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Coding of modified body schema during tool use by macaque postcentral neurones
Abstract
A tool is an extension of the hand in both a physical and a perceptual sense. The presence of body schemata has been postulated as the basis of the perceptual assimilation of tool and hand. We trained macaque monkeys to retrieve distant objects using a rake, and neuronal activity was recorded in the caudal postcentral gyrus where the somatosensory and visual signals converge. There we found a large number of bimodal neurones which appeared to code the schema of the hand. During tool use, their visual receptive fields were altered to include the entire length of the rake or to cover the expanded accessible space. These findings may represent neural correlates of the modified schema of the hand in which the tool was incorporated.
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“These additional regions encode diverse information related to one’s own body or the body of others, as well as their spatial position (such as PoCG, SII, LOC, or cerebellar lobule VI) (lriki et al. 1996; Disbrow et al. 2000; Grodd et al. 2001; Eickhoff et al. 2010; Bernasconi et al. 2018; Sonobe et al. 2023), visual and auditory space representation and movement detection (such as PT, STS, POS,”
From Neuroanatomical correlates of peripersonal space: bridging the gap between perception, action, emotion and social cognition (2024) · cites this paper as lriki et al. 1996
In the citing paper
“Tool use may cause changes in visuo-tactile integration (39–41) and in the receptive fields of visuo-tactile cells in the parietal cortex (42), so that it appears as if peripersonal space extends from the hand to the tool.”
From Threatening a rubber hand that you feel is yours elicits a cortical anxiety response. (2007) · cites this paper as [42]
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BackgroundCoding of Far and Near Space in Neglect Patients
Berti, A., Smania, N., & Allport, A. (2001) · NeuroImage · doi:10.1006/nimg.2001.0815 · Cited by 58
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“A dynamic, tool-use dependent re-sizing of peri-hand space representation was first reported in monkeys by Iriki and colleagues ( Iriki, Tanaka, & Iwamura, 1996 ).”
BackgroundMethodResultInfluentialCoding of far and near space during walking in neglect patients.
Berti, A., Smania, N., Rabuffetti, M., et al. (2002) · Neuropsychology · doi:10.1037/0894-4105.16.3.390 · Cited by 57
Improved visual sensitivity in the perihand space
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Gestural Communication in Nonhuman and Human Primates
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Flexible Representations of Dynamics Are Used in Object Manipulation
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Frontier of Self and Impact Prediction
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Rapid Assimilation of External Objects Into the Body Schema
Carlson, T. A., Alvarez, G. A., Wu, D.-A. J., & Verstraten, F. A. J. (2010) · Psychological Science · doi:10.1177/0956797610371962 · Cited by 53
“In a landmark study, Iriki et al. (1996) showed that neurons in intraparietal cortex reshaped their receptive fields to include tools (objects).”
BackgroundPhilosophie, technologie et cognition. Etats des lieux et perspectives
Steiner, P. (2010) · Intellectica Revue de l Association pour la Recherche Cognitive · doi:10.3406/intel.2010.1176 · Cited by 79
Somatosensory-guided tool use modifies arm representation for action
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Integration of vision and haptics during tool use
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“…et al., 2004; Tsakiris et al., 2007; Evans and Blanke, 2013) and analogous regions in the monkey brain have been found to contain trimodal neurons that integrate tactile, visual and proprioceptive signals (Fogassi et al., 1996; Iriki et al., 1996; Graziano et al., 1997; Graziano and Gandhi, 2000).”
BackgroundOn the Brain-Basis of Visual Consciousness: A Sensorimotor Account
Noë, A., & O'Regan, J. K. (2002) · The MIT Press eBooks · doi:10.7551/mitpress/7111.003.0025 · Cited by 54
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“Some neurons in the intraparietal sulcus of macaques have tactile receptive Welds (RF) on the hand, and visual RFs which encompass the space around the tactile RF. When the monkey uses a tool rather than the hand to reach for food, the visual RF of these neurons change within minutes of tool use such that the RF inclu…”
MethodIntegrating perception and action through cognitive neuropsychology (broadly conceived)
Bruno, N., & Battaglini, P. P. (2008) · Cognitive Neuropsychology · doi:10.1080/02643290802519591 · Cited by 53
“This finding extends previous data from monkey neurophysiology (Iriki, Tanaka, & Iwamura, 1996 ) and suggests that the representation of personal space is plastic and can be modified by experience with objects that extend the range of possible multisensory interactions, including tools in the standard sense but also d…”
ResultParietal mechanisms of target representation
Gottlieb, J. P. (2002) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(02)00312-4 · Cited by 54
Auletta, G. (2011) · doi:10.1093/acprof:oso/9780199608485.001.0001 · Cited by 91
Rapid and Long-Lasting Plasticity of Input-Output Mapping
Yamamoto, K., Hoffman, D. S., & Strick, P. L. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00209.2006 · Cited by 50
“Similarly, monkeys can be trained to operate complex manipulanda (Kakei et al. 1999) and to use tools like a rake to gather food treats (Iriki et al. 1996).”
BackgroundKraskov, A., Prabhu, G., Quallo, M. M., Lemon, R., & Brochier, T. G. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0525-11.2011 · Cited by 49
“…and M43) had to perform a precision grip between the tip of the thumb and the index finger to move two levers into a position window (Lemon et al., 1986) and, in the same session, use a rake to retrieve distant pieces of food from a horizontal flat board (Iriki et al., 1996; Quallo et al., 2009).”
BackgroundMethodA neuropsychological perspective on the link between language and praxis in modern humans
Roby-Brami, A., Hermsdörfer, J., Roy, A. C., & Jacobs, S. (2011) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2011.0122 · Cited by 56
Technition: When Tools Come Out of the Closet
Osiurak, F., Lesourd, M., Navarro, J., & Reynaud, E. (2020) · Perspectives on Psychological Science · doi:10.1177/1745691620902145 · Cited by 54
“This phenomenon occurs not only in humans but also in non-tool-using species trained to use tools (e.g., macaques; Iriki, Tanaka, & Iwamura, 1996; for review, see Maravita & Iriki, 2004).”
BackgroundSensory- and Action-Oriented Embodiment of Neurally-Interfaced Robotic Hand Prostheses
Di Pino, G., Romano, D., Spaccasassi, C., Mioli, A., D’Alonzo, M., Sacchetti, R., Guglielmelli, E., Zollo, L., Di Lazzaro, V., Denaro, V., et al. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00389 · Cited by 52
Dynamic expansion of alert responses to incoming painful stimuli following tool use
Rossetti, A., Romano, D., Bolognini, N., & Maravita, A. (2015) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2015.01.019 · Cited by 52
“In his seminal study, Iriki et al. (1996) trained monkeys to retrieve bits of food placed in the extra-personal space, by means of a hand-wielded rake.”
BackgroundThe Activity of Primary Motor Cortex Corticospinal Neurons during Tool Use by Macaque Monkeys
Quallo, M. M., Kraskov, A., & Lemon, R. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1009-12.2012 · Cited by 54
“It is now well established that captive macaque monkeys can learn to use a rake as a tool, using it to retrieve food rewards placed just beyond their reach (Warden et al., 1940; Shurcliff et al., 1971; Iriki et al., 1996).”
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“We also considered many other empirical, theoretical, and phenomenological studies to prepare for potential new items (e.g., Cahill, 1996; Iriki et al., 1996; Daprati et al., 1997; Botvinick and Cohen, 1998; Blakemore et al., 2000; Frith et al., 2000a; Peled et al., 2000; Fourneret et al., 2001;…”
BackgroundDifferent tool training induces specific effects on body metric representation
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Peripersonal space : a multisensory interface for body-objects interactions
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“…and functional homologies and have consequently been proposed to form a second parieto-premotor network dedicated for action (Gallese et al., 1996; Iriki et al., 1996; Matelli and Luppino, 2001; Rizzolatti and Luppino, 2001; Rizzolatti and Matelli, 2003; see for discussion Cléry et al.,…”
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“In a recent study in monkeys, Iriki et al. (1996) reported that the visual receptive field of neurons in the anterior bank of the intraparietal sulcus (IPS) changed when the monkeys were using a rake, covering not only the area around the hand but also the area along the rake.”
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Exploring self-presence in collaborative virtual teams
Ratan, R., & Hasler, B. S. (2010) · Cited by 50
Tool-use learning by common marmosets (Callithrix jacchus)
Yamazaki, Y., Echigo, C., Saiki, M., Inada, M., Watanabe, S., & Iriki, A. (2011) · Experimental Brain Research · doi:10.1007/s00221-011-2778-9 · Cited by 51
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Pia, L., Garbarini, F., Fossataro, C., Fornia, L., & Berti, A. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00298 · Cited by 48
“This is an important point since it is often assumed that touch can be referred to external objects (e.g., tips of tools; Iriki et al., 1996), whereas pain cannot.”
BackgroundEmbodied prosthetic arm stabilizes body posture, while unembodied one perturbs it
Imaizumi, S., Asai, T., & Koyama, S. (2016) · Consciousness and Cognition · doi:10.1016/j.concog.2016.08.019 · Cited by 49
Embodiment of supernumerary robotic limbs in virtual reality
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A hand in blindsight: Hand placement near target improves size perception in the blind visual field
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“For example, Iriki et al. (1996) reported that the visual receptive fields of bimodal neurons (somatosensory and vision) in the posterior parietal cortices (PPCs) of monkeys were altered during tool use such that they included the entire length of a rake or covered an expanded accessible space.”
BackgroundThe recalibration of tactile perception during tool use is body-part specific
Miller, L. E., Cawley-Bennett, A., Longo, M. R., & Saygın, A. P. (2017) · Experimental Brain Research · doi:10.1007/s00221-017-5028-y · Cited by 45
“There is strong multimodal evidence in macaques for the involvement of posterior parietal regions coding for multisensory body representations (Iriki et al. 1996; Hihara et al. 2006; Quallo et al. 2009); a recent study using repetitive transcranial magnetic stimulation has extended this finding to…”
Sensory and Motor Interfering Influences on Somatosensory Evoked Potentials
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Reaching Out With the Imagination
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“1, plain text), wherein body schemas may become adapted to perceptually assimilate objects as extensions of our own body (Paillard, 1993; Iriki et al., 1996).”
BackgroundThis racket is not mine: The influence of the tool-use on peripersonal space
Biggio, M., Bisio, A., Avanzino, L., Ruggeri, P., & Bove, M. (2017) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2017.07.018 · Cited by 50
“A great amount of studies, both on humans and monkeys, focused on the plasticity of the peripersonal space (Bourgeois and Coello, 2012; Farnè and Làdavas, 2000; Garbarini et al., 2015; Iriki et al., 1996) and on the possibility to modulate its boundaries by integrating within it a tool.”
Skill, corporality and alerting capacity in an account of sensory consciousness
O'Regan, J. K., Myin, E., & Noë, A. (2005) · Progress in brain research · doi:10.1016/s0079-6123(05)50005-0 · Cited by 50
“4; also related work on the body image in tool use: Iriki et al., 1996; Farne and Ladavas, 2000; Yamamoto and Kitazawa, 2001).”
BackgroundVisuotactile Representation of Peripersonal Space: A Neural Network Study
Magosso, E., Zavaglia, M., Serino, A., di Pellegrino, G., & Ursino, M. (2009) · Neural Computation · doi:10.1162/neco.2009.01-08-694 · Cited by 47
Neural Interaction between Spatial Domain and Spatial Reference Frame in Parietal–Occipital Junction
Chen, Q., Weidner, R., Weiss, P. H., Marshall, J. C., & Fink, G. R. (2012) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00260 · Cited by 46
“Growing evidence from neurophysiological and neuropsychological studies has shown that the active, purposeful use of a tool can extend the range of near space by changing both neural and behavioral responses (Legrand, Brozzoli, Rossetti, & Farne, 2007 ; Farne, Iriki, & Ladavas, 2005 ; Maravita, Husain, Clarke, & Drive…”
BackgroundSeeing the hand being touched modulates the primary somatosensory cortex
Schaefer, M., Heinze, H., & Rotte, M. (2005) · Neuroreport · doi:10.1097/00001756-200507130-00014 · Cited by 46
“[5] suggested that several visuotactile representations might be stored concurrently.”
BackgroundScandola, M., Aglioti, S. M., Bonente, C., Avesani, R., & Moro, V. (2016) · Scientific Reports · doi:10.1038/srep24126 · Cited by 45
Visuo-tactile integration and body ownership during self-generated action
Rognini, G., Sengül, A., Aspell, J. E., Salomon, R., Bleuler, H., & Blanke, O. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12128 · Cited by 46
Vestibular modulation of peripersonal space boundaries
Pfeiffer, C., Noel, J., Serino, A., & Blanke, O. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.13872 · Cited by 45
Kaas, J. H. (2012) · Elsevier eBooks · doi:10.1016/b978-0-12-374236-0.10030-6 · Cited by 48
Povinelli, D. J., Reaux, J. E., & Frey, S. H. (2009) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2009.09.010 · Cited by 44
fMRI Investigations of Reaching and Ego Space in Human Superior Parieto-Occipital Cortex
(2008) · Psychology Press eBooks · doi:10.4324/9780203809891-13 · Cited by 46
HandMorph: a Passive Exoskeleton that Miniaturizes Grasp
Nishida, J., Matsuda, S., Matsui, H., Teng, S.-Y., Liu, Z., Suzuki, K., & Lopes, P. (2020) · ACM Symposium on User Interface Software and Technology (UIST) · doi:10.1145/3379337.3415875 · Cited by 43
Berti, A., & Rizzolatti, G. (2002) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198508335.003.0008 · Cited by 43
Dominici, N., Daprati, E., Nico, D., Cappellini, G., Ivanenko, Y. P., & Lacquaniti, F. (2008) · Journal of Neurophysiology · doi:10.1152/jn.91165.2008 · Cited by 50
Metadata
- Authors
- lriki, A., Tanaka, M., & Iwamura, Y.
- Affiliations
- Toho University (JP)
- Venue
- NeuroReport
- Published
- 1996-10
- Volume
- 7
- Issue
- 14
- Pages
- 2325-2330
- ISSN
- 0959-4965 (ISSN-L)
- OpenAlex
- W2119233587
- Cited by
- 1,274
- References
- 0
- Citations by year
- 2026: 32 · 2025: 30 · 2024: 30 · 2023: 49 · 2022: 57 · 2021: 58 · 2020: 39 · 2019: 49 · 2018: 58 · 2017: 53 · 2016: 40 · 2015: 51 · 2014: 63 · 2013: 58 · 2012: 53
- FWCI
- 3.68
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroreport (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Life Sciences › Neuroscience › Cognitive Neuroscience › Tactile and Sensory Interactions
- Life Sciences › Neuroscience › Cognitive Neuroscience › Embodied and Extended Cognition
- Keywords
- body schema, tool use, bimodal neurons, somatosensory cortex, visual receptive fields, perceptual assimilation, macaque, neural coding
- MeSH terms
- Animals, Body Image, Macaca, Psychomotor Performance, Spatial Behavior, Visual Perception
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