Elsevier

Neuropsychologia

Volume 70, April 2015, Pages 375-384
Neuropsychologia

Full body action remapping of peripersonal space: The case of walking

https://doi.org/10.1016/j.neuropsychologia.2014.08.030Get rights and content

Highlights

  • We measure the extension of peripersonal space (PPS) during locomotion.

  • Results show that during locomotion PPS extends from about ~65cm to about ~165cm.

  • Enlargement of PPS during walking is driven by motor commands and proprioception.

  • Our findings support the view that PPS is a sensory-motor interface for individual-environment interaction.

Abstract

The space immediately surrounding the body, i.e. peripersonal space (PPS), is represented by populations of multisensory neurons, from a network of premotor and parietal areas, which integrate tactile stimuli from the body’s surface with visual or auditory stimuli presented within a limited distance from the body. Here we show that PPS boundaries extend while walking. We used an audio–tactile interaction task to identify the location in space where looming sounds affect reaction time to tactile stimuli on the chest, taken as a proxy of the PPS boundary. The task was administered while participants either stood still or walked on a treadmill. In addition, in two separate experiments, subjects either received or not additional visual inputs, i.e. optic flow, implying a translation congruent with the direction of their walking. Results revealed that when participants were standing still, sounds boosted tactile processing when located within 65–100 cm from the participants’ body, but not at farther distances. Instead, when participants were walking PPS expands as reflected in boosted tactile processing at ~1.66 m. This was found despite the fact the spatial relationship between the participant’s body and the sound’s source did not vary between the Standing and the Walking condition. This expansion effect on PPS boundaries due to walking was the same with or without optic flow, suggesting that kinematics and proprioceptive cues, rather than visual cues, are critical in triggering the effect. These results are the first to demonstrate an adaptation of the chest’s PPS representation due to whole body motion and are compatible with the view that PPS constitutes a dynamic sensory–motor interface between the individual and the environment.

Introduction

Most human interactions, be it sensorimotor or be it social, are carried out by our body and are performed in our peripersonal space (PPS), that is, the space immediately surrounding our body (Rizzolatti et al., 1981, Di Pellegrino et al., 1997, Rizzolatti et al., 1997). Landmark electrophysiological studies in monkeys claimed the existence of multimodal neurons in the posterior parietal cortex, in particular in the ventral intraparietal sulcus (VIP, Hyvärinen and Poranen, 1974, Schlack et al., 2005), in the premotor cortex (PMc, Fogassi et al., 1996, Duhamel et al., 1998, Bremmer et al., 2002) and in the putamen (Graziano & Gross, 1994), devoted to the representation of PPS. These neurons respond to tactile stimuli administered to specific body parts, most commonly the arm, the head, and the chest (Duhamel et al., 1998), and also to visual or auditory stimuli presented within a limited space surrounding these body parts. The fact that the response properties of these neurons are independent from eye position, whereas they depend on the position of the different body parts in space, suggests that they do not encode an eye-centered, but a body-part centered, multisensory representation of PPS (Avillac et al., 2005, Graziano et al., 2000, Graziano and Cooke, 2006).

Notably, electrical stimulation of premotor and parietal brain areas containing PPS neurons elicits complex motor responses of the arm and head (Graziano, Taylor, & Moore, 2002), suggesting that PPS representation, which is constructed based on multisensory integration mechanisms, also supports motor functions. In particular, PPS can be conceived as a multisensory-motor system interfacing the body and the environment. Two main non-mutually exclusive hypotheses have been advanced as to the functional relevance of PPS. On the one hand it is proposed that PPS, serving as a rapid, putatively coarse-grain, sensorimotor interface (Makin, Holmes, Brozzoli, & Farnè, 2012) could act as a personal safety boundary allowing for timely responses to approaching threats (Graziano & Cooke, 2006). This view is primarily supported by the observation that electrical stimulation to VIP and PMc areas in monkeys provokes defensive-like motor outputs, such as squinting, blocking, and ducking (Cooke and Graziano, 2004, Cooke et al., 2003). Furthermore, evidence indicates that looming stimuli elicit a greater response in the aforementioned neural areas than receding stimuli do (Graziano, Hu, & Gross, 1997). In turn, defensive reactions to looming stimuli have been documented across a wide range of animals (Schiff, Caviness, & Gibson, 1962).

On the other hand, it has been proposed that PPS might represent a sensorimotor interface subserving goal-oriented actions and the rapid online update and correction between motor outputs and their concomitant sensory consequences (Rizzolatti et al., 1981, Rizzolatti et al., 1997, Brozzoli et al., 2014). This latter view is most prominently supported by the fact that visual responses of bimodal neurons increase during the execution of reaching movements (Godschalk, Lemon, Kuypers, & van der Steen, 1985). In addition, VIP neurons appear to be a fundamental nexus in spatial coordinate system transformation (Avillac et al., 2005) aiding in converting sensory input from its native reference frames (eye-centered, head-centered, and chest-centered) to a spatiotopic and egocentric coordinate system allowing for motor output. Lastly it has been proposed that PPS might not only be germane to action execution, but also to action observation, as some mirror neurons seem to show selectivity between actions performed inside and outside PPS (Caggiano et al., 2009, Bonini et al., 2014).

Although extensive, the literature reviewed above refers exclusively to single-cell data on monkeys. Yet it is indeed conceivable that PPS may play a different functional role as we move across animal models and from single cell recordings, to systems neuroscience, to behavior. Extensive literature from neuropsychology (Di Pellegrino et al., 1997, Farnè et al., 2005), experimental psychology (Spence et al., 2000, Holmes et al., 2007, Zampini et al., 2007, Tajadura-Jimenez et al., 2009) and neuroimaging (Bremmer et al., 2001, Makin et al., 2007, Gentile et al., 2011, Brozzoli et al., 2011, Huang et al., 2012, Sereno and Huang, 2014) supports the existence of a similar system integrating multisensory information within the PPS in the human brain (see Makin et al., 2007, Ladavas and Serino, 2008, Macaluso and Maravita, 2010, Brozzoli et al., 2014 for reviews).

Recent studies have focused on elucidating the interaction between PPS representation and the motor system in humans. Makin, Holmes, Brozzoli, Rossetti, and Farnè (2009), as well as Serino, Annella, and Avenanti (2009), have shown that the excitability of the hand representation along the corticospinal tract is modulated as a function of the location of visual (Makin et al., 2009) or auditory (Serino et al., 2009) stimuli presented near or far from the hand. It was found that the direction (facilitation vs. inhibition) and the timing (from 50 to 300 ms) of the modulation of the motor hand representation depends on the current state of the motor system itself (i.e., whether participants were preparing an action or were at rest) and originates from areas within the parieto-frontal PPS network. Indeed, Avenanti, Annela, and Serino (2012) have shown that virtual lesions to the PMc (provoked by means of transcutaneous direct current stimulation) abolished the modulation of the hand motor representation in the cortico-spinal tract due to the presence of near or far sounds (Avenanti et al., 2012, see also Serino, Canzoneri, and Avenanti (2011), for similar effects on reaction time data). Taken together these findings reveal a direct connection between the processing of sensory stimuli near the hand and on-going motor outputs, supporting the claim that PPS representation might act as multisensory–motor interface between the body and the environment also in humans.

Other lines of evidence further suggest that it is not only the case that PPS representation modulates the motor system, but also that actions conversely define PPS representation, i.e. actions determine what is coded as far and near space. For instance, both in monkeys (Iriki, Tanaka, & Iwamura, 1996) and in humans (Farnè and Làdavas, 2000, Berti and Frassinetti, 2000, Maravita et al., 2001, Serino et al., 2007, Canzoneri et al., 2013) using a tool to act upon the far space extends PPS representation, so that far stimuli in the space where the tool is used are subsequently coded as being within the PPS (see Maravita and Iriki (2004) for a review). More recently, Brozzoli, Pavani, Urquizar, Cardinali, and Farnè (2009) showed that visuo–tactile interaction between tactile stimuli applied to the hand and visual stimuli shown on a far object, that participants were asked to reach-to-grasp, was stronger during the execution and even during the initiation of the reach-to-grasp movement, as compared to when the hand was static (see also Brozzoli, Cardinali, Pavani, and Farnè (2010)).

In summary, data from monkeys and humans support the view that the fronto-parietal PPS system integrates multisensory stimuli in the space around the body and is involved in the translation of such multisensory representations into potential motor acts. However, most evidence supporting this view comes from studies investigating the representation of PPS around the hand, mainly focusing on visuo–tactile interactions and involving hand movements, while head or full body movements have been relatively neglected. Our movements, however, are not limited to upper limb actions, but frequently involve movements of the whole body in space; as during locomotion. In the present study, we asked whether and how the PPS representation varies during the most common full body action, i.e., walking.

Our group has developed a behavioral measure to quantify the extension of PPS around different body parts, i.e. the upper limb (Canzoneri et al., 2012, Canzoneri et al., 2013;Canzoneri, Amoresano, Marzolla, Verni, & Serino, 2013), and the face (Teneggi, Canzoneri, di Pellegrino, & Serino, 2013). In this task, participants are requested to respond as fast as possible to a tactile stimulus administered on their chest, while task-irrelevant sounds are presented, giving the impression of a sound source looming toward or receding from their bodies. The tactile stimulus is given at five different temporal delays from sound onset, implying that tactile information is processed when the sound is perceived at five different distances from the subject. Because we have repeatedly shown that a sound boosts tactile reaction times when presented close to, but not far from, the stimulated body part, that is, within and not outside the PPS (Serino et al., 2007, Serino et al., 2011, Bassolino et al., 2010), we use that task to capture the critical distance from the participant’s bodies where sounds affect tactile reaction time as a proxy for the boundary of PPS representation.

In Experiment 1, the aforementioned paradigm was applied while participants either stood immobile or walked on a treadmill. In such a manner we measured the extension of peri-chest space, and how it varied during locomotion, while the body part onto which we applied touch was neither moving in tridimensional space, nor performing the motor execution itself (as it is mainly the legs and also arms, but not the chest, that move during locomotion). In this way we minimized any confounding effect on tactile processing due to movement of the stimulated body part and we kept constant the relative distance between the sound source and the stimulated body part for the walking and the immobile condition. If whole-body actions shape PPS representation, we predicted that PPS would be extended while participants walked, as compared to they were immobile, implying that the distance where sounds affect tactile processing should be farther away from the participants in the former as compared to the latter condition.

In Experiment 2 we tested the role of concurrent visual information conveying optic flow cues in shaping PPS representation. To this aim, while walking or standing immobile on the treadmill, participants were also exposed to an optic flow projected onto a 10 m2 screen in front of them. Optic flow is a powerful visual cue implying forward translations (Royden & Moore, 2012), especially during walking (Gibson, 1950). Thus, results from Experiment 2, i.e., with optic flow, have been compared to the no-optic flow conditions run in Experiment 1, in order to determine whether kinematic information related to body motion or visual information related to the environment is critical in shaping PPS representation.

Section snippets

Participants

Eighteen (7 female, mean age 23 years old, ±3) participants took part in Experiment 1 and another 18 in Experiment 2 (9 female, mean age 25 years old, ±4). None of the subjects participated in both experiments. Participants had normal or corrected-to-normal visual acuity and reported normal tactile and auditory sensitivity. All participants gave their informed consent to take part in this study, which was approved by the local ethics committee – La Commission d’Ethique de la Recherche Clinique

Results

Experiment 1

There were no detection omissions, and a Paired-Samples t-test on the number of false alarms reveled no difference between Standing still (2.0%, S.E.M.=1.1%) and Walking (M=1.8%, S.E.M.=1.4) (t<1).

Baseline-corrected audio–tactile RT were submitted to a repeated-measures ANOVA (Locomotion condition×Sound Direction×Sound Distance), and findings presented a significant Locomotion condition×Sound Direction (F(1,17)=8.93, p<0.001, η2=0. 34), Locomotion condition×Sound Distance (F(4,68)=3.71, p

Discussion

In the present study we show that during a full body action, as is the case of walking, the PPS representation of the chest expands in the direction of walking. We found that, while our participants were walking, looming sounds interacted with processing of tactile information on the body when they were located at farther distances than compared to when participants were standing. Two related findings support this conclusion. First, we found that while participants were standing and immobile,

Acknowledgments and funding

Authors would like to acknowledge Javier Bello Ruiz and Henrique De Barba for technical assistance. AS is supported by the Volkswagen Foundation (the Un(bound) Body project, Ref. 87 336) and OB is supported by the Swiss National Science Foundation (CRSII1_125135/1) and the Bertarelli foundation.

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