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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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InfluentialArchitectonic mapping of somatosensory areas involved in skilled forelimb movements and tool use
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“The neurophysiological analysis of tool-use in Japanese macaques has shown that the acquisition of these skills is accompanied by long-lasting modifications of their body schema (Iriki et al. 1996; Maravita and Iriki 2004).”
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“…in premotor and parietal cortical areas are responsive to nearby stimuli relative to a particular body surface, anticipate approaching stimuli, and partially relocate their receptive fields during tool usage (Canzoneri et al. 2013; Fogassi et al. 1996; Holmes and Spence 2004; Iriki et al. 1996).”
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“For example. they are expanded after active tool use, which allows interactions with non-reachable, far objects, both in monkeys [6] and humans [7], and are modulated by positive or negative social interactions [8].”
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“For instance, Iriki, Tanaka, and Iwamura (1996) found that macaque monkeys who were allowed to use a handheld rake to reach food pellets showed an extension of their receptive fields for certain neurons ordinarily receptive to visual input from the monkey’s hand alone.”
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“Receptive fields of neurons coding events near the hand expanded to include the entire range of the rake (Iriki et al., 1996), indicating that the tool was included in the body schema (Maravita & Iriki, 2004).”
BackgroundAssociating and reshaping of whole body motions for object manipulation
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“Recent neuroscience research [10] [ 11 ] revealed that, when primates use a tool to reach for a distant object, the extended motor capability is followed by changes in specific neural networks that hold an updated map of body shape and posture.”
BackgroundTowards mastery of complex visuo-motor transformations
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“This lead to the finding that learning to use a tool extends the body schema to incorporate the tool (Iriki et al. 1996).”
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“In a study bearing on the neural correlates of this phenomenology, monkeys were trained to make use of a rake to drag back towards them with one hand pellets of food to be grabbed with the other ( Iriki, Tanaka, and Iwamura 1996 ).”
MethodTool manipulation by rats (Rattus norvegicus) according to the position of food
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Tool Use Unravels Body Morphology Representation in the Brain
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BackgroundGirondini, M., Montanaro, M., & Gallace, A. (2024) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2024.1354633 · Cited by 8
Skillful action in peripersonal space
Jackson, G. B. (2013) · Phenomenology and the Cognitive Sciences · doi:10.1007/s11097-013-9301-7 · Cited by 7
“15 Many early studies on peripersonal space and tool use were conducted on monkeys, using PET and fMRI scans (Rizzolatti et al. 1981; Rizzolatti et al. 1983; Iriki et al. 1996).”
BackgroundMethodThe cognitive and neural bases of human tool use
Osiurak, F., & Massen, C. (2014) · Frontiers in Psychology · doi:10.3389/fpsyg.2014.01107 · Cited by 7
“Likewise, body representations can be modified when using a tool so that the tool is incorporated and becomes part of our body (Iriki et al., 1996; Cardinalli et al., 2009).”
BackgroundArbib, M. A. (2012) · Behavioral and Brain Sciences · doi:10.1017/s0140525x11002123 · Cited by 6
Piovesan, É. J., Lange, M. C., Kowacs, P. A., Pacheco, C., & Werneck, L. C. (2001) · Arquivos de Neuro-Psiquiatria · doi:10.1590/s0004-282x2001000500009 · Cited by 7
Dynamic Manipulation Generates Touch Information That Can Modify Vision
Bruggeman, H., Kliman-Silver, C. E., Domini, F., et al. (2013) · Psychological Science · doi:10.1177/0956797612457398 · Cited by 7
Learning Visuomotor Transformations and End Effector Appearance by Local Visual Consistency
Zhou, T., & Shi, B. E. (2015) · IEEE Transactions on Cognitive and Developmental Systems · doi:10.1109/tamd.2015.2502758 · Cited by 7
“Changes in the visual receptive fields of macaque bimodal visual-tactile neurons after tool use demonstrate it at the neuronal level [14], [15].”
BackgroundResultParisi, F. (2018) · Phenomenology and the Cognitive Sciences · doi:10.1007/s11097-018-9599-2 · Cited by 8
Motor memories in manipulation tasks are linked to contact goals between objects
McGarity-Shipley, M. R., Heald, J. B., Ingram, J. N., Gallivan, J. P., Wolpert, D. M., & Flanagan, J. R. (2020) · Journal of Neurophysiology · doi:10.1152/jn.00252.2020 · Cited by 5
Smartphone use can modify the body schema: An ERP study based on hand mental rotation task
Liu, Q., Wu, J., Zhou, Z., & Wang, W. (2021) · Computers in Human Behavior · doi:10.1016/j.chb.2021.107134 · Cited by 8
Multisensory Perception and Bodily Self-Consciousness
Aspell, J. E., Lenggenhager, B., & Blanke, O. (2011) · Frontiers in neuroscience · doi:10.1201/9781439812174-30 · Cited by 40
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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