An Action Field Theory of Peripersonal Space
Authors: Rory J. Bufacchi, Gian Domenico Iannetti
Journal: Trends in Cognitive Sciences (2018)

Many behavioural and neurophysiological responses depend on the proximity of environmental stimuli to the body or to specific body parts. This has led to the intuitive, but ill-defined, concept of PPS as a single, distance-based, in-or-out zone. However, this intuitive framework is contradicted by empirical data. PPS is instead better conceptualised as a set of several different graded fields, affected by many factors other than stimulus proximity. PPS fields emphasize different behavioural functions and, thus, are better understood as mappings onto behaviour, rather than as representations of stimulus configuration. This reconceptualisation incorporates PPS into mainstream theories of action selection and behaviour. Predominant conceptual frameworks often describe peripersonal space (PPS) as a single, distance-based, in-or-out zone within which stimuli elicit enhanced neural and behavioural responses. Here we argue that this intuitive framework is contradicted by neurophysiological and behavioural data. First, PPS-related measures are not binary, but graded with proximity. Second, they are strongly influenced by factors other than proximity, such as walking, tool use, stimulus valence, and social cues. Third, many different PPS-related responses exist, and each can be used to describe a different space. Here, we reconceptualise PPS as a set of graded fields describing behavioural relevance of actions aiming to create or avoid contact between objects and the body. This reconceptualisation incorporates PPS into mainstream theories of action selection and behaviour. Predominant conceptual frameworks often describe peripersonal space (PPS) as a single, distance-based, in-or-out zone within which stimuli elicit enhanced neural and behavioural responses. Here we argue that this intuitive framework is contradicted by neurophysiological and behavioural data. First, PPS-related measures are not binary, but graded with proximity. Second, they are strongly influenced by factors other than proximity, such as walking, tool use, stimulus valence, and social cues. Third, many different PPS-related responses exist, and each can be used to describe a different space. Here, we reconceptualise PPS as a set of graded fields describing behavioural relevance of actions aiming to create or avoid contact between objects and the body. This reconceptualisation incorporates PPS into mainstream theories of action selection and behaviour. Interactions occurring within the space near the body have been studied in a range of disciplines, including ethology, neurophysiology, social science, architecture, and philosophy [1Remland M.S. et al.Interpersonal distance, body orientation, and touch: effects of culture, gender, and age.J. Soc. Psychol. 1995; 135: 281-297Crossref PubMed Scopus (156) Google Scholar, 2Høgh-Olesen H. Human spatial behaviour: the spacing of people, objects and animals in six cross-cultural samples.J. Cogn. Cult. 2008; 8: 245-280Crossref Scopus (14) Google Scholar, 3Hall E. The Hidden Dimension: Man's Use of Space in Public and in Private. Anchor Books, 1969Google Scholar, 4Hediger H. Studies of the Psychology and Behaviour of Captive Animals in Zoos and Circuses. Butterworths Scientific Publications, 1955Google Scholar, 5de Vignemont F. Mind the Body: An Exploration of Bodily Self-Awareness. Oxford University Press, 2017Crossref Scopus (48) Google Scholar]. Such studies have shown that many behavioural responses are increased when stimuli occur near the body. This phenomenon makes evolutionary sense: a predator within striking distance is more relevant than one farther away. Neuroscientific studies in both primates and humans have suggested a physiological foundation for such behavioural modulations, leading to the concept of peripersonal space (PPS). But what is precisely meant when referring to PPS? This seemingly naïve question is in fact not easy to answer, as demonstrated by the great deal of terminological and conceptual confusion in the field (Box 1). A clear conceptual framework is lacking. A current and predominant perspective on PPS describes it as a single, distance-based, in-or-out space. While a sharp spatial boundary may be intuitively appealing, neurophysiological and behavioural data contradict the description of an in-or-out space. For example, many PPS-related neurons respond to stimuli with graded or even reverse relationships to distance [6Duhamel J.R. et al.Ventral intraparietal area of the macaque: congruent visual and somatic response properties.J. Neurophysiol. 1998; 79: 126-136Crossref PubMed Scopus (611) Google Scholar, 7Colby C.L. et al.Ventral intraparietal area of the macaque: anatomic location and visual response properties.J. Neurophysiol. 1993; 69: 902-914Crossref PubMed Scopus (557) Google Scholar]. Behavioural responses in humans are also graded with distance [8Van der Stoep N. et al.Multisensory interactions in the depth plane in front and rear space: a review.Neuropsychologia. 2015; 70: 335-349Crossref PubMed Scopus (42) Google Scholar, 9Bufacchi R.J. et al.A geometric model of defensive peripersonal space.J. Neurophysiol. 2016; 115: 218-225Crossref PubMed Scopus (34) Google Scholar, 10Longo M.R. Lourenco S.F. Space perception and body morphology: extent of near space scales with arm length.Exp. Brain Res. 2007; 177: 285-290Crossref PubMed Scopus (98) Google Scholar]. These findings challenge a simple in-or-out definition. There is also reason to question a purely distance-based definition of PPS. PPS responses are influenced by factors such as walking, motion of body parts, tool use, stimulus trajectory, and stimulus valence [11Noel J.P. et al.Full body action remapping of peripersonal space: the case of walking.Neuropsychologia. 2014; 70: 375-384Crossref PubMed Scopus (88) Google Scholar, 12Wallwork S.B. et al.The blink reflex magnitude is continuously adjusted according to both current and predicted stimulus position with respect to the face.Cortex. 2016; 81: 168-175Crossref PubMed Scopus (19) Google Scholar, 13Iriki A. et al.Coding of modified body schema during tool use by macaque postcentral neurones.Neuroreport. 1996; 7: 2325-2330Crossref PubMed Scopus (929) Google Scholar, 14Taffou M. Viaud-Delmon I. Cynophobic fear adaptively extends peri-personal space.Front. Psychiatry. 2014; 5: 3-9Crossref PubMed Scopus (62) Google Scholar, 15Cléry J. et al.Impact prediction by looming visual stimuli enhances tactile detection.J. Neurosci. 2015; 35: 4179-4189Crossref PubMed Scopus (57) Google Scholar]. Finally, PPS is often presented as 'the' PPS, implying it to be a single entity. However, many different PPS-related responses exist [8Van der Stoep N. et al.Multisensory interactions in the depth plane in front and rear space: a review.Neuropsychologia. 2015; 70: 335-349Crossref PubMed Scopus (42) Google Scholar, 16Cléry J. et al.Neuronal bases of peripersonal and extrapersonal spaces, their plasticity and their dynamics: knowns and unknowns.Neuropsychologia. 2015; 70: 313-326Crossref PubMed Scopus (148) Google Scholar], and each can be used to describe a different space. These facts call the notion of a single PPS into question.Box 1Definitional Issues with Peripersonal SpaceHere, we provide examples of the terminological and conceptual confusion in the existing literature about peripersonal space (PPS). This term is typically used with three different meanings, as described below.Meaning 1: the portion of space within a given Euclidian distance of the body (e.g.: '[…] the space immediately around the animal (peripersonal space)' [22Gentilucci M. et al.Visual responses in the postarcuate cortex (area 6) of the monkey that are independent of eye position.Exp. Brain Res. 1983; 50: 464-468PubMed Google Scholar]).Meaning 2: the space within which certain physiological or behavioural responses are larger when the stimuli eliciting them occur near the body (e.g. 'The spatial extent to which visuotactile interactions strongly occur is known as visuotactile peripersonal space (hereafter called "peripersonal space")' [83van der Stoep N. et al.Depth: the forgotten dimension.Multisens. Res. 2016; 29: 493-524Crossref Scopus (23) Google Scholar]).Meaning 3: the mechanisms through which the brain represents the space near the body (e.g. 'a multisensory representation of the space surrounding the body, i.e. the peripersonal space (PPS)' [85Farnè A. et al.Shaping multisensory action-space with tools: evidence from patients with cross-modal extinction.Neuropsychologia. 2005; 43: 238-248Crossref PubMed Scopus (179) Google Scholar]).While meaning #1 poses no problems, it is not physiologically interesting: in this meaning, PPS is immutable and exists regardless of the individual being alive or dead, and therefore is not adequate to explain the phenomenon that PPS can change in size. When this occurs, meanings #2 and/or #3 are invoked. However, a serious problem arises when meanings #2 and #3 are considered equivalent. Typically, when it is observed that a physiological response function changes with proximity (i.e., PPS in meaning #2), it is also presented as evidence that the neural representation of near space (i.e., PPS in meaning #3) expands, contracts, or changes shape. However, this equivalence between 'the space within which certain physiological or perceptual responses are larger when the stimuli eliciting them occur near the body' and 'the mechanisms through which the brain represents the space near the body' is false. While it is true that a measure dependent on spatial proximity (meaning #2) tells us something about how the brain represents near space (meaning #3), it is not true that a modulation of the measure dependent on spatial proximity (meaning #2) necessarily means that the brain has changed how it represents near space (and that 'PPS has expanded/contracted'; meaning #3). In fact, this false equivalence can even be found when PPS is initially defined geometrically (i.e., using meaning #1), but is later said to change in size or shape to accommodate observations. These various definitions are often used even within the same sentence, for example 'Peripersonal space (PPS), defined as the space immediately surrounding the body [meaning #1], is now well accepted as a region of integration of somatosensory, visual, and auditory information [meaning #2]. It is a privileged interface for interaction with nearby objects [meaning #3]' [86Yang G.Z. et al.The grand challenges of science robotics.Sci. Robot. 2018; 3eaar7650Crossref PubMed Scopus (555) Google Scholar]. Notably, we are not exempt from this criticism ourselves: 'The defensive peripersonal space (DPPS) is a portion of space surrounding the body [meaning #1] with a crucial protective function [meaning #3]. Whenever a potentially dangerous stimulus approaches or enters this area, the individual engages in protective actions aimed at avoiding or minimising harm [meaning #2]' [42Bufacchi R.J. et al.Pain outside the body: defensive peripersonal space deformation in trigeminal neuralgia.Sci. Rep. 2017; 712487Crossref PubMed Scopus (15) Google Scholar]. Such conflations of meanings are likely to cause conceptual misunderstandings. Here, we provide examples of the terminological and conceptual confusion in the existing literature about peripersonal space (PPS). This term is typically used with three different meanings, as described below. Meaning 1: the portion of space within a given Euclidian distance of the body (e.g.: '[…] the space immediately around the animal (peripersonal space)' [22Gentilucci M. et al.Visual responses in the postarcuate cortex (area 6) of the monkey that are independent of eye position.Exp. Brain Res. 1983; 50: 464-468PubMed Google Scholar]). Meaning 2: the space within which certain physiological or behavioural responses are larger when the stimuli eliciting them occur near the body (e.g. 'The spatial extent to which visuotactile interactions strongly occur is known as visuotactile peripersonal space (hereafter called "peripersonal space")' [83van der Stoep N. et al.Depth: the forgotten dimension.Multisens. Res. 2016; 29: 493-524Crossref Scopus (23) Google Scholar]). Meaning 3: the mechanisms through which the brain represents the space near the body (e.g. 'a multisensory representation of the space surrounding the body, i.e. the peripersonal space (PPS)' [85Farnè A. et al.Shaping multisensory action-space with tools: evidence from patients with cross-modal extinction.Neuropsychologia. 2005; 43: 238-248Crossref PubMed Scopus (179) Google Scholar]). While meaning #1 poses no problems, it is not physiologically interesting: in this meaning, PPS is immutable and exists regardless of the individual being alive or dead, and therefore is not adequate to explain the phenomenon that PPS can change in size. When this occurs, meanings #2 and/or #3 are invoked. However, a serious problem arises when meanings #2 and #3 are considered equivalent. Typically, when it is observed that a physiological response function changes with proximity (i.e., PPS in meaning #2), it is also presented as evidence that the neural representation of near space (i.e., PPS in meaning #3) expands, contracts, or changes shape. However, this equivalence between 'the space within which certain physiological or perceptual responses are larger when the stimuli eliciting them occur near the body' and 'the mechanisms through which the brain represents the space near the body' is false. While it is true that a measure dependent on spatial proximity (meaning #2) tells us something about how the brain represents near space (meaning #3), it is not true that a modulation of the measure dependent on spatial proximity (meaning #2) necessarily means that the brain has changed how it represents near space (and that 'PPS has expanded/contracted'; meaning #3). In fact, this false equivalence can even be found when PPS is initially defined geometrically (i.e., using meaning #1), but is later said to change in size or shape to accommodate observations. These various definitions are often used even within the same sentence, for example 'Peripersonal space (PPS), defined as the space immediately surrounding the body [meaning #1], is now well accepted as a region of integration of somatosensory, visual, and auditory information [meaning #2]. It is a privileged interface for interaction with nearby objects [meaning #3]' [86Yang G.Z. et al.The grand challenges of science robotics.Sci. Robot. 2018; 3eaar7650Crossref PubMed Scopus (555) Google Scholar]. Notably, we are not exempt from this criticism ourselves: 'The defensive peripersonal space (DPPS) is a portion of space surrounding the body [meaning #1] with a crucial protective function [meaning #3]. Whenever a potentially dangerous stimulus approaches or enters this area, the individual engages in protective actions aimed at avoiding or minimising harm [meaning #2]' [42Bufacchi R.J. et al.Pain outside the body: defensive peripersonal space deformation in trigeminal neuralgia.Sci. Rep. 2017; 712487Crossref PubMed Scopus (15) Google Scholar]. Such conflations of meanings are likely to cause conceptual misunderstandings. While conceptualising PPS as a single distance-based in-or-out zone may allow for efficient summary of results, it is increasingly clear that this simple framework has become a source of data misinterpretations and conceptual misunderstandings. Here, we offer a new framework. Rather than describe PPS simply as an in-or-out zone, we propose reconceptualising PPS as a set of graded response fields. Each field describes the magnitude of a certain physiological or perceptual measure that reflects the behavioural relevance of a stimulus to a given action or set of actions. Specifically, we refer to those actions that aim to either create or avoid contact between objects and the body. This framework contains three concepts with important implications: (i) a field allows PPS measures to change gradually with distance, rather than to define an in-or-out space; (ii) a set of fields reflects the fact that there are many different PPS measures showing different response profiles; and (iii) behavioural relevance to actions aiming to create or avoid contact between objects and the body explains the functional significance of the values composing the PPS field of each action, and the fact that factors other than proximity affect PPS measures. We believe that this framework can explain seemingly anomalous empirical observations, and resolve some of the definitional and conceptual issues affecting the field. In probably the first observations of a link between brain function and the processing of sensory stimuli occurring near the body, the British neurologist Lord Brain [17Brain W.R. Visual disorientation with special reference to lesions of the right cerebral hemisphere.Brain. 1941; 64: 244-272Crossref Scopus (491) Google Scholar] noticed that certain lesions of parietal cortex led to perceptual problems in near space, but not in far space. During the 1950s, the Swiss zoologist Heini Hediger observed that behavioural responses depended upon the distance of the triggering stimulus. He reported that stimuli near the animal (inside a so-called 'flight zone') elicited a flight response, whereas stimuli outside the flight zone elicited no response [4Hediger H. Studies of the Psychology and Behaviour of Captive Animals in Zoos and Circuses. Butterworths Scientific Publications, 1955Google Scholar, 18Hediger H. Wild Animals in Captivity. Buttersworth Scientific Publications, 1950Google Scholar]. In 1969, the influential anthropologist Edward Hall, the father of proxemics, published a book about the importance of space to human behaviour [3Hall E. The Hidden Dimension: Man's Use of Space in Public and in Private. Anchor Books, 1969Google Scholar]. He distinguished between intimate space (up to 45 cm), personal space (up to 1.2 m), social space (up to 3.6 m), and public space. While their empirical evidence did not support the existence of multiple distinct spaces, these authors nonetheless opted to present their findings as though there were multiple distinct spaces, probably to ease the understanding of the reader. While informative, these early seminal studies therefore implicitly set the tone that near and far space have sharp boundaries. Studies and interpretations over the next several decades adopted this simple framework. However, a closer look at many of these studies challenges such a framework. For example, studies of bimodal single neurons in macaques illustrate how data and interpretation often disconnect [7Colby C.L. et al.Ventral intraparietal area of the macaque: anatomic location and visual response properties.J. Neurophysiol. 1993; 69: 902-914Crossref PubMed Scopus (557) Google Scholar, 19Hyvarinen J. Poranen A. Function of the parietal associative area 7 as revealed from cellular discharges in alert monkeys.Brain. 1974; 97: 673-692Crossref PubMed Google Scholar, 20Leinonen L. Nyman II, G. Functional properties of cells in anterolateral part of area 7 associative face area of awake monkeys.Exp. Brain Res. 1979; 34: 321-333Crossref PubMed Scopus (150) Google Scholar, 21Rizzolatti G. et al.Afferent properties of periarcuate neurons in macaque monkeys. II. Visual responses.Behav. Brain Res. 1981; 2: 147-163Crossref PubMed Scopus (526) Google Scholar, 22Gentilucci M. et al.Visual responses in the postarcuate cortex (area 6) of the monkey that are independent of eye position.Exp. Brain Res. 1983; 50: 464-468PubMed Google Scholar, 23Graziano M.S. Gross C.G. A bimodal map of space: somatosensory receptive fields in the macaque putamen with corresponding visual receptive fields.Exp. Brain Res. 1993; 97: 96-109Crossref PubMed Scopus (304) Google Scholar]. In these studies, bimodal neurons were identified in both cortical and subcortical structures (putamen, parietal, and premotor areas). These neurons responded not only to somatosensory stimuli, but also to visual or auditory stimuli presented in spatial proximity to the somatosensory receptive field. The authors emphasised the larger neural response magnitudes to stimuli in near space versus the smaller neural response magnitudes to stimuli in far space. To illustrate these findings, such neurons were often described as demarcating zones of space, represented as bubbles with clear boundaries [24Graziano M.S. Cooke D.F. Parieto-frontal interactions, personal space, and defensive behavior.Neuropsychologia. 2006; 44: 845-859Crossref PubMed Scopus (421) Google Scholar] (Figure 1). However, these boundaries were simply lines of arbitrary response magnitude [25Graziano M.S. et al.Visuospatial properties of ventral premotor cortex.J. Neurophysiol. 1997; 77: 2268-2292Crossref PubMed Scopus (481) Google Scholar]. Other authors similarly defined such boundaries as the 'part of space which gave consistent responses', again resulting in arbitrary and ill-defined in-or-out zones [26Gentilucci M. et al.Functional organization of inferior area 6 in the macaque monkey. I. Somatotopy and the control of proximal movements.Exp. Brain Res. 1988; 71: 475-490Crossref PubMed Scopus (430) Google Scholar]. The fact that some neurons did respond preferentially to stimuli occurring near a given body part was presented as the most novel and memorable aspect of these studies. Therefore, on the surface, these neurophysiological studies appeared to confirm, at the neural level, the conception by seminal studies of a sharply defined 'in-or-out' near space. However, the data in these same studies clearly illustrate that response magnitudes are not simple step-like functions but have far more complex properties. In many cases, the responses appear to be gradual, rather than step-wise, proximity functions [6Duhamel J.R. et al.Ventral intraparietal area of the macaque: congruent visual and somatic response properties.J. Neurophysiol. 1998; 79: 126-136Crossref PubMed Scopus (611) Google Scholar, 7Colby C.L. et al.Ventral intraparietal area of the macaque: anatomic location and visual response properties.J. 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Indeed, while the response magnitude of some neurons increases rapidly with stimulus proximity between two consecutive tested points, thus defining what appears to be a 'sharply delimited receptive field' [7Colby C.L. et al.Ventral intraparietal area of the macaque: anatomic location and visual response properties.J. Neurophysiol. 1993; 69: 902-914Crossref PubMed Scopus (557) Google Scholar], most neurons show a less steep response gradient [7Colby C.L. et al.Ventral intraparietal area of the macaque: anatomic location and visual response properties.J. Neurophysiol. 1993; 69: 902-914Crossref PubMed Scopus (557) Google Scholar]. In addition to this graded response, a sizeable portion of multimodal neurons (e.g., ∼5% of recorded neurons in ventral premotor cortex [24Graziano M.S. Cooke D.F. Parieto-frontal interactions, personal space, and defensive behavior.Neuropsychologia. 2006; 44: 845-859Crossref PubMed Scopus (421) Google Scholar]) exhibit receptive fields that extend further than reaching distance, sometimes even to the end of the room [7Colby C.L. et al.Ventral intraparietal area of the macaque: anatomic location and visual response properties.J. Neurophysiol. 1993; 69: 902-914Crossref PubMed Scopus (557) Google Scholar, 25Graziano M.S. et al.Visuospatial properties of ventral premotor cortex.J. Neurophysiol. 1997; 77: 2268-2292Crossref PubMed Scopus (481) Google Scholar]. Therefore, neuronal response functions are not only more continuous than usually presented, but some of these response functions also encompass a much larger area than commonly reported. Finally, some neurons even show the reverse of the expected near versus far relationship: in both premotor and parietal regions, they respond less strongly to visual stimuli near their somatosensory receptive field than to visual stimuli slightly further away in space [7Colby C.L. et al.Ventral intraparietal area of the macaque: anatomic location and visual response properties.J. Neurophysiol. 1993; 69: 902-914Crossref PubMed Scopus (557) Google Scholar, 21Rizzolatti G. et al.Afferent properties of periarcuate neurons in macaque monkeys. II. Visual responses.Behav. Brain Res. 1981; 2: 147-163Crossref PubMed Scopus (526) Google Scholar, 26Gentilucci M. et al.Functional organization of inferior area 6 in the macaque monkey. I. Somatotopy and the control of proximal movements.Exp. Brain Res. 1988; 71: 475-490Crossref PubMed Scopus (430) Google Scholar]. Taken together, these empirical data demonstrate that a step-like proximity function is an inadequate description of PPS. These interpretive issues are not limited to neurophysiology experiments: the psychophysical literature suffers analogous oversimplifications. At first, most psychophysical experiments would often test only two conditions: near versus far. Such 'near versus far' experiments were performed using various behavioural measures, such as line bisection [29McCourt M.E. Garlinghouse M. Asymmetries of visuospatial attention are modulated by viewing distance and visual field elevation: pseudoneglect in peripersonal and extrapersonal space.Cortex. 2000; 36: 715-731Abstract Full Text PDF PubMed Scopus (84) Google Scholar], visuotactile extinction [30Làdavas E. et al.Visual peripersonal space centred on the face in humans.Brain. 1998; 121: 2317-2326Crossref PubMed Scopus (84) Google Scholar], audiotactile extinction [31Farnè A. Làdavas E. Auditory peripersonal space in humans.J. Cogn. Neurosci. 2002; 14: 1030-1043Crossref PubMed Scopus (98) Google Scholar], visuotacile interaction [32Sambo C.F. 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Indeed, most researchers are aware that the responses change continuously between the sampled near and far positions: sampling two points along a continuum does not negate that continuum. However, the binary experimental design implies a binary response pattern, precluding a more complete conceptual understanding of PPS. Even in the subset of psychophysical experiments where more stimulus locations were tested, and the corresponding responses clearly showed a graded fall-off, authors often continued to present results as 'in-or-out' zones using simple summary statistics, such as the point of first increase over baseline activity [35Sambo C.F. Iannetti G.D. Better safe than sorry? The safety margin surrounding the body is increased by anxiety.J. 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