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      Task demands affect spatial reference frame weighting during tactile localization in sighted and congenitally blind adults

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          Abstract

          Task demands modulate tactile localization in sighted humans, presumably through weight adjustments in the spatial integration of anatomical, skin-based, and external, posture-based information. In contrast, previous studies have suggested that congenitally blind humans, by default, refrain from automatic spatial integration and localize touch using only skin-based information. Here, sighted and congenitally blind participants localized tactile targets on the palm or back of one hand, while ignoring simultaneous tactile distractors at congruent or incongruent locations on the other hand. We probed the interplay of anatomical and external location codes for spatial congruency effects by varying hand posture: the palms either both faced down, or one faced down and one up. In the latter posture, externally congruent target and distractor locations were anatomically incongruent and vice versa. Target locations had to be reported either anatomically (“palm” or “back” of the hand), or externally (“up” or “down” in space). Under anatomical instructions, performance was more accurate for anatomically congruent than incongruent target-distractor pairs. In contrast, under external instructions, performance was more accurate for externally congruent than incongruent pairs. These modulations were evident in sighted and blind individuals. Notably, distractor effects were overall far smaller in blind than in sighted participants, despite comparable target-distractor identification performance. Thus, the absence of developmental vision seems to be associated with an increased ability to focus tactile attention towards a non-spatially defined target. Nevertheless, that blind individuals exhibited effects of hand posture and task instructions in their congruency effects suggests that, like the sighted, they automatically integrate anatomical and external information during tactile localization. Moreover, spatial integration in tactile processing is, thus, flexibly adapted by top-down information—here, task instruction—even in the absence of developmental vision.

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          The ventriloquist effect results from near-optimal bimodal integration.

          Ventriloquism is the ancient art of making one's voice appear to come from elsewhere, an art exploited by the Greek and Roman oracles, and possibly earlier. We regularly experience the effect when watching television and movies, where the voices seem to emanate from the actors' lips rather than from the actual sound source. Originally, ventriloquism was explained by performers projecting sound to their puppets by special techniques, but more recently it is assumed that ventriloquism results from vision "capturing" sound. In this study we investigate spatial localization of audio-visual stimuli. When visual localization is good, vision does indeed dominate and capture sound. However, for severely blurred visual stimuli (that are poorly localized), the reverse holds: sound captures vision. For less blurred stimuli, neither sense dominates and perception follows the mean position. Precision of bimodal localization is usually better than either the visual or the auditory unimodal presentation. All the results are well explained not by one sense capturing the other, but by a simple model of optimal combination of visual and auditory information.
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            Improved auditory spatial tuning in blind humans.

            Despite reports of improved auditory discrimination capabilities in blind humans and visually deprived animals, there is no general agreement as to the nature or pervasiveness of such compensatory sensory enhancements. Neuroimaging studies have pointed out differences in cerebral organization between blind and sighted humans, but the relationship between these altered cortical activation patterns and auditory sensory acuity remains unclear. Here we compare behavioural and electrophysiological indices of spatial tuning within central and peripheral auditory space in congenitally blind and normally sighted but blindfolded adults to test the hypothesis (raised by earlier studies of the effects of auditory deprivation on visual processing) that the effects of visual deprivation might be more pronounced for processing peripheral sounds. We find that blind participants displayed localization abilities that were superior to those of sighted controls, but only when attending to sounds in peripheral auditory space. Electrophysiological recordings obtained at the same time revealed sharper tuning of early spatial attention mechanisms in the blind subjects. Differences in the scalp distribution of brain electrical activity between the two groups suggest a compensatory reorganization of brain areas in the blind that may contribute to the improved spatial resolution for peripheral sound sources.
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              Flexible strategies for sensory integration during motor planning.

              When planning target-directed reaching movements, human subjects combine visual and proprioceptive feedback to form two estimates of the arm's position: one to plan the reach direction, and another to convert that direction into a motor command. These position estimates are based on the same sensory signals but rely on different combinations of visual and proprioceptive input, suggesting that the brain weights sensory inputs differently depending on the computation being performed. Here we show that the relative weighting of vision and proprioception depends both on the sensory modality of the target and on the information content of the visual feedback, and that these factors affect the two stages of planning independently. The observed diversity of weightings demonstrates the flexibility of sensory integration and suggests a unifying principle by which the brain chooses sensory inputs so as to minimize errors arising from the transformation of sensory signals between coordinate frames.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: SoftwareRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: ResourcesRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                11 December 2017
                2017
                : 12
                : 12
                : e0189067
                Affiliations
                [1 ] Biological Psychology and Neuropsychology, Faculty of Psychology and Human Movement Science, University of Hamburg, Hamburg, Germany
                [2 ] Department of Psychology, New York University, New York, United States of America
                [3 ] Biopsychology & Cognitive Neuroscience, Faculty of Psychology & Sports Science, Bielefeld University, Bielefeld, Germany
                [4 ] Center of Excellence in Cognitive Interaction Technology (CITEC), Bielefeld University, Bielefeld, Germany
                Pennsylvania State University, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0001-5632-6091
                Article
                PONE-D-17-18939
                10.1371/journal.pone.0189067
                5724835
                29228023
                05ad5f5f-ce06-498c-908d-0f4b98165573

                This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                History
                : 17 May 2017
                : 17 November 2017
                Page count
                Figures: 3, Tables: 4, Pages: 19
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: He 6368/1-1
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: SFB 936 (project B1)
                Funded by: funder-id http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: BA 5600/1-1
                Award Recipient :
                This work was supported through the German Research Foundation’s (DFG) Research Collaborative SFB 936 (project B1), and Emmy Noether grant Hed 6368/1-1, by which TH was funded. SB was supported by a DFG research fellowship Ba 5600/1-1. We acknowledge support for the Article Processing Charge by the Deutsche Forschungsgemeinschaft and the Open Access Publication Fund of Bielefeld University.
                Categories
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                Ophthalmology
                Visual Impairments
                Blindness
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