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      Shaping visual space perception through bodily sensations: Testing the impact of nociceptive stimuli on visual perception in peripersonal space with temporal order judgments

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          Abstract

          Coordinating spatial perception between body space and its external surrounding space is essential to adapt behaviors to objects, especially when they are noxious. Such coherent multisensory representation of the body extended into external space is conceptualized by the notion of peripersonal reference frame, mapping the portion of space in which somatic and extra-somatic inputs interact closely. Studies on crossmodal interactions between nociception and vision have been scarce. Here we investigated how the perception of visual stimuli, especially those surrounding the body, can be impacted by a nociceptive and potentially harmful stimulus inflicted on a particular body part. In two temporal order judgment tasks, participants judged which of two lateralized visual stimuli, presented either near or far from the body, had been presented first. Visual stimuli were preceded by nociceptive stimuli, either applied unilaterally (on one single hand) or bilaterally (on both hands simultaneously). In Experiment 1 participants’ hands were always placed next to the visual stimuli presented near the trunk, while in Experiment 2 they could also be placed next to the visual stimuli presented far from the trunk. In Experiment 1, the presence of unilateral nociceptive stimuli prioritized the perception of visual stimuli presented in the same side of space as the stimulated hand, with a significantly larger effect when visual stimuli were presented near the body than when presented farther away. Experiment 2 showed that these visuospatial biases were related to the spatial congruency between the hand on which nociceptive stimuli were applied and the visual stimuli, independently of the relative distance of both the stimulated hand and the visual stimuli from the trunk. Indeed, nociceptive stimuli mostly impacted the perception of the closest visual stimuli. It is hypothesized that these crossmodal interactions may rely on representations of the space directly surrounding specific body parts.

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          Confidence intervals in within-subject designs: A simpler solution to Loftus and Masson's method

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            Parieto-frontal interactions, personal space, and defensive behavior.

            In the monkey brain, two interconnected cortical areas have distinctive neuronal responses to visual, tactile, and auditory stimuli. These areas are the ventral intraparietal area (VIP) and a polysensory zone in the precentral gyrus (PZ). The multimodal neurons in these areas typically respond to objects touching, near, or looming toward the body surface. Electrical stimulation of these areas evokes defensive-like withdrawing or blocking movements. These areas have been suggested to participate in a range of functions including navigation by optic flow, attention to nearby space, and the processing of object location for the guidance of movement. We suggest that a major emphasis of these areas is the construction of a margin of safety around the body and the selection and coordination of defensive behavior. In this review, we summarize the physiological properties of these brain areas and discuss a range of behavioral phenomena that might be served by those neuronal properties, including the ducking and blocking reactions that follow startle, the flight zone of animals, the personal space of humans, the nearby, multimodal attentional space that has been studied in humans, the withdrawal reaction to looming visual stimuli, and the avoidance of obstacles during self-motion such as locomotion or reaching.
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              Is that near my hand? Multisensory representation of peripersonal space in human intraparietal sulcus.

              Our ability to interact with the immediate surroundings depends not only on an adequate representation of external space but also on our ability to represent the location of objects with respect to our own body and especially to our hands. Indeed, electrophysiological studies in monkeys revealed multimodal neurons with spatially corresponding tactile and visual receptive fields in a number of brain areas, suggesting a representation of visual peripersonal space with respect to the body. In this functional magnetic resonance imaging study, we localized areas in human intraparietal sulcus (IPS) and lateral occipital complex (LOC) that represent nearby visual space with respect to the hands (perihand space), by contrasting the response to a ball moving near-to versus far-from the hands. Furthermore, by independently manipulating sensory information about the hand, in the visual (using a dummy hand) and proprioceptive domains (by changing the unseen hand position), we determined the sensory contributions to the representation of hand-centered space. In the posterior IPS, the visual contribution was dominant, overriding proprioceptive information. Surprisingly, regions within LOC also displayed visually dominant, hand-related activation. In contrast, the anterior IPS was characterized by a proprioceptive representation of the hand, as well as showing tactile hand-specific activation, suggesting a homology with monkey parietal hand-centered areas. We therefore suggest that, whereas cortical regions within the posterior IPS and LOC represent hand-centered space in a predominantly visual manner, the anterior IPS uses multisensory information in representing perihand space.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: MethodologyRole: ResourcesRole: SoftwareRole: Visualization
                Role: Formal analysisRole: InvestigationRole: Resources
                Role: Formal analysisRole: InvestigationRole: Resources
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: 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
                4 August 2017
                2017
                : 12
                : 8
                : e0182634
                Affiliations
                [1 ] Institute of Neuroscience, Université catholique de Louvain, Brussels, Belgium
                [2 ] Faculty of Psychology and Educational Sciences, Université catholique de Louvain, Louvain-la-Neuve, Belgium
                Centre de neuroscience cognitive, FRANCE
                Author notes

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

                [¤]

                Current address: Coma Science Group, GIGA Research Center, Université de Liège, Liège, Belgium

                Article
                PONE-D-17-05387
                10.1371/journal.pone.0182634
                5544212
                28777824
                2aa69eb7-c36d-4332-a583-6e3836c12bf9
                © 2017 Filbrich et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 9 February 2017
                : 22 July 2017
                Page count
                Figures: 5, Tables: 0, Pages: 20
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100002661, Fonds De La Recherche Scientifique - FNRS;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100002661, Fonds De La Recherche Scientifique - FNRS;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100002661, Fonds De La Recherche Scientifique - FNRS;
                Award Recipient :
                LF, AA, and VL are supported by the Fund for Scientific Research of the French-speaking Community of Belgium (F.R.S.-FNRS; http://www1.frs-fnrs.be/). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Neuroscience
                Sensory Perception
                Vision
                Biology and Life Sciences
                Psychology
                Sensory Perception
                Vision
                Social Sciences
                Psychology
                Sensory Perception
                Vision
                Biology and Life Sciences
                Neuroscience
                Sensory Perception
                Biology and Life Sciences
                Psychology
                Sensory Perception
                Social Sciences
                Psychology
                Sensory Perception
                Biology and Life Sciences
                Physiology
                Sensory Physiology
                Somatosensory System
                Pain Sensation
                Medicine and Health Sciences
                Physiology
                Sensory Physiology
                Somatosensory System
                Pain Sensation
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                Neuroscience
                Sensory Systems
                Somatosensory System
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                Cell Biology
                Cellular Types
                Animal Cells
                Neurons
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                Anatomy
                Musculoskeletal System
                Limbs (Anatomy)
                Arms
                Hands
                Medicine and Health Sciences
                Anatomy
                Musculoskeletal System
                Limbs (Anatomy)
                Arms
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                Biology and Life Sciences
                Neuroscience
                Sensory Perception
                Nociception
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                Psychology
                Sensory Perception
                Nociception
                Social Sciences
                Psychology
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                Nociception
                Biology and Life Sciences
                Neuroscience
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                Medicine and Health Sciences
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                Sensory Physiology
                Somatosensory System
                Biology and Life Sciences
                Neuroscience
                Sensory Systems
                Somatosensory System
                Custom metadata
                All data used for the manuscript are available from the OSF data repository at the address: https://osf.io/s583x/ (doi: 10.17605/OSF.IO/S583X).

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