Extending peripersonal space representation without tool-use: evidence from a combined behavioural-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. How...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2015-02-01
|
| Series: | Frontiers in Behavioral Neuroscience |
| Subjects: | |
| Online Access: | http://journal.frontiersin.org/Journal/10.3389/fnbeh.2015.00004/full |
| _version_ | 1818595109210423296 |
|---|---|
| author | Andrea eSerino Andrea eSerino Elisa eCanzoneri Elisa eCanzoneri Marilena eMarzolla Giuseppe eDi Pellegrino Giuseppe eDi Pellegrino Elisa eMagosso Elisa eMagosso |
| author_facet | Andrea eSerino Andrea eSerino Elisa eCanzoneri Elisa eCanzoneri Marilena eMarzolla Giuseppe eDi Pellegrino Giuseppe eDi Pellegrino Elisa eMagosso Elisa eMagosso |
| author_sort | Andrea eSerino |
| collection | DOAJ |
| 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-behavioural 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 behavioural 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 behavioural settings showed that asynchronous tactile and auditory inputs did not change PPS. We conclude by proposing a biological-plausible model to explain plasticity in PPS representation after tool-use, supported by computational and behavioural data. |
| first_indexed | 2024-12-16T11:10:47Z |
| format | Article |
| id | doaj.art-4854dee83936473c88c83198c2ecc96a |
| institution | Directory Open Access Journal |
| issn | 1662-5153 |
| language | English |
| last_indexed | 2024-12-16T11:10:47Z |
| publishDate | 2015-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Behavioral Neuroscience |
| spelling | doaj.art-4854dee83936473c88c83198c2ecc96a2022-12-21T22:33:44ZengFrontiers Media S.A.Frontiers in Behavioral Neuroscience1662-51532015-02-01910.3389/fnbeh.2015.00004122759Extending peripersonal space representation without tool-use: evidence from a combined behavioural-computational approachAndrea eSerino0Andrea eSerino1Elisa eCanzoneri2Elisa eCanzoneri3Marilena eMarzolla4Giuseppe eDi Pellegrino5Giuseppe eDi Pellegrino6Elisa eMagosso7Elisa eMagosso8Center for Neuroprosthetics, Ecole Polytechnique Fédérale de LausanneUniversity of BolognaCenter for Neuroprosthetics, Ecole Polytechnique Fédérale de LausanneUniversity of BolognaUniversity of BolognaUniversity of BolognaUniversity of BolognaALMA MATER STUDIORUM, University of BolognaALMA MATER STUDIORUM, University of BolognaStimuli 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-behavioural 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 behavioural 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 behavioural settings showed that asynchronous tactile and auditory inputs did not change PPS. We conclude by proposing a biological-plausible model to explain plasticity in PPS representation after tool-use, supported by computational and behavioural data.http://journal.frontiersin.org/Journal/10.3389/fnbeh.2015.00004/fullplasticityneural network modelmultisensory processingtool-useperipersonal space |
| spellingShingle | Andrea eSerino Andrea eSerino Elisa eCanzoneri Elisa eCanzoneri Marilena eMarzolla Giuseppe eDi Pellegrino Giuseppe eDi Pellegrino Elisa eMagosso Elisa eMagosso Extending peripersonal space representation without tool-use: evidence from a combined behavioural-computational approach Frontiers in Behavioral Neuroscience plasticity neural network model multisensory processing tool-use peripersonal space |
| title | Extending peripersonal space representation without tool-use: evidence from a combined behavioural-computational approach |
| title_full | Extending peripersonal space representation without tool-use: evidence from a combined behavioural-computational approach |
| title_fullStr | Extending peripersonal space representation without tool-use: evidence from a combined behavioural-computational approach |
| title_full_unstemmed | Extending peripersonal space representation without tool-use: evidence from a combined behavioural-computational approach |
| title_short | Extending peripersonal space representation without tool-use: evidence from a combined behavioural-computational approach |
| title_sort | extending peripersonal space representation without tool use evidence from a combined behavioural computational approach |
| topic | plasticity neural network model multisensory processing tool-use peripersonal space |
| url | http://journal.frontiersin.org/Journal/10.3389/fnbeh.2015.00004/full |
| work_keys_str_mv | AT andreaeserino extendingperipersonalspacerepresentationwithouttooluseevidencefromacombinedbehaviouralcomputationalapproach AT andreaeserino extendingperipersonalspacerepresentationwithouttooluseevidencefromacombinedbehaviouralcomputationalapproach AT elisaecanzoneri extendingperipersonalspacerepresentationwithouttooluseevidencefromacombinedbehaviouralcomputationalapproach AT elisaecanzoneri extendingperipersonalspacerepresentationwithouttooluseevidencefromacombinedbehaviouralcomputationalapproach AT marilenaemarzolla extendingperipersonalspacerepresentationwithouttooluseevidencefromacombinedbehaviouralcomputationalapproach AT giuseppeedipellegrino extendingperipersonalspacerepresentationwithouttooluseevidencefromacombinedbehaviouralcomputationalapproach AT giuseppeedipellegrino extendingperipersonalspacerepresentationwithouttooluseevidencefromacombinedbehaviouralcomputationalapproach AT elisaemagosso extendingperipersonalspacerepresentationwithouttooluseevidencefromacombinedbehaviouralcomputationalapproach AT elisaemagosso extendingperipersonalspacerepresentationwithouttooluseevidencefromacombinedbehaviouralcomputationalapproach |