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Patterns of multisensory facilitation distinguish peripersonal from reaching space

View ORCID ProfileA. Zanini, I. Patané, E. Blini, R. Salemme, E. Koun, A. Farnè, C. Brozzoli
doi: https://doi.org/10.1101/2020.06.01.127282
A. Zanini
1ImpAct Team, Lyon Neuroscience Research Centre, INSERM U1028, CNRS UMR5292, Lyon, France
2University Claude Bernard Lyon I, Université de Lyon, Lyon, France
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  • ORCID record for A. Zanini
  • For correspondence: alessandro.zanini@inserm.fr claudio.brozzoli@inserm.fr
I. Patané
1ImpAct Team, Lyon Neuroscience Research Centre, INSERM U1028, CNRS UMR5292, Lyon, France
2University Claude Bernard Lyon I, Université de Lyon, Lyon, France
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E. Blini
1ImpAct Team, Lyon Neuroscience Research Centre, INSERM U1028, CNRS UMR5292, Lyon, France
2University Claude Bernard Lyon I, Université de Lyon, Lyon, France
3Department of General Psychology, University of Padova, Padova, Italy
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R. Salemme
1ImpAct Team, Lyon Neuroscience Research Centre, INSERM U1028, CNRS UMR5292, Lyon, France
2University Claude Bernard Lyon I, Université de Lyon, Lyon, France
4Hospices Civils de Lyon, Neuro-immersion – Mouvement et Handicap, Lyon, France
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E. Koun
1ImpAct Team, Lyon Neuroscience Research Centre, INSERM U1028, CNRS UMR5292, Lyon, France
2University Claude Bernard Lyon I, Université de Lyon, Lyon, France
4Hospices Civils de Lyon, Neuro-immersion – Mouvement et Handicap, Lyon, France
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A. Farnè
1ImpAct Team, Lyon Neuroscience Research Centre, INSERM U1028, CNRS UMR5292, Lyon, France
2University Claude Bernard Lyon I, Université de Lyon, Lyon, France
4Hospices Civils de Lyon, Neuro-immersion – Mouvement et Handicap, Lyon, France
5Center for Mind/Brain Sciences, University of Trento, Rovereto, Italy
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C. Brozzoli
1ImpAct Team, Lyon Neuroscience Research Centre, INSERM U1028, CNRS UMR5292, Lyon, France
2University Claude Bernard Lyon I, Université de Lyon, Lyon, France
4Hospices Civils de Lyon, Neuro-immersion – Mouvement et Handicap, Lyon, France
6Department of Neurobiology, Care Sciences and Society, Aging Research Center, Karolinska Institutet, Stockholm, Sweden
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  • For correspondence: alessandro.zanini@inserm.fr claudio.brozzoli@inserm.fr
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Abstract

Peripersonal space is a multisensory representation of the space near body parts facilitating interactions with the close environment. Studies on non-human and human primates converge in showing that peripersonal space (PPS) is a body-part-centred representation that guides actions. Because of these characteristics, growing confusion conflates peripersonal and arm-reaching space (ARS) that is the space one’s arm can reach. Despite neuroanatomical evidence favors their distinction, whether PPS and ARS tap into different spatial representations remains poorly understood. Here, in five experiments we found that PPS differs from ARS in male and female human participants (N = 120), as evidenced both by their performance and the modeling of their multisensory facilitation. We mapped multisensory facilitation in detecting touches at the hand, placed in different locations radially within ARS. Results showed that 1) PPS is smaller than ARS; 2) multivariate modeling of spatial patterns of multisensory facilitation predicts well the position of the participants’ hand within ARS; 3) multisensory facilitation maps shift according to changes of hand position, revealing hand-centred coding of PPS, but not ARS; and 4) cross-correlation analyses highlight isomorphic multisensory facilitation maps across hand positions, suggesting their functional similarity to the receptive fields of monkeys’ multisensory neurons. In sharp contrast, ARS mapping produced undistinguishable patterns across hand positions, cross-validating the conclusion that PPS and ARS are distinct. These findings call for a refinement of theoretical models of PPS and ARS, which are relevant in constructs as diverse as action and self representation, (social) interpersonal distance, brain-machine interfaces and neuroprosthetics.

Significance Statement The peripersonal space (PPS) is a multisensory interface allowing us to interact with objects in the space close to our body-parts, playing a fundamental role for the defense of the body and for the motor control of actions. Recent research has conflated PPS with the arm-reaching space (ARS), that is whole space reachable by the arm. However, there is actually no evidence supporting this equivalence and the anatomical and functional differences between PPS and ARS have been largely overlooked. In this paper, we frame the theoretical issue in depth, validate a novel methodological paradigm across five experiments, and eventually report robust and cross-validated evidence for the distinction between PPS and ARS, supported by both multivariate and univariate analyses.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Conflict of Interest: The authors declare no competing financial interests.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted June 02, 2020.
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Patterns of multisensory facilitation distinguish peripersonal from reaching space
A. Zanini, I. Patané, E. Blini, R. Salemme, E. Koun, A. Farnè, C. Brozzoli
bioRxiv 2020.06.01.127282; doi: https://doi.org/10.1101/2020.06.01.127282
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Patterns of multisensory facilitation distinguish peripersonal from reaching space
A. Zanini, I. Patané, E. Blini, R. Salemme, E. Koun, A. Farnè, C. Brozzoli
bioRxiv 2020.06.01.127282; doi: https://doi.org/10.1101/2020.06.01.127282

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