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

Abstract

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.

Behavioral, Neural, and Computational Principles of Bodily Self-Consciousness

“…By presenting tactile target stimuli at different delays from sound onset (simulating different sound distances from the body), reaction times to tactile targets became faster (compared to unimodal tactile stimulation) once the sound entered the participants' PPS. This facilitation effect was not linearly proportional to the spatial position of the sound, but occurred for sounds within a limited distance from the body (i.e., 40-50 cm for the hand), beyond which no space-dependent modulation of reaction times was found (Bassolino et al, 2015;Canzoneri et al, 2013aCanzoneri et al, , 2013bSerino et al, 2015;Teneggi et al, 2013). These data show that multisensory integration of bodily signals not only is governed by the metric distance of external stimuli from the body, but also depends on a third constraint of BSC that is absent for non-bodily multisensory perception: PPS.…”

Peripersonal Space: An Index of Multisensory Body–Environment Interactions in Real, Virtual, and Mixed Realities

“…On each trial, the tactile target stimulus is delivered at a different delay from the moment when the trial start; thus, in the multisensory trials, the tactile stimulus is processed when the visual (or audiovisual) stimulus is perceived as being at different distances from the participant (see Serino et al, 2015a, Figure 1, for evidence that approaching auditory stimuli within this context is localized by participants as closer the longer the stimuli has loomed for). In the case of Experiment 1, the visual stimulus approached the participant's face at a constant speed of 75 cm/s and was presented for 2,600 ms.…”

“…The PPS measurement task, originally developed to measure audiotactile interactions, has been adapted to a visuotactile version using 3D computer graphics and head-mounted displays (HMDs) in order to present dynamic visual stimuli (Herbelin et al, 2015;Serino et al, 2015a). Here, we describe the most recent evolution of the task based on MR where real environment and virtual objects are blended.…”

“…This approach has been extensively used in neuroscience research in order to investigate different properties of human PPS (Canzoneri et al, 2013a;Bassolino et al, 2014;Taffou and Viaud-Delmon, 2014;Ferri et al, 2015a,b;Galli et al, 2015;Noel et al, 2015b;Serino et al, 2015a;Kandula et al, 2017;Pellencin et al, 2017;Salomon et al, 2017). In this task, participants are requested to respond as fast as possible to a tactile stimulus administered on a given body part, while a taskirrelevant auditory or visual stimulus, which they are instructed to ignore, are presented approaching along the frontal plane at different distances from the participant's body.…”

“…Directly inspired by the monkey neurophysiology work, we have developed a psychophysical experimental task to measure behaviorally in humans the extent of PPS around the different parts of the body (Canzoneri et al, 2012;Teneggi et al, 2013;Serino et al, 2015a). This approach has been extensively used in neuroscience research in order to investigate different properties of human PPS (Canzoneri et al, 2013a;Bassolino et al, 2014;Taffou and Viaud-Delmon, 2014;Ferri et al, 2015a,b;Galli et al, 2015;Noel et al, 2015b;Serino et al, 2015a;Kandula et al, 2017;Pellencin et al, 2017;Salomon et al, 2017).…”