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Spotlight
Variability in Multisensory Responses Predicts the Self-Space Andrea Serino1,2,* Our brains distinguish between stimuli that are close enough to interact with our bodies and those that are further away by generating a multisensory representation of space near the self, termed peripersonal space. Recent findings show that variability in neuronal response to audio-tactile stimuli predicts the location of the peripersonal space boundary at the individual level. Mapping the space immediately surrounding the body is critical for behaviour, as this is where most interactions between the individual and the external world happen, both in terms of defending the body from threats or approaching interesting stimuli. Thus, the brain hosts a dedicated system to specifically process information occurring on and near the body, [1_TD$IF]that is, to represent the so-called peripersonal space (PPS). PPS was originally described in monkeys as the result of the activity of special multisensory neurons, mostly in fronto-parietal regions, integrating tactile stimulation on a part of the animal's body and visual or auditory stimuli presented close to that body part [1]. Further studies showed that a similar PPS system is implemented in the human brain by a homologous network of fronto-parietal areas [2]. Thus, although there is no physical separation in the real world between the PPS and the far, or extrapersonal, space, our brains do represent a boundary between what is close to our bodies, and therefore can potentially and rapidly interact with them, and what is further away. Interestingly, the location of the
PPS boundary is not fixed. It varies both between individuals and within individuals between contexts. For instance, PPS appears to be larger in people with high anxiety or claustrophobia traits than those without these traits [3]. For the same individual, PPS also appears to be extended after the individual uses a tool to reach into extrapersonal space [4]. A recent paper by Ferri and colleagues [5] proposes a possible neural mechanism determining the extent of individuals’ PPS. They first used a behavioural task developed by my group to measure participants’ PPS [6]. Subjects received a tactile stimulation on their hand while a looming sound approached their hand. Tactile stimuli can be administered at different delays from sound onset, so that touch is processed when the sound is perceived at different distances. Although participants were instructed to ignore sounds, reaction times to touch became faster as the sound approached their bodies and the critical spatial position where this multisensory facilitation effect occurred was used as a proxy for the location of the PPS boundary. A similar task was also administered during fMRI: the authors compared neural activity to tactile hand stimulation when a sound was presented either near or far from the hand.
boundaries at the individual level. Specifically, the PPS boundary was closer to the body in participants whose neural activity in the premotor cortex was more variable when the sound was presented in the far space. The Ferri et al. study and its findings are interesting for at least two reasons. First, it represents the first attempt to study not only how PPS is represented in the human brain, but to actually investigate the neural mechanisms explaining how PPS differs among individuals. This is a key approach for future studies in neuroscience. Our knowledge about the neural correlates of human behaviour should aim at explaining not only how a standardized, ideal brain works, but how everyone's brains work. It is particularly interesting that Ferri et al. applied this approach to study PPS representation, as in this field individual differences seem extensive and grounded in the way people perceive and act in their environment. Next, it would be interesting to understand why these individual differences at the neural and behavioural levels occur. Research on PPS plasticity shows that PPS boundaries adapt as a function of experience: PPS expands after using a rake to [3_TD$IF]‘touch[4_TD$IF]’ far objects [4], or even after receiving tactile stimulation on the hand coupled with synchronous stimulation from a far location. It also contracts if an arm is restricted or amputated [2]. Thus, it is likely that the extent of individuals’ PPS depends on the nature of the interactions they have experienced during their lifespan. Interactions, in this context, are not limited to low-level hand-objects contacts, but could also include abstract and cognitive exchanges with other people, as PPS also reshapes based on social interactions [7]. Thus, the open question is how individuals’ experiences with interactions have forged the neural mechanism underlying their PPS, as described by Ferri et al.
In line with previous studies [2], Ferri et al. identified a region of the premotor cortex that responded to tactile stimulation depending on the sound location. The authors then asked whether activity within this area predicted the inter-individual variability in the location of the PPS boundary, as measured by the behavioural task. Interestingly, PPS boundaries were not predicted by the level of neural activity (i.e[2_TD$IF]., mean BOLD, or blood-oxygen-level dependent, response) elicited by near versus far stimulation. Rather, the intertrial variability (i.e[2_TD$IF]., the modulation of the standard deviation of the BOLD signal Second, these data suggest that the procafter stimulus onset) in the responses to essing of far stimuli, more than near ones, far stimuli predicted the location of PPS is critical to defining PPS. The PPS system
Trends in Cognitive Sciences, Month Year, Vol. xx, No. yy
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TICS 1536 No. of Pages 2
immediately projects to the motor system to transform multisensory coding of space into potential motor reactions. Previous findings suggest that motor preparation related to PPS coding is stronger for far as compared to near stimuli [8], resonating with Ferri et al.’s data. The current findings suggest that neural coding of near stimuli is much less variable and thus more predictable than that of far stimuli. The key function of PPS neurons might be in deciding whether an approaching object would potentially touch the body or not [9]. Once this object is close to the body, the solution is easy, whereas additional neural processing is necessary to generate predictions concerning a far stimulus, and therefore related neural signal is more variable and noisy. In this view, the PPS boundary constitutes a limit between two regions of the world where external objects can or cannot interact with our bodies. In other words, PPS can be conceived as an extension of the body beyond the body, as if the skin surface is projected outward in space by a multisensory integration mechanism, creating a new interface for body-object contacts. Such a basic mechanism might also
2
Trends in Cognitive Sciences, Month Year, Vol. xx, No. yy
have evolved to support more abstract interactions, becoming a general boundary between the individual and the environment. We have recently shown that PPS boundaries shift towards a virtual body placed at a distance when participants self-identify with the virtual body during the full body illusion [2]. We suggested that PPS should be considered as the space where one perceives one's self to be, beyond that surrounding the body. Recent accounts of how the self is represented posit that self-related processing is associated with lower variability than other-related processing, as if self-consciousness arises from coherence and higher predictability of self-related signals [10]. The finding by Ferri et al. that stimuli within the PPS are associated with lower variability as compared to far stimuli resonates with these self models and suggests new intriguing links between multisensory processing within the PPS and self-representation[5_TD$IF]. Acknowledgments A.S. is supported by Bertarelli Foundation and W Investments ‘RealiSM’).
S.A.,
Switzerland
(industrial
grant
1 Laboratory of Cognitive Neuroscience, Brain Mind Institute, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland 2 Center for Neuroprosthetics, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
*Correspondence: Andrea.serino@epfl.ch (A. Serino). http://dx.doi.org/10.1016/j.tics.2016.01.005 References 1. Graziano, M.S. and Cooke, D.F. (2006) Parieto-frontal interactions, personal space, and defensive behavior. Neuropsychologia 44, 2621–2635 2. Blanke, O. et al. (2015) Behavioral, neural, and computational principles of bodily self-consciousness. Neuron 88, 145–166 3. de Vignemont, F. and Iannetti, G.D. (2015) How many peripersonal spaces? Neuropsychologia 70, 327–334 4. Maravita, A. and Iriki, A. (2004) Tools for the body (schema). Trends Cogn. Sci. 8, 79–86 5. Ferri, F. et al. (2015) Intertrial variability in the premotor cortex accounts for individual differences in peripersonal space. J. Neurosci. 35, 16328–16339 6. Serino, A. et al. (2015) Body part-centered and full bodycentered peripersonal space representations. Sci. Rep. 5, 18603 7. Teneggi, C. et al. (2013) Social modulation of peripersonal space boundaries. Curr. Biol. 23, 406–411 8. Avenanti, A. et al. (2012) Suppression of premotor cortex disrupts motor coding of peripersonal space. Neuroimage 63, 281–288 9. Cléry, J. et al. (2015) Impact prediction by looming visual stimuli enhances tactile detection. J. Neurosci. 35, 4179–4189 10. Metzinger, T. (2004) Being No One: The Self-Model Theory of Subjectivity, MIT Press
Spotlight
Variability in Multisensory Responses Predicts the Self-Space Andrea Serino1,2,* Our brains distinguish between stimuli that are close enough to interact with our bodies and those that are further away by generating a multisensory representation of space near the self, termed peripersonal space. Recent findings show that variability in neuronal response to audio-tactile stimuli predicts the location of the peripersonal space boundary at the individual level. Mapping the space immediately surrounding the body is critical for behaviour, as this is where most interactions between the individual and the external world happen, both in terms of defending the body from threats or approaching interesting stimuli. Thus, the brain hosts a dedicated system to specifically process information occurring on and near the body, [1_TD$IF]that is, to represent the so-called peripersonal space (PPS). PPS was originally described in monkeys as the result of the activity of special multisensory neurons, mostly in fronto-parietal regions, integrating tactile stimulation on a part of the animal's body and visual or auditory stimuli presented close to that body part [1]. Further studies showed that a similar PPS system is implemented in the human brain by a homologous network of fronto-parietal areas [2]. Thus, although there is no physical separation in the real world between the PPS and the far, or extrapersonal, space, our brains do represent a boundary between what is close to our bodies, and therefore can potentially and rapidly interact with them, and what is further away. Interestingly, the location of the
PPS boundary is not fixed. It varies both between individuals and within individuals between contexts. For instance, PPS appears to be larger in people with high anxiety or claustrophobia traits than those without these traits [3]. For the same individual, PPS also appears to be extended after the individual uses a tool to reach into extrapersonal space [4]. A recent paper by Ferri and colleagues [5] proposes a possible neural mechanism determining the extent of individuals’ PPS. They first used a behavioural task developed by my group to measure participants’ PPS [6]. Subjects received a tactile stimulation on their hand while a looming sound approached their hand. Tactile stimuli can be administered at different delays from sound onset, so that touch is processed when the sound is perceived at different distances. Although participants were instructed to ignore sounds, reaction times to touch became faster as the sound approached their bodies and the critical spatial position where this multisensory facilitation effect occurred was used as a proxy for the location of the PPS boundary. A similar task was also administered during fMRI: the authors compared neural activity to tactile hand stimulation when a sound was presented either near or far from the hand.
boundaries at the individual level. Specifically, the PPS boundary was closer to the body in participants whose neural activity in the premotor cortex was more variable when the sound was presented in the far space. The Ferri et al. study and its findings are interesting for at least two reasons. First, it represents the first attempt to study not only how PPS is represented in the human brain, but to actually investigate the neural mechanisms explaining how PPS differs among individuals. This is a key approach for future studies in neuroscience. Our knowledge about the neural correlates of human behaviour should aim at explaining not only how a standardized, ideal brain works, but how everyone's brains work. It is particularly interesting that Ferri et al. applied this approach to study PPS representation, as in this field individual differences seem extensive and grounded in the way people perceive and act in their environment. Next, it would be interesting to understand why these individual differences at the neural and behavioural levels occur. Research on PPS plasticity shows that PPS boundaries adapt as a function of experience: PPS expands after using a rake to [3_TD$IF]‘touch[4_TD$IF]’ far objects [4], or even after receiving tactile stimulation on the hand coupled with synchronous stimulation from a far location. It also contracts if an arm is restricted or amputated [2]. Thus, it is likely that the extent of individuals’ PPS depends on the nature of the interactions they have experienced during their lifespan. Interactions, in this context, are not limited to low-level hand-objects contacts, but could also include abstract and cognitive exchanges with other people, as PPS also reshapes based on social interactions [7]. Thus, the open question is how individuals’ experiences with interactions have forged the neural mechanism underlying their PPS, as described by Ferri et al.
In line with previous studies [2], Ferri et al. identified a region of the premotor cortex that responded to tactile stimulation depending on the sound location. The authors then asked whether activity within this area predicted the inter-individual variability in the location of the PPS boundary, as measured by the behavioural task. Interestingly, PPS boundaries were not predicted by the level of neural activity (i.e[2_TD$IF]., mean BOLD, or blood-oxygen-level dependent, response) elicited by near versus far stimulation. Rather, the intertrial variability (i.e[2_TD$IF]., the modulation of the standard deviation of the BOLD signal Second, these data suggest that the procafter stimulus onset) in the responses to essing of far stimuli, more than near ones, far stimuli predicted the location of PPS is critical to defining PPS. The PPS system
Trends in Cognitive Sciences, Month Year, Vol. xx, No. yy
1
TICS 1536 No. of Pages 2
immediately projects to the motor system to transform multisensory coding of space into potential motor reactions. Previous findings suggest that motor preparation related to PPS coding is stronger for far as compared to near stimuli [8], resonating with Ferri et al.’s data. The current findings suggest that neural coding of near stimuli is much less variable and thus more predictable than that of far stimuli. The key function of PPS neurons might be in deciding whether an approaching object would potentially touch the body or not [9]. Once this object is close to the body, the solution is easy, whereas additional neural processing is necessary to generate predictions concerning a far stimulus, and therefore related neural signal is more variable and noisy. In this view, the PPS boundary constitutes a limit between two regions of the world where external objects can or cannot interact with our bodies. In other words, PPS can be conceived as an extension of the body beyond the body, as if the skin surface is projected outward in space by a multisensory integration mechanism, creating a new interface for body-object contacts. Such a basic mechanism might also
2
Trends in Cognitive Sciences, Month Year, Vol. xx, No. yy
have evolved to support more abstract interactions, becoming a general boundary between the individual and the environment. We have recently shown that PPS boundaries shift towards a virtual body placed at a distance when participants self-identify with the virtual body during the full body illusion [2]. We suggested that PPS should be considered as the space where one perceives one's self to be, beyond that surrounding the body. Recent accounts of how the self is represented posit that self-related processing is associated with lower variability than other-related processing, as if self-consciousness arises from coherence and higher predictability of self-related signals [10]. The finding by Ferri et al. that stimuli within the PPS are associated with lower variability as compared to far stimuli resonates with these self models and suggests new intriguing links between multisensory processing within the PPS and self-representation[5_TD$IF]. Acknowledgments A.S. is supported by Bertarelli Foundation and W Investments ‘RealiSM’).
S.A.,
Switzerland
(industrial
grant
1 Laboratory of Cognitive Neuroscience, Brain Mind Institute, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland 2 Center for Neuroprosthetics, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
*Correspondence: Andrea.serino@epfl.ch (A. Serino). http://dx.doi.org/10.1016/j.tics.2016.01.005 References 1. Graziano, M.S. and Cooke, D.F. (2006) Parieto-frontal interactions, personal space, and defensive behavior. Neuropsychologia 44, 2621–2635 2. Blanke, O. et al. (2015) Behavioral, neural, and computational principles of bodily self-consciousness. Neuron 88, 145–166 3. de Vignemont, F. and Iannetti, G.D. (2015) How many peripersonal spaces? Neuropsychologia 70, 327–334 4. Maravita, A. and Iriki, A. (2004) Tools for the body (schema). Trends Cogn. Sci. 8, 79–86 5. Ferri, F. et al. (2015) Intertrial variability in the premotor cortex accounts for individual differences in peripersonal space. J. Neurosci. 35, 16328–16339 6. Serino, A. et al. (2015) Body part-centered and full bodycentered peripersonal space representations. Sci. Rep. 5, 18603 7. Teneggi, C. et al. (2013) Social modulation of peripersonal space boundaries. Curr. Biol. 23, 406–411 8. Avenanti, A. et al. (2012) Suppression of premotor cortex disrupts motor coding of peripersonal space. Neuroimage 63, 281–288 9. Cléry, J. et al. (2015) Impact prediction by looming visual stimuli enhances tactile detection. J. Neurosci. 35, 4179–4189 10. Metzinger, T. (2004) Being No One: The Self-Model Theory of Subjectivity, MIT Press
