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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Additional regions encode diverse information related to one's own body or the body of others, as well as their spatial position, visual and auditory space representation and movement detection, and emotional and behavioral relevance of stimuli.
“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
Tool use may cause changes in visuo-tactile integration and in the receptive fields of visuo-tactile cells in the parietal cortex, such that peripersonal space appears to extend from the hand to the tool.
“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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“In particular, they describe bimodal neurons, in the medial anterior intraparietal sulcus and in the post-central gyrus, whose visual receptive fields expand following tool use training so as to encompass the tool in addition to the hand or arm (Iriki et al., 1996; Maravita and Iriki, 2004).”
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“Irikis’ findings in the monkey (Iriki et al. 1996), showing enlarged visual RFs of bimodal neurons in the parietal cortex after training with a rake, as well as humans tool-use studies showing changes of multisensory interactions in the peripersonal space of both healthy subjects and neurological…”
BackgroundInfluentialTool-use reshapes the boundaries of body and peripersonal space representations
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“Indeed, single cell recordings from the inferior parietal lobule of the macaque brain showed that the extent of the peripersonal space can be modified by tool use (Iriki et al. 1996).”
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BackgroundKeeping the world a constant size: object constancy in human touch
Taylor-Clarke, M., Jacobsen, P. C., & Haggard, P. (2004) · Nature Neuroscience · doi:10.1038/nn1199 · Cited by 244 · see citing works
Body Schema in Robotics: A Review
Hoffmann, M., Marques, H. G., Arieta, A. H., Sumioka, H., Lungarella, M., & Pfeifer, R. (2010) · IEEE Transactions on Autonomous Mental Development · doi:10.1109/tamd.2010.2086454 · Cited by 242 · see citing works
“Maravita and Iriki [27] investigated the integration of a tool into one’s body schema in a macaque monkey that was retrieving food with the help of a rake.”
MethodEvolving intentions for social interaction: from entrainment to joint action
Knoblich, G., & Sebanz, N. (2008) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2008.0006 · Cited by 244 · see citing works
Shaping multisensory action–space with tools: evidence from patients with cross-modal extinction
Farnè, A., Iriki, A., & Làdavas, E. (2005) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2004.11.010 · Cited by 235 · see citing works
“This finding is also consistent with the activity of ‘distal type’ neurons previously reported ( Iriki et al., 1996 ), whose visual receptive fields specifically extended along the axis of the tool used by the monkey.”
BackgroundMethodResultInfluentialde Vignemont, F., & Iannetti, G. D. (2015) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2014.11.018 · Cited by 238 · see citing works
Visuo-tactile cross-modal associations in cortical somatosensory cells
Zhou, Y., & Fuster, J. M. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.17.9777 · Cited by 233 · see citing works
Left and right hand recognition in upper limb amputees
Nico, D. (2003) · Brain · doi:10.1093/brain/awh006 · Cited by 230 · see citing works
“This result would be in close agreement with studies on monkeys which showed that tools can become part of the body, being included in its representation (Iriki et al., 1996, 2001).”
BackgroundResultSelf-images in the video monitor coded by monkey intraparietal neurons
Iriki, A., Tanaka, M., Obayashi, S., & Iwamura, Y. (2001) · Neuroscience Research · doi:10.1016/s0168-0102(01)00225-5 · Cited by 229 · see citing works
“Tool-use in the monitor and modification of coding of the hand image along the tool As earlier reported (Iriki et al., 1996), the visual RF of these bimodal neurons extend to include a hand-held tool used to retrieve distant food.”
InfluentialSelf-citationThe bodily self as power for action
Gallese, V., & Sinigaglia, C. (2009) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2009.09.038 · Cited by 227 · see citing works
Decoding the neural mechanisms of human tool use
Gallivan, J. P., McLean, D. A., Valyear, K. F., & Culham, J. C. (2013) · eLife · doi:10.7554/elife.00425 · Cited by 225 · see citing works
“, 2009, 2012), and macaque monkey neurophysiology (Iriki et al., 1996) suggest that following training, a tool may actually become incorporated into the body schema of the actor and coded as an extension of the hand/limb.”
BackgroundDifferential Dynamic Plasticity of A1 Receptive Fields during Multiple Spectral Tasks
Fritz, J. B., Elhilali, M., & Shamma, S. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1318-05.2005 · Cited by 226 · see citing works
“The combination of such taskdependent, adaptive neural plasticity and the resultant possibility that neurons and networks may multiplex for different perceptual tasks may be an important mechanism in A1 underlying active listening and a general principle of cortical processing during attentive behavior in other sensor…”
BackgroundSelective visuo‐haptic processing of shape and texture
Stilla, R. F., & Sathian, K. (2007) · Human Brain Mapping · doi:10.1002/hbm.20456 · Cited by 228 · see citing works
“Visual responsiveness has not previously been reported in the human PCS, although some of the multisensory neurons described in the IPS of monkeys were on the anterior bank of this sulcus (Iriki et al., 1996) and thus may have been in area 2 (Iwamura, 1998).”
BackgroundMaravita, A., Husain, M., Clarke, K., & Driver, J. (2001) · Neuropsychologia · doi:10.1016/s0028-3932(00)00150-0 · Cited by 222 · see citing works
“Increased extinction when wielding the stick could be predicted on the basis of recent physiological results from multimodal neurons in the intraparietal sulcus [13].”
BackgroundWhat is an affordance? 40 years later
Osiurak, F., Rossetti, Y., & Badets, A. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.04.014 · Cited by 226 · see citing works
Central mechanisms in phantom limb perception: The past, present and future
Giummarra, M. J., Gibson, S. J., Georgiou‐Karistianis, N., & Bradshaw, J. L. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.01.009 · Cited by 222 · see citing works
Mechanisms underlying embodiment, disembodiment and loss of embodiment
Giummarra, M. J., Gibson, S. J., Georgiou‐Karistianis, N., & Bradshaw, J. L. (2007) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.07.001 · Cited by 221 · see citing works
Functional Brain Mapping of Monkey Tool Use
Obayashi, S., Suhara, T., Kawabe, K., Okauchi, T., Maeda, J., Akine, Y., Onoe, H., & Iriki, A. (2001) · NeuroImage · doi:10.1006/nimg.2001.0878 · Cited by 223 · see citing works
An action field theory of peripersonal space
Bufacchi, R. J., & Iannetti, G. D. (2018) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2018.09.004 · Cited by 221 · see citing works
“Data reproduced, with permission, from [11,13,14,25,38,54,89].”
BackgroundGentile, G., Guterstam, A., Brozzoli, C., & Ehrsson, H. H. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.1363-13.2013 · Cited by 221 · see citing works
“…between anterior and medial portions of the intraparietal cortex (Grefkes and Fink, 2005) and posterior superior parietal (Mountcastle et al., 1975; Iriki et al., 1996; Graziano et al., 2000), inferior parietal (Hyvärinen and Poranen, 1974; Luppino and Rizzolatti, 2000), and premotor (Rizzolatti…”
BackgroundGallivan, J. P., Cavina‐Pratesi, C., & Culham, J. C. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0377-09.2009 · Cited by 210 · see citing works
Shared mapping of own and others' bodies in visuotactile bimodal area of monkey parietal cortex
Ishida, H., Nakajima, K., Inase, M., & Murata, A. (2010) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21185 · Cited by 212 · see citing works
“Physiological studies of visuotactile body representation have demonstrated that bimodal neurons in area 5 and PEa are related to coding of the egocentric reference frame and may also contribute to monitoring of one’s own body (Graziano, Cooke, & Taylor, 2000; Obayashi, Tanaka, & Iriki, 2000; Iriki, Tanaka, & Iwamura,…”
BackgroundGrivaz, P., Blanke, O., & Serino, A. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2016.12.052 · Cited by 203 · see citing works
“…superior parietal cluster is likely to be the human homologue of monkey area 5 (as well as adjacent area 2) where multisensory and sensorimotor neurons have been extensively described by using invasive electrophysiological recordings (Graziano et al., 2000; Iriki et al., 1996; Sakata et al., 1973).”
Tool use, communicative gesture and cerebral asymmetries in the modern human brain
Frey, S. H. (2008) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2008.0008 · Cited by 206 · see citing works
- 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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