target but she is denied haptics-based information about the target. In the first of two experiments, we show that when DF performs real-time pantomimed grasps towards a 7.5 cm displaced imagined copy of a visible object such that her fingers make contact with the surface of the table, her grip scaling is in fact quite normal. This finding suggests that real-time vision and terminal tactile feedback are sufficient to preserve DF’s grip scaling slopes. In the second experiment, we examined an “unnatural” grasping task variant in which a tangible target (along with any proxy such as the surface of the table) is denied (i.e., no terminal tactile feedback). To do this, we used a mirror-apparatus to present virtual targets with and without a spatially coincident copy for the participants to grasp. We compared the grasp kinematics from trials with and without terminal tactile feedback to a real-time-pantomimed grasping task (one without tactile feedback) in which participants visualized a copy of the visible target as instructed in our laboratory in the past. Compared to natural grasps, removing tactile feedback increased RT, slowed the velocity of the reach, reduced in-flight grip aperture, increased the slopes relating grip aperture to target width, and reduced the final grip aperture (FGA). All of these effects were also observed in the real time-pantomime grasping task. These effects seem to be independent of those that arise from using the mirror in general as we also compared grasps directed towards virtual targets to those directed at real ones viewed directly through a pane of glass. These comparisons showed that the grasps directed at virtual targets increased grip aperture, slowed the velocity of the reach, and reduced the slopes relating grip aperture to the widths of the target. Thus, using the mirror has real consequences on grasp kinematics, reflecting the importance of task-relevant sources of online visual information for the programming and updating of natural prehensile movements. Taken together, these results provide compelling support for the view that removing terminal tactile feedback, even when the grasps are target-directed, induces a switch from real-time visual control towards one that depends more on visual perception and cognitive supervision. Providing terminal tactile feedback and real-time visual information can evidently keep the dorsal visuomotor system operating normally for prehensile acts.

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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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            A new neural framework for visuospatial processing.

            The division of cortical visual processing into distinct dorsal and ventral streams is a key framework that has guided visual neuroscience. The characterization of the ventral stream as a 'What' pathway is relatively uncontroversial, but the nature of dorsal stream processing is less clear. Originally proposed as mediating spatial perception ('Where'), more recent accounts suggest it primarily serves non-conscious visually guided action ('How'). Here, we identify three pathways emerging from the dorsal stream that consist of projections to the prefrontal and premotor cortices, and a major projection to the medial temporal lobe that courses both directly and indirectly through the posterior cingulate and retrosplenial cortices. These three pathways support both conscious and non-conscious visuospatial processing, including spatial working memory, visually guided action and navigation, respectively.
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              The ventral visual pathway: an expanded neural framework for the processing of object quality.

              Since the original characterization of the ventral visual pathway, our knowledge of its neuroanatomy, functional properties, and extrinsic targets has grown considerably. Here we synthesize this recent evidence and propose that the ventral pathway is best understood as a recurrent occipitotemporal network containing neural representations of object quality both utilized and constrained by at least six distinct cortical and subcortical systems. Each system serves its own specialized behavioral, cognitive, or affective function, collectively providing the raison d'être for the ventral visual pathway. This expanded framework contrasts with the depiction of the ventral visual pathway as a largely serial staged hierarchy culminating in singular object representations and more parsimoniously incorporates attentional, contextual, and feedback effects. Published by Elsevier Ltd.
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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
                06 May 2015
                2015
                : 9
                : 216
                Affiliations
                [1] 1Graduate Program in Neuroscience, The University of Western Ontario London, ON, Canada
                [2] 2Department of Psychology, The University of Western Ontario London, ON, Canada
                [3] 3The Brain and Mind Institute, The University of Western Ontario London, ON, Canada
                [4] 4Department of Psychology, Ben-Gurion University of the Negev Beer-Sheva, Israel
                [5] 5Department of Physiology and Pharmacology, The University of Western Ontario London, ON, Canada
                Author notes

                Edited by: Simona Monaco, University of Trento, Italy

                Reviewed by: Claudio Galletti, University of Bologna, Italy; David A. Westwood, Dalhousie University, Canada

                *Correspondence: Robert L. Whitwell, Graduate Program in Neuroscience, Department of Psychology, The Brain and Mind Institute, The University of Western Ontario, Room 245, London, ON N6A 5B7, Canada rwhitwel@ 123456gmail.com
                Article
                10.3389/fnhum.2015.00216
                4422037
                25999834
                4bc6decb-ffee-45fa-8b34-9412fd7f7d78
                Copyright © 2015 Whitwell, Ganel, Byrne and Goodale.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution and 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
                : 15 October 2014
                : 02 April 2015
                Page count
                Figures: 7, Tables: 0, Equations: 5, References: 78, Pages: 18, Words: 17283
                Categories
                Neuroscience
                Original Research

                Neurosciences
                grasping,pantomime grasps,haptic feedback,visual feedback,visual form agnosia
                Neurosciences
                grasping, pantomime grasps, haptic feedback, visual feedback, visual form agnosia

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