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Extending peripersonal space representation without tool-use: evidence from a combined behavioral-computational approach

Stimuli from different sensory modalities occurring on or close to the body are integrated in a multisensory representation of the space surrounding the body, i.e., peripersonal space (PPS). PPS dynamically modifies depending on experience, e.g., it extends after using a tool to reach far objects. H...

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Autores principales: Serino, Andrea, Canzoneri, Elisa, Marzolla, Marilena, di Pellegrino, Giuseppe, Magosso, Elisa
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4313698/
https://www.ncbi.nlm.nih.gov/pubmed/25698947
http://dx.doi.org/10.3389/fnbeh.2015.00004
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author Serino, Andrea
Canzoneri, Elisa
Marzolla, Marilena
di Pellegrino, Giuseppe
Magosso, Elisa
author_facet Serino, Andrea
Canzoneri, Elisa
Marzolla, Marilena
di Pellegrino, Giuseppe
Magosso, Elisa
author_sort Serino, Andrea
collection PubMed
description Stimuli from different sensory modalities occurring on or close to the body are integrated in a multisensory representation of the space surrounding the body, i.e., peripersonal space (PPS). PPS dynamically modifies depending on experience, e.g., it extends after using a tool to reach far objects. However, the neural mechanism underlying PPS plasticity after tool use is largely unknown. Here we use a combined computational-behavioral approach to propose and test a possible mechanism accounting for PPS extension. We first present a neural network model simulating audio-tactile representation in the PPS around one hand. Simulation experiments showed that our model reproduced the main property of PPS neurons, i.e., selective multisensory response for stimuli occurring close to the hand. We used the neural network model to simulate the effects of a tool-use training. In terms of sensory inputs, tool use was conceptualized as a concurrent tactile stimulation from the hand, due to holding the tool, and an auditory stimulation from the far space, due to tool-mediated action. Results showed that after exposure to those inputs, PPS neurons responded also to multisensory stimuli far from the hand. The model thus suggests that synchronous pairing of tactile hand stimulation and auditory stimulation from the far space is sufficient to extend PPS, such as after tool-use. Such prediction was confirmed by a behavioral experiment, where we used an audio-tactile interaction paradigm to measure the boundaries of PPS representation. We found that PPS extended after synchronous tactile-hand stimulation and auditory-far stimulation in a group of healthy volunteers. Control experiments both in simulation and behavioral settings showed that the same amount of tactile and auditory inputs administered out of synchrony did not change PPS representation. We conclude by proposing a simple, biological-plausible model to explain plasticity in PPS representation after tool-use, which is supported by computational and behavioral data.
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spelling pubmed-43136982015-02-19 Extending peripersonal space representation without tool-use: evidence from a combined behavioral-computational approach Serino, Andrea Canzoneri, Elisa Marzolla, Marilena di Pellegrino, Giuseppe Magosso, Elisa Front Behav Neurosci Neuroscience Stimuli from different sensory modalities occurring on or close to the body are integrated in a multisensory representation of the space surrounding the body, i.e., peripersonal space (PPS). PPS dynamically modifies depending on experience, e.g., it extends after using a tool to reach far objects. However, the neural mechanism underlying PPS plasticity after tool use is largely unknown. Here we use a combined computational-behavioral approach to propose and test a possible mechanism accounting for PPS extension. We first present a neural network model simulating audio-tactile representation in the PPS around one hand. Simulation experiments showed that our model reproduced the main property of PPS neurons, i.e., selective multisensory response for stimuli occurring close to the hand. We used the neural network model to simulate the effects of a tool-use training. In terms of sensory inputs, tool use was conceptualized as a concurrent tactile stimulation from the hand, due to holding the tool, and an auditory stimulation from the far space, due to tool-mediated action. Results showed that after exposure to those inputs, PPS neurons responded also to multisensory stimuli far from the hand. The model thus suggests that synchronous pairing of tactile hand stimulation and auditory stimulation from the far space is sufficient to extend PPS, such as after tool-use. Such prediction was confirmed by a behavioral experiment, where we used an audio-tactile interaction paradigm to measure the boundaries of PPS representation. We found that PPS extended after synchronous tactile-hand stimulation and auditory-far stimulation in a group of healthy volunteers. Control experiments both in simulation and behavioral settings showed that the same amount of tactile and auditory inputs administered out of synchrony did not change PPS representation. We conclude by proposing a simple, biological-plausible model to explain plasticity in PPS representation after tool-use, which is supported by computational and behavioral data. Frontiers Media S.A. 2015-02-02 /pmc/articles/PMC4313698/ /pubmed/25698947 http://dx.doi.org/10.3389/fnbeh.2015.00004 Text en Copyright © 2015 Serino, Canzoneri, Marzolla, di Pellegrino and Magosso. http://creativecommons.org/licenses/by/4.0/ 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.
spellingShingle Neuroscience
Serino, Andrea
Canzoneri, Elisa
Marzolla, Marilena
di Pellegrino, Giuseppe
Magosso, Elisa
Extending peripersonal space representation without tool-use: evidence from a combined behavioral-computational approach
title Extending peripersonal space representation without tool-use: evidence from a combined behavioral-computational approach
title_full Extending peripersonal space representation without tool-use: evidence from a combined behavioral-computational approach
title_fullStr Extending peripersonal space representation without tool-use: evidence from a combined behavioral-computational approach
title_full_unstemmed Extending peripersonal space representation without tool-use: evidence from a combined behavioral-computational approach
title_short Extending peripersonal space representation without tool-use: evidence from a combined behavioral-computational approach
title_sort extending peripersonal space representation without tool-use: evidence from a combined behavioral-computational approach
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4313698/
https://www.ncbi.nlm.nih.gov/pubmed/25698947
http://dx.doi.org/10.3389/fnbeh.2015.00004
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