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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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The Remapping of Peripersonal Space in a Real but Not in a Virtual Environment
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MethodTestosterone administration in women increases the size of their peripersonal space
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BackgroundInfluentialSomatosensory association cortices
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Self-citationRobot tool behavior: a developmental approach to autonomous tool use
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MethodIntensive tool-practice and skillfulness facilitate the extension of body representations in humans
Rademaker, R. L., Wu, D.-A. J., Bloem, I. M., & Sack, A. T. (2014) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2014.01.011 · Cited by 16
“Although the monkey physiology studies found that tool integration developed after weeks of use (Iriki et al., 1996), the human behavioral studies found tool integration as soon as the tools were grasped (Cardinali et al., 2009; Carlson et al., 2010).”
InfluentialNeural changes in the primate brain correlated with the evolution of complex motor skills
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Cognitive Paleoanthropology and Technology: Toward a Parsimonious Theory (PATH)
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Disconnected hand avatar can be integrated into the peripersonal space
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14C-Deoxyglucose mapping of the monkey brain during reaching to visual targets
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Altered attention for stimuli on the hands
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“When the monkey learns to use a rake to grab items at longer distances, the receptive fields of those neurons quickly expand to include the newly reachable area (Iriki et al., 1996; Maravita & Iriki, 2004).”
Interacting hands: the role of attention for the joint Simon effect
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Quinlan, D. J., & Culham, J. C. (2015) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2015.00580 · Cited by 15
“Frontiers in Human Neuroscience | www.frontiersin.org 1 October 2015 | Volume 9 | Article 580”
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“Humans also have a capability to use new tools without the prior-knowledge as if they are part of the human bodies, known as tool-body assimilation through trial and experience [15], [26].”
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“It has been suggested that the space closely around one's body is uniquely represented, and its range can be modulated by tools (Iriki, Tanaka, & Iwamura, 1996 ; Ladavas & Serino, 2008 ; Maravita, Spence, & Driver, 2003 ).”
Cross-modal body representation based on visual attention by saliency
Hikita, M., Fuke, S., Ogino, M., & Asada, M. (2008) · IEEE/RSJ International Conference on Intelligent Robots and Systems (IROS) · doi:10.1109/iros.2008.4650948 · Cited by 16
“NEUROPHYSIOLOGICAL FINDING Iriki et al. [1] recorded the activities of some neurons in the intraparietal cortex before and after the Japanese macaque monkeys were trained to use a tool.”
BackgroundMethodOn the Significance of Bodily Awareness for Bodily Action: Figure 1.
Wong, H. Y. (2015) · The Philosophical Quarterly · doi:10.1093/pq/pqv007 · Cited by 15
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Parieto-frontal gradients and domains underlying eye and hand operations in the action space
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“It has been suggested that tool use extends the visuotactile representation of peripersonal space (Berti and Frassinetti 2000; Farne et al. 2005; Iriki et al. 1996; Maravita et al. 2001).”
BackgroundMethodReshaping the peripersonal space in virtual reality
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Alpha oscillations reflect similar mapping mechanisms for localizing touch on hands and tools
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A brief review of the role of training in near-tool effects
Brown, L. E., & Goodale, M. A. (2013) · Frontiers in Psychology · doi:10.3389/fpsyg.2013.00576 · Cited by 17
“In short, active use of the hand (Obayashi et al., 2000) or a hand-held tool (Iriki et al., 1996; Maravita and Iriki, 2004) may change how the CNS represents the space surrounding the hand or tool.”
InfluentialBaugh, L. A., Hoe, E., & Flanagan, J. R. (2012) · Journal of Neurophysiology · doi:10.1152/jn.00157.2012 · Cited by 14
“Specifically, the visual receptive fields of bimodal neurons within the intraparietal sulcus (IPS) have been shown to elongate from the hand along the body of a utilized tool to the tip when a monkey was trained to use a rake to retrieve food (Iriki et al. 1996).”
BackgroundResultMSI Caterpillar: An Effective Multisensory System to Evaluate Spatial Body Representation
Gori, M., Bollini, A., Maviglia, A., et al. (2019) · IEEE International Symposium on Medical Measurements and Applications (MeMeA) · doi:10.1109/memea.2019.8802133 · Cited by 14
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BackgroundEnhancing the Sense of Agency by Transitional Weight Control in Virtual Co-Embodiment
Kodama, D., Mizuho, T., Hatada, Y., Narumi, T., & Hirose, M. (2022) · Proceedings - International Symposium on Mixed and Augmented Reality, ISMAR · doi:10.1109/ismar55827.2022.00043 · Cited by 14
“For instance, Iriki et al. [42] trained macaque monkeys to retrieve distant objects by using a rake.”
MethodEtiology of phantom limb syndrome: Insights from a 3D default space consciousness model
Jerath, R., Crawford, M. W., & Jensen, M. (2015) · Medical Hypotheses · doi:10.1016/j.mehy.2015.04.025 · Cited by 14
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MethodTo the end! Distribution of attention along a tool in peri- and extrapersonal space
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BackgroundThe Body in a Multisensory World
Heed, T., & Röder, B. (2011) · Frontiers in neuroscience · doi:10.1201/b11092-35 · Cited by 18
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BackgroundMethodInfluentialOn Proprioception in Action: Multimodality versus Deafferentation
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MethodDe l'image du corps à l'image de soi
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BackgroundPhenomenal transparency, cognitive extension, and predictive processing
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“…shape and posture in the brain, the “body schema” (Berlucchi & Aglioti, 1997; Maravita & Iriki, 2004), is another example of individualization as is the phenomenon of “tool extension”, namely the changes to the body schema through the use of tools (Berti & Frassinetti, 2000; Iriki et al., 1996).”
Understanding the neural bases of bodily self-consciousness: recent achievements and main challenges
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Imitation of hand and tool actions is effector-independent
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“The consciousness to be able to move the leg might lead to an extension of the peripersonal space through multisensory integration [44].”
BackgroundEmbodied Cooperation to Promote Forgiving Interactions With Autonomous Machines
Schofield, J. S., Battraw, M. A., Parker, A. S. R., Pilarski, P. M., Sensinger, J. W., & Marasco, P. D. (2021) · Frontiers in Neurorobotics · doi:10.3389/fnbot.2021.661603 · Cited by 13
“Similar effects are observed in numerous tools spanning the complexities of a rake through an automobile (Iriki et al., 1996; Sposito et al., 2012; Moeller et al., 2016).”
BackgroundOwn body perception based on visuomotor correlation
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BackgroundMethodResultInfluentialHand-use and tool-use in grasping control
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“Procedure After a verbal “Go” cue from the experimenter, the participants started reaching at own timing with their fingers 1 3 or tips of the tool closed.”
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Brain-Inspired Coding of Robot Body Schema Through Visuo-Motor Integration of Touched Events
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“, 2016) as well as for the purpose of other cognitive tasks such as tool-use and body extension (Iriki et al., 1996; Murata et al., 2016), perspective-taking to have person-centered viewpoints (Iriki et al.”
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“In this perspective, the studies by Iriki in the macaque monkeys are particularly interesting as they showed evidences of a dynamical readaptation of the body schema with respect to the ongoing situation [5].”
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“Maravita & Iriki (2004) have also noted that the phenomenon of expansion of the visual RF observed by Iriki et al. (1996) concerned neurons with RFs on the arm/hand, but not with RFs on the fingers.”
BackgroundResultInfluentialCrossmodal and Multisensory Interactions Between Vision and Touch
Lacey, S., & Sathian, K. (2015) · Atlantis Press eBooks · doi:10.2991/978-94-6239-133-8_25 · Cited by 12
Investigating multisensory spatial cognition through the phenomenon of extinction
Farnè, A., Brozzoli, C., Làdavas, E., & Ro, T. (1993) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199231447.003.0009 · Cited by 14
“The same visual RF shrunk following passive toolwielding , recorded immediately after tool-use, thus showing a tool-use-dependent extension of the visual–tactile space immediately surrounding the hand (Iriki et al., 1996).”
BackgroundMethodResultInfluentialBody Definition Based on Visuomotor Correlation
Saegusa, R., Giorgio Metta, B., & Sandini, G. (2011) · IEEE Transactions on Industrial Electronics · doi:10.1109/tie.2011.2157280 · Cited by 11
Cognitive representations of tool-use interactions
Massen, C. (2013) · New Ideas in Psychology · doi:10.1016/j.newideapsych.2012.12.002 · Cited by 12
Incremental Development of Multiple Tool Models for Robotic Reaching Through Autonomous Exploration
Jamone, L., Damas, B., Endo, N., et al. (2012) · Paladyn Journal of Behavioral Robotics · doi:10.2478/s13230-013-0102-z · Cited by 12
“Taking direct inspiration from the studies of Iriki about neural adaptation in monkeys [15], the work in [22] proposes a visual attention module that can extend the robot body representation through Hebbian learning when a tool is being used; simulation results are provided.”
MethodRobotic grasping and manipulation through human visuomotor learning
Moore, B., & Öztop, E. (2011) · Robotics and Autonomous Systems · doi:10.1016/j.robot.2011.09.002 · Cited by 12
A behavioural experiment in virtual reality to verify the role of action function in space coding
Gamberini, L., Carlesso, C., Seraglia, B., & Craighero, L. (2013) · Visual Cognition · doi:10.1080/13506285.2013.840348 · Cited by 11
“Iriki, Tanaka, and Iwamura (1996) trained macaques to retrieve distant objects using a rake and they recorded neurons in the intraparietal cortex responding to both somatosensory and visual stimulation.”
BackgroundUgolini, G., Prevosto, V., & Graf, W. M. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14426 · Cited by 11
“, 2009, 2010, 2011), neurons at the rostral MIP injection site were characterized by prominent vestibular responses, sensitivity to somatosensory stimulation on the arms and hands (Klam & Graf, 2003, 2006) and bimodal somatosensory/visual responses (e.g., Colby & Duhamel 1991; Iriki et al., 1996; Graziano et al., 2000…”
BackgroundKirsh, D. (2019) · Oxford University Press eBooks · doi:10.1093/oso/9780190662813.003.0011 · Cited by 13
Functional organization of monkey brain for abstract operation.
Obayashi, S., Matsumoto, R., Suhara, T., Nagai, Y., Iriki, A., & Maeda, J. (2007) · Cortex; a journal devoted to the study of the nervous system and behavior · doi:10.1016/s0010-9452(08)70464-7 · Cited by 13
An action perspective on tool use and its development
Bongers, R. M. (2001) · Radboud Repository (Radboud University) · Cited by 12
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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