Full body action remapping of peripersonal space: The case of walking
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.
References (84)
- et al.
Suppression of premotor cortex disrupts motor coding of peripersonal space
NeuroImage
(2012) - et al.
Everyday use of the computer mouse extends peripersonal space representation
Neuropsychologia
(2010) - et al.
Full-body illusions and minimal phenomenal selfhood
Trends in Cognitive Sciences
(2009) - et al.
Polymodal motion processing in posterior parietal and premotor cortex: a human fMRI study strongly implies equivalencies between humans and monkeys
Neuron
(2001) - et al.
Action specific remapping of peripersonal space
Neuropsychologia
(2010) - et al.
Shaping multisensory action-space with tools: evidence from patients with cross-modal extinction
Neuropsychologia
(2005) - et al.
The involve- ment of monkey premotor cortex neurones in preparation of visually cued arm movements
Behavioral Brain Research
(1985) - et al.
Complex movements evoked by microstimulation of precentral cortex
Neuron
(2002) - et al.
Parieto-frontal interactions, personal space, and defensive behavior
Neuropsychologia
(2006) - et al.
Tool-use: capturing multisensory spatial attention or extending multisensory peripersonal space?
Cortex
(2007)
The limits of agency in walking humans
Neuropsychologia
The representation of space near the body through touch and vision
Neuropsychologia
Neural bases of peri-hand space plasticity through tool-use: insights from a combined computational–experimental approach
Neuropsychologia
On the other hand: dummy hands and peripersonal space
Behavioural Brain Research
Reaching with a tool extends visual-tactile interactions into far space: evidence from cross-modal extinction
Neuropsychologia
Tools for the body (schema)
Trends in Cognitive Sciences
Afferent properties of periarcuate neurons in macque monkeys
Behavioural Brain Research
Use of speed cues in the detection of moving objects by moving observers
Vision Research
Virtual-reality techniques resolve the visual cues used by fruit flies to evaluate object distances
Current Biology
Multisensory maps in parietal cortex
Current Opinion in Neurobiology
Auditory-somatosensory multisensory interactions are spatially modulated by stimulated body surface and acoustic spectra
Neuropsychologia
Social modulation of peripersonal space boundaries
Current Biology
Auditory-somatosensory multisensory interactions in front and rear space
Neuropsychologia
Reference frames for representing visual and tactile locations in parietal cortex
Nature Neuroscience
Motion parallax is used to control postural sway during walking
Experimental Brain Research
The role of central and peripheral vision in postural control during walking
Perception & Psychophysics
When far becomes near: remapping of space by tool use
Journal of Cognitive Neuroscience
Coding of far and near space during walking in neglect patients
Neuropsychology
Multisensory brain mechanisms of bodily self- consciousness
Nature Reviews Neuroscience
Space-dependent representation of objects and other’s action in monkey ventral premotor grasping neurons
Journal of Neuroscience
Visual disorientation with special reference to lesions of the right cerebral hemisphere
Brain
Heading encoding in the macaque ventral intraparietal area (VIP)
European Journal of Neuroscience
Multisensory representation of the space near the hand: from perception to action and interindividual interactions
Neuroscientist
That’s near my hand! Parietal and premotor coding of hand-centered space contributes to localization and self-attribution of the hand
Journal of Neuroscience
FMRI adaptation reveals a cortical mechanism for the coding of space near the hand
Journal of Neuroscience
Grasping actions remap peripersonal space
NeuroReport
Mirror neurons differently encode the peripersonal and extrapersonal space of monkeys
Science
Amputation and prosthesis implantation shape body and peripersonal space representations
Scientific Reports
Dynamic sounds capture the boundaries of peripersonal space representation in humans
PLoS One
Tool-use reshapes the boundaries of body and peripersonal space representations
Experimental Brain Research
Whatever next? Predictive brains, situated agents, and the future of cognitive science
Behavioral and Brain Sciences
Sensorimotor integration in the precentral gyrus: polysensory neurons and defensive movements
Journal of Neurophysiology
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2022, Consciousness and CognitionCitation Excerpt :Thus, not only individuals with higher EC scores appear to have a ‘weaker’ representation of PPS (irrelevant stimuli presented within PPS, at near and middle locations, elicit a weaker interference response) as compared to lower EC individuals, they also show less differentiation between the representation of the space immediately surrounding the body (PPS) and the space beyond reach (extra-personal space, EPS). The multisensory representation of the space near the body where body-object interactions occur is characterized by plastic properties, with PPS boundaries shaped by the intention to execute a goal-directed movement (e.g. Brozzoli, 2009; Brozzoli, 2010; Canzoneri, Magosso, & Serino, 2012; Noel et al., 2015) and by temporary or permanent changes to the body that restrict or increase the range of possible movements (e.g. Canzoneri, Marzolla, Amoresano, Verni, & Serino, 2013; Holmes, 2012; Maravita et al., 2001; Serino et al., 2007). Notably, the system responsible for PPS appears to be involved also in the representation of other people whose PPS is likely to overlap with one’s own during social interactions (social PPS; e.g. Bogdanova et al., 2021; Brozzoli, Ehrsson, & Farnè, 2014; Coello & Cartaud, 2021; Di Pellegrino & Ladavas, 2015; Serino, 2019).
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2021, CortexCitation Excerpt :In addition, participants who were able to improve their interoceptive accuracy show more pronounced changes in sigmoid curve slope in the visual-tactile task and changes in their subjective experience of the self in space assessed by means of questionnaires (Noel, Park, et al., 2018). Interoceptive awareness, based on the perception of inner state of the body may thus be related to PPS representation (Ardizzi & Ferri, 2018; Cartaud et al., 2018; Noel, Park, et al., 2018; Noel, Pfeiffer, et al., 2015; Rabellino, Frewen, McKinnon, & Lanius, 2020; Rossetti et al., 2015; Scandola et al., 2020). Interestingly, it has recently been suggested that the multisensory mechanism of PPS representation contributes to a representation of the self as distinct from the environment and the others and contributes to Bodily Self-Consciousness (Blanke, Slater, & Serino, 2015; Noel, Bertoni, et al., 2020; Noel, Failla, et al., 2020; Noel, Lytle, Cascio, & Wallace, 2018; Scandola et al., 2020; Serino, 2019).