Abstract

Peripersonal space (PPS), the interface between the self and the environment, is represented by a network of multisensory neurons with visual (or auditory) receptive fields anchored to specific body parts, and tactile receptive fields covering the same body parts. Neurophysiological and behavioural features of hand PPS representation have been previously modelled through a neural network constituted by one multisensory population integrating tactile inputs with visual/auditory external stimuli. Reference frame transformations were not explicitly modelled, as stimuli were encoded in pre‐computed hand‐centred coordinates. Here we present a novel model, aiming to overcome this limitation by including a proprioceptive population encoding hand position. We confirmed behaviourally the plausibility of the proposed architecture, showing that visuo‐proprioceptive information is integrated to enhance tactile processing on the hand. Moreover, the network's connectivity was spontaneously tuned through a Hebbian‐like mechanism, under two minimal assumptions. First, the plasticity rule was designed to learn the statistical regularities of visual, proprioceptive and tactile inputs. Second, such statistical regularities were simply those imposed by the body structure. The network learned to integrate proprioceptive and visual stimuli, and to compute their hand‐centred coordinates to predict tactile stimulation. Through the same mechanism, the network reproduced behavioural correlates of manipulations implicated in subjective body ownership: the invisible and the rubber hand illusion. We thus propose that PPS representation and body ownership may emerge through a unified neurocomputational process; the integration of multisensory information consistently with a model of the body in the environment, learned from the natural statistics of sensory inputs.

Highlights

  • We proposed that spatially aligned visual and proprioceptive multisensory receptive fields collectively account for the reference frame transformations that allow the maintenance of the overlap between visual and tactile receptive fields, which is at the core of peripersonal space (PPS) representation

  • 4.2 | Visuo-tactile facilitation in handcentred reference frames emerges from statistical regularities in the environment Following classical behavioural and neurophysiological assessments, we focused on visuotactile interactions, and how they are modulated by proprioception, to test PPS representation as emerging from the network

  • We found the network's tactile predictions to be based on the hand-centred coordinates of the visual stimulus, with a maximal strength when visual stimuli are close to the hand and an activation profile depending on the distance from the hand, closely resembling what reported from single cell responses by neurophysiological studies in monkeys

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Summary

| INTRODUCTION

Peripersonal space (PPS) is typically defined as the region of space immediately surrounding the body, or the space where we can physically interact with external objects, either actively, by reaching to touch them, or passively, when we enter in contact with an incoming object (di Pellegrino & Làdavas, 2015; Serino, 2019). PPS was originally defined in terms of a physical space, with a specific neural representation, following long-known selective impairments of action and perception for stimuli in the near space induced by natural lesions in brain-damaged patients (Brain, 1941) and by experimental lesions in monkeys (Rizzolatti et al, 1983) This concept was expanded by neurophysiological and behavioural studies focusing on multisensory processing of stimuli within a limited distance from the body. By adjusting the weight of feedback and feedforward synapses, the model could either compute the position in a given reference frame based on the activity in the other two populations, or optimally integrate the three of them to increase the reliability of the information in each modality It has not been investigated whether a similar model could account for the emergence of body-part centred visuo-tactile interactions as the key property of PPS representation. A key question in the field is to render how multisensory integration within overlapping visual and tactile receptive fields occurs, and how such overlap is formed and maintained throughout development and everyday life

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| MATERIALS AND METHODS
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Findings
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