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.
Highlights
Stimuli from different sensory modalities occurring on or close to the body are integrated in order to provide a multisensory representation of the space where the body physically interacts with objects in the environment, that is the peripersonal space (PPS)
We found that sounds speeded up the tactile reaction time (RT) only when they were administered within a limited distance from the hand, i.e., within the boundaries of PPS representation
This ensues from modification of the auditory feedforward synapses that causes an enlargement of the auditory receptive field (RF) of the multisensory neuron to include the far space
Summary
Stimuli from different sensory modalities (somatosensation, vision, audition) occurring on or close to the body are integrated in order to provide a multisensory representation of the space where the body physically interacts with objects in the environment, that is the peripersonal space (PPS). Analogous forms of multisensory responses for the space around the body have been repeatedly shown in humans and in brain areas homologous to those where PPS neurons have been shown in monkeys (Bremmer et al, 2001; Makin et al, 2007; Gentile et al, 2011; Serino et al, 2011; Brozzoli et al, 2012). We found that sounds speeded up the tactile reaction time (RT) only when they were administered within a limited distance from the hand, i.e., within the boundaries of PPS representation (see Serino et al, 2007, 2011). We were able to calculate the critical distance where sounds affected tactile RT along a continuum between near and far space, estimating the boundaries of PPS
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