To Watch is to Work: a Review of NeuroImaging Data on Tool Use Observation Network

Abstract

Since the discovery of mirror neurons in the 1990s, many neuroimaging studies have tackled the issue of action observation with the aim of unravelling a putative homolog human system. However, these studies do not distinguish between non-tool-use versus tool-use actions, implying that a common brain network is systematically involved in the observation of any action. Here we provide evidence for a brain network dedicated to tool-use action observation, called the tool-use observation network, mostly situated in the left hemisphere, and distinct from the non-tool-use action observation network. Areas specific for tool-use action observation are the left cytoarchitectonic area PF within the left inferior parietal lobe and the left inferior frontal gyrus. The neural correlates associated with the observation of tool-use reported here offer new insights into the neurocognitive bases of action observation and tool use, as well as addressing more fundamental issues on the origins of specifically human phenomena such as cumulative technological evolution.

This is a preview of subscription content, access via your institution.

We’re sorry, something doesn't seem to be working properly.

Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Data Availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

Notes

  1. 1.

    The term network used here must be understood as a collection of brain areas, with no assessment of the structural or functional connectivity that could exist between these areas.

References

  1. Abdollahi, R. O., Kolster, H., Glasser, M. F., Robinson, E. C., Coalson, T. S., Dierker, D., … Orban, G. A. (2014). Correspondences between retinotopic areas and myelin maps in human visual cortex. NeuroImage. https://doi.org/10.1016/j.neuroimage.2014.06.042

    PubMed  PubMed Central  Article  Google Scholar 

  2. Binkofski, F., Buccino, G., Zilles, K., & Fink, G. (2004). Supramodal representation of objects and actions in the human inferior temporal and ventral premotor cortex. Cortex, 40(1), 159–161.

    PubMed  Article  PubMed Central  Google Scholar 

  3. Boronat, C. B., Buxbaum, L. J., Coslett, H. B., Tang, K., Saffran, E. M., Kimberg, D. Y., & Detre, J. A. (2005). Distinctions between manipulation and function knowledge of objects: Evidence from functional magnetic resonance imaging. Cognitive Brain Research. https://doi.org/10.1016/j.cogbrainres.2004.11.001

    PubMed  Article  PubMed Central  Google Scholar 

  4. Bortoletto, M., & Cunnington, R. (2010). Motor timing and motor sequencing contribute differently to the preparation for voluntary movement. NeuroImage. https://doi.org/10.1016/j.neuroimage.2009.11.048

    PubMed  Article  PubMed Central  Google Scholar 

  5. Boyd, R., & Richerson, P. J. (1996). Why culture is common, but cultural evolution is rare. In W. G. Runciman, J. M. Smith, & R. I. M. Dunbar (Eds.), Proceedings of The British Academy, Vol. 88. Evolution of social behaviour patterns in primates and man (pp. 77-93). New York, NY, US: Oxford University Press.

  6. Brass, M., & Heyes, C. (2005). Imitation: Is cognitive neuroscience solving the correspondence problem? Trends in Cognitive Sciences. https://doi.org/10.1016/j.tics.2005.08.007

    PubMed  Article  PubMed Central  Google Scholar 

  7. Buccino, G., Binkofski, F., Fink, G. R., Fadiga, L., Fogassi, L., Gallese, V., … Freund, H. J. (2001). Action observation activates premotor and parietal areas in a somatotopic manner: An fMRI study. European Journal of Neuroscience, 13(2), 400–404. https://doi.org/10.1046/j.1460-9568.2001.01385.x

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. Buxbaum, L. J. (2001). Ideomotor apraxia: A call to action. Neurocase, 7(6), 445–458.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  9. Buxbaum, L. J. (2017). Learning, remembering, and predicting how to use tools: Distributed neurocognitive mechanisms: Comment on osiurak and badets (2016). Psychological Review. https://doi.org/10.1037/rev0000051

    PubMed  PubMed Central  Article  Google Scholar 

  10. Buxbaum, L. J., Giovannetti, T., & Libon, D. (2000). The role of the dynamic body schema in praxis: Evidence from primary progressive apraxia. Brain and Cognition. https://doi.org/10.1006/brcg.2000.1227

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  11. Buxbaum, L. J., & Saffran, E. M. (2002). Knowledge of object manipulation and object function: Dissociations in apraxic and nonapraxic subjects. Brain and Language. https://doi.org/10.1016/S0093-934X(02)00014-7

    PubMed  Article  PubMed Central  Google Scholar 

  12. Caspers, S., Geyer, S., Schleicher, A., Mohlberg, H., Amunts, K., & Zilles, K. (2006). The human inferior parietal cortex: Cytoarchitectonic parcellation and interindividual variability. NeuroImage. https://doi.org/10.1016/j.neuroimage.2006.06.054

    PubMed  Article  PubMed Central  Google Scholar 

  13. Caspers, S., Zilles, K., Laird, A. R., & Eickhoff, S. B. (2010). ALE meta-analysis of action observation and imitation in the human brain. NeuroImage, 50(3), 1148–1167. https://doi.org/10.1016/j.neuroimage.2009.12.112

    Article  PubMed  PubMed Central  Google Scholar 

  14. Chao, L. L., & Martin, A. (2000). Representation of manipulable man-made objects in the dorsal stream. NeuroImage. https://doi.org/10.1006/nimg.2000.0635

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  15. Chen, Q., Garcea, F. E., Jacobs, R. A., & Mahon, B. Z. (2018). Abstract representations of object-directed action in the left inferior parietal lobule. Cerebral Cortex. https://doi.org/10.1093/cercor/bhx120

    Article  Google Scholar 

  16. Chong, T. T.-J., Williams, M. A., Cunnington, R., & Mattingley, J. B. (2008). Selective attention modulates inferior frontal gyrus activity during action observation. NeuroImage, 40(1), 298–307. https://doi.org/10.1016/j.neuroimage.2007.11.030

    Article  PubMed  PubMed Central  Google Scholar 

  17. Creem-Regehr, S. H., & Lee, J. N. (2005). Neural representations of graspable objects: Are tools special? Cognitive Brain Research. https://doi.org/10.1016/j.cogbrainres.2004.10.006

    PubMed  Article  PubMed Central  Google Scholar 

  18. Cross, E. S., Kraemer, D. J. M., Hamilton, A. F. D. C., Kelley, W. M., & Grafton, S. T. (2009). Sensitivity of the action observation network to physical and observational learning. Cerebral Cortex, 19(2), 315–326. https://doi.org/10.1093/cercor/bhn083

    Article  PubMed  PubMed Central  Google Scholar 

  19. Cubelli, R., Marchetti, C., Boscolo, G., & Della Sala, S. (2000). Cognition in action: Testing a model of limb apraxia. Brain and Cognition. https://doi.org/10.1006/brcg.2000.1226

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  20. Culham, J. C., Brandt, S. A., Cavanagh, P., Kanwisher, N. G., Dale, A. M., & Tootell, R. B. (1998). Cortical fMRI activation produced by attentive tracking of moving targets. Journal of Neurophysiology, 80(5), 2657–2670 9819271.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  21. Daprati, E., & Sirigu, A. (2006). How we interact with objects: Learning from brain lesions. Trends in Cognitive Sciences. https://doi.org/10.1016/j.tics.2006.04.005

    PubMed  Article  PubMed Central  Google Scholar 

  22. De Renzi, E. (1989). Apraxia. In F. Boller & J. Grafman (Eds.), Handbook of neuropsychology (vol. 2, pp. 245–263). Amsterdam: Elsevier.

    Google Scholar 

  23. Decety, J., & Grezes, J. (1999). Neural mechanisms subserving the perception of human actions. Trends in Cognitive Sciences, 3(5), 172–178.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  24. Dinstein, I., Gardner, J. L., Jazayeri, M., & Heeger, D. J. (2008). Executed and observed movements have different distributed representations in human aIPS. Journal of Neuroscience. https://doi.org/10.1523/JNEUROSCI.3585-08.2008

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  25. Dinstein, I., Hasson, U., Rubin, N., & Heeger, D. J. (2007). Brain areas selective for both observed and executed movements. Journal of Neurophysiology, 98(3), 1415–1427. https://doi.org/10.1152/jn.00238.2007

    Article  PubMed  PubMed Central  Google Scholar 

  26. Eickhoff, S. B., Bzdok, D., Laird, A. R., Kurth, F., & Fox, P. T. (2012). Activation likelihood estimation meta-analysis revisited. Neuroimage, 59(3), 2349–2361.

    PubMed  PubMed Central  Article  Google Scholar 

  27. Eickhoff, S. B., Laird, A. R., Fox, P. M., Lancaster, J. L., & Fox, P. T. (2017). Implementation errors in the GingerALE software: Description and recommendations. Human Brain Mapping, 38(1), 7–11. https://doi.org/10.1002/hbm.23342

    Article  PubMed  PubMed Central  Google Scholar 

  28. Evans, C., Edwards, M. G., Taylor, L. J., & Ietswaart, M. (2016). Perceptual decisions regarding object manipulation are selectively impaired in apraxia or when tDCS is applied over the left IPL. Neuropsychologia. https://doi.org/10.1016/j.neuropsychologia.2016.04.020

    PubMed  Article  PubMed Central  Google Scholar 

  29. Fadiga, L., Craighero, L., & Olivier, E. (2005). Human motor cortex excitability during the perception of others’ action. Current Opinion in Neurobiology. https://doi.org/10.1016/j.conb.2005.03.013

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  30. Fadiga, L., Fogassi, L., Pavesi, G., & Rizzolatti, G. (1995). Motor facilitation during action observation: A magnetic stimulation study. Journal of Neurophysiology, 73(6), 2608–2611 https://doi.org/10.1152/jn.1995.73.6.2608

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. Gallese, V., Fadiga, L., Fogassi, L., & Rizzolatti, G. (1996). Action recognition in the premotor cortex. Brain, 119(2), 593–609. https://doi.org/10.1093/brain/119.2.593

    Article  PubMed  PubMed Central  Google Scholar 

  32. Gallese, V., & Goldman, A. (1998). Mirror neurons and the mind-reading. Trens in Cognitive Sciences, 2(12), 493–501. https://doi.org/10.1016/S1364-6613(98)01262-5

    CAS  Article  Google Scholar 

  33. Garcea, F. E., Dombovy, M., & Mahon, B. Z. (2013). Preserved tool knowledge in the context of impaired action knowledge: Implications for models of semantic memory. Frontiers in Human Neuroscience. https://doi.org/10.3389/fnhum.2013.00120

  34. Georgieva, S., Peeters, R., Kolster, H., Todd, J. T., & Orban, G. A. (2009). The processing of three-dimensional shape from disparity in the human brain. Journal of Neuroscience. https://doi.org/10.1523/JNEUROSCI.4753-08.2009

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  35. Goghari, V. M., & MacDonald, A. W. (2009). The neural basis of cognitive control: Response selection and inhibition. Brain and Cognition. https://doi.org/10.1016/j.bandc.2009.04.004

    PubMed  PubMed Central  Article  Google Scholar 

  36. Goldenberg, G., & Spatt, J. (2009). The neural basis of tool use. Brain, 132(Pt 6), 1645–1655. https://doi.org/10.1093/brain/awp080

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  37. Goldenberg, G, & Hagmann, S. (1998). Tool use and mechanical problem solving in apraxia. Neuropsychologia.

  38. Goldenberg, G. (2013). Apraxia - the cognitive side of motor control. Cortex. https://doi.org/10.1016/j.cortex.2013.07.016

    PubMed  Article  PubMed Central  Google Scholar 

  39. Gonzalez Rothi, L. J., Ochipa, C., & Heilman, K. M. (1991). A cognitive neuropsychological model of limb praxis. Cognitive Neuropsychology, 8(6), 443–458. https://doi.org/10.1080/02643299108253382

    Article  Google Scholar 

  40. Grafton, S., Arbib, M., Fadiga, L., & Rizzolatti, G. (1996). Localization of grasp representations in humans by positron emission tomography. Experimental Brain Research. https://doi.org/10.1007/BF00227183

  41. Greenfield, P. M. (1991). Language, tools and brain: The ontogeny and phylogeny of hierarchically organized sequential behavior. Behavioral and Brain Sciences. https://doi.org/10.1017/S0140525X00071235

    Article  Google Scholar 

  42. Halsband, U., Schmitt, J., Weyers, M., Binkofski, F., Grützner, G., & Freund, H. J. (2001). Recognition and imitation of pantomimed motor acts after unilateral parietal and premotor lesions: A perspective on apraxia. Neuropsychologia. https://doi.org/10.1016/S0028-3932(00)00088-9

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  43. Hamilton, A., & Grafton, S. T. (2006). Goal representation in human anterior intraparietal sulcus. Journal of Neuroscience. https://doi.org/10.1523/jneurosci.4551-05.2006

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  44. Hartmann, K., Goldenberg, G., Daumüller, M., & Hermsdörfer, J. (2005). It takes the whole brain to make a cup of coffee: The neuropsychology of naturalistic actions involving technical devices. Neuropsychologia. https://doi.org/10.1016/j.neuropsychologia.2004.07.015

    PubMed  Article  PubMed Central  Google Scholar 

  45. Heilman, K. M., Rothi, L. J., & Valenstein, E. (1982). Two forms of ideomotor apraxia. Neurology. https://doi.org/10.1212/WNL.32.4.342

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  46. Hickok, G. (2009). Eight problems for the mirror neuron theory of action understanding in monkeys and humans. Journal of Cognitive Neuroscience. https://doi.org/10.1162/jocn.2009.21189

    PubMed  PubMed Central  Article  Google Scholar 

  47. Hickok, G. (2014). The myth of mirror neurons: The real neuroscience of communication and cognition. New-York: Norton.

    Google Scholar 

  48. Higuchi, S., Chaminade, T., Imamizu, H., & Kawato, M. (2009). Shared neural correlates for language and tool use in Broca’s area. NeuroReport. https://doi.org/10.1097/WNR.0b013e3283315570

    PubMed  Article  PubMed Central  Google Scholar 

  49. Iacoboni, M. (2009). Imitation, empathy, and mirror neurons. Annual Review of Psychology, 60(1), 653–670. https://doi.org/10.1146/annurev.psych.60.110707.163604

    Article  PubMed  PubMed Central  Google Scholar 

  50. Ishibashi, R., Lambon Ralph, M. A., Saito, S., & Pobric, G. (2011). Different roles of lateral anterior temporal lobe and inferior parietal lobule in coding function and manipulation tool knowledge: Evidence from an rTMS study. Neuropsychologia. https://doi.org/10.1016/j.neuropsychologia.2011.01.004

    PubMed  Article  PubMed Central  Google Scholar 

  51. Ishibashi, R., Pobric, G., Saito, S., & Lambon Ralph, M. A. (2016). The neural network for tool-related cognition: An activation likelihood estimation meta-analysis of 70 neuroimaging contrasts. Cognitive Neuropsychology. https://doi.org/10.1080/02643294.2016.1188798

    PubMed  PubMed Central  Article  Google Scholar 

  52. Jacob, P., & Jeannerod, M. (2005). The motor theory of social cognition: A critique. Trends in Cognitive Sciences. https://doi.org/10.1016/j.tics.2004.11.003

    PubMed  Article  PubMed Central  Google Scholar 

  53. Jastorff, J., Begliomini, C., Fabbri-Destro, M., Rizzolatti, G., & Orban, G. A. (2010). Coding observed motor acts: Different organizational principles in the parietal and premotor cortex of humans. Journal of Neurophysiology. https://doi.org/10.1152/jn.00254.2010

    PubMed  Article  PubMed Central  Google Scholar 

  54. Jeannerod, M. (1994). The representing brain: Neural correlates of motor intention and imagery. Behavioral and Brain Sciences, 17(02), 187. https://doi.org/10.1017/S0140525X00034026

    Article  Google Scholar 

  55. Johnson-Frey, S. H., Maloof, F. R., Newman-Norlund, R., Farrer, C., Inati, S., & Grafton, S. T. (2003). Actions or hand-object interactions? Human inferior frontal cortex and action observation. Neuron, 39(6), 1053–1058. https://doi.org/10.1016/S0896-6273(03)00524-5

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  56. Johnson-Frey, S. H., Newman-Norlund, R., & Grafton, S. T. (2005). A distributed left hemisphere network active during planning of everyday tool use skills. Cerebral Cortex, 15(6), 681–695.

    PubMed  Article  PubMed Central  Google Scholar 

  57. Kalénine, S., Shapiro, A. D., & Buxbaum, L. J. (2013). Dissociations of action means and outcome processing in left-hemisphere stroke. Neuropsychologia. https://doi.org/10.1016/j.neuropsychologia.2013.03.017

    PubMed  PubMed Central  Article  Google Scholar 

  58. Kalénine, S., Buxbaum, L. J., & Coslett, H. B. (2010). Critical brain regions for action recognition: Lesion symptom mapping in left hemisphere stroke. Brain. https://doi.org/10.1093/brain/awq210

    PubMed  PubMed Central  Article  Google Scholar 

  59. Kilner, J. M. (2009). Dissociable functional roles of the human action-observation network (commentary on E. S. Cross et al.). European Journal of Neuroscience. https://doi.org/10.1111/j.1460-9568.2009.06958.x

    PubMed  Article  PubMed Central  Google Scholar 

  60. Lancaster, J. L., Tordesillas-Gutierrez, D., Martinez, M., Salinas, F., Evans, A., Zilles, K., … Fox, P. T. (2007). Bias between MNI and Talairach coordinates analyzed using the ICBM-152 brain template. Human Brain Mapping, 28(11), 1194–1205.

    PubMed  PubMed Central  Article  Google Scholar 

  61. Lesourd, M., Osiurak, F., Navarro, J., & Reynaud, E. (2017). Involvement of the left supramarginal gyrus in manipulation judgment tasks: Contributions to theories of tool use. Journal of the International Neuropsychological Society, 1–7. https://doi.org/10.1017/S1355617717000455

    PubMed  Article  PubMed Central  Google Scholar 

  62. Lingnau, A., Gesierich, B., & Caramazza, A. (2009). Asymmetric fMRI adaptation reveals no evidence for mirror neurons in humans. Proceedings of the National Academy of Sciences. https://doi.org/10.1073/pnas.0902262106

    CAS  Article  Google Scholar 

  63. Mahon, B. Z., & Caramazza, A. (2005). The orchestration of the sensory-motor systems: Clues from neuropsychology. Cognitive Neuropsychology. https://doi.org/10.1080/02643290442000446

    PubMed  Article  PubMed Central  Google Scholar 

  64. Mahon, B. Z., & Caramazza, A. (2008). A critical look at the embodied cognition hypothesis and a new proposal for grounding conceptual content. Journal of Physiology Paris. https://doi.org/10.1016/j.jphysparis.2008.03.004

    Article  Google Scholar 

  65. Meltzoff, A., & Moore, M. (1977). Imitation of facial and manual gestures by human neonates. Science, 198(4312), 74–78. https://doi.org/10.1126/science.897687

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  66. Negri, G. A. L., Rumiati, R., Zadini, A., Ukmar, M., Mahon, B., & Caramazza, A. (2007). What is the role of motor simulation in action and object recognition? Evidence from apraxia. Cognitive Neuropsychology. https://doi.org/10.1080/02643290701707412

    PubMed  Article  PubMed Central  Google Scholar 

  67. Orban, G. A., & Rizzolatti, G. (2012). An area specifically devoted to tool use in human left inferior parietal lobule. The Behavioral and Brain Sciences.

  68. Orban, G. A., Claeys, K., Nelissen, K., Smans, R., Sunaert, S., Todd, J. T., … Vanduffel, W. (2006). Mapping the parietal cortex of human and non-human primates. Neuropsychologia, 44(13), 2647–2667. https://doi.org/10.1016/j.neuropsychologia.2005.11.001

    Article  PubMed  PubMed Central  Google Scholar 

  69. Orban, G. A., Sunaert, S., Todd, J. T., Van Hecke, P., & Marchal, G. (1999). Human cortical regions involved in extracting depth from motion. Neuron. https://doi.org/10.1016/S0896-6273(00)81040-5

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  70. Orban, G. A., & Caruana, F. (2014). The neural basis of human tool use. Frontiers in Psychology, 5, 310.

    PubMed  PubMed Central  Google Scholar 

  71. Osiurak, F. (2014a). What neuropsychology tells us about human tool use? The four constraints theory (4CT): Mechanics, space, time, and effort. Neuropsychology Review. https://doi.org/10.1007/s11065-014-9260-y

    PubMed  Article  PubMed Central  Google Scholar 

  72. Osiurak, F., Jarry, C., Allain, P., Aubin, G., Etcharry-Bouyx, F., Richard, I., … Le Gall, D. (2009). Unusual use of objects after unilateral brain damage. The technical reasoning model. Cortex, 45(6), 769–783. https://doi.org/10.1016/j.cortex.2008.06.013

    Article  PubMed  PubMed Central  Google Scholar 

  73. Osiurak, F. (2014b). Mechanical knowledge, but not manipulation knowledge, might support action prediction. Frontiers in Human Neuroscience, 8, 737.

    PubMed  PubMed Central  Article  Google Scholar 

  74. Osiurak, F., & Badets, A. (2016). Tool use and affordance: Manipulation-based versus reasoning-based approaches tool use and affordance: Manipulation-based versus reasoning-based approaches. Psychological Review, 123(5), 534–568. https://doi.org/10.1037/rev0000027

    Article  PubMed  PubMed Central  Google Scholar 

  75. Osiurak, F., De Oliveira, E., Navarro, J., Lesourd, M., Claidière, N., & Reynaud, E. (2016). Physical intelligence does matter to cumulative technological culture. Journal of Experimental Psychology: General, 145(8), 941–948. https://doi.org/10.1037/xge0000189

    Article  Google Scholar 

  76. Osiurak, F., De Oliveira, E., Navarro, J., & Reynaud, E. (2019). The Castaway island: Distinct roles of theory of mind and technical reasoning in cumulative technological culture. Journal of Experimental Psychology: General. https://doi.org/10.1037/xge0000614

  77. Osiurak, F., & Heinke, D. (2018). Looking for intoolligence: A unified framework for the cognitive study of human tool use and technology. American Psychologist. https://doi.org/10.1037/amp0000162

    PubMed  Article  PubMed Central  Google Scholar 

  78. Osiurak, F., Jarry, C., & Le Gall, D. (2010). Grasping the affordances, understanding the reasoning: Toward a dialectical theory of human tool use. Psychological Review, 117(2), 517–540. https://doi.org/10.1037/a0019004

    Article  PubMed  PubMed Central  Google Scholar 

  79. Osiurak, F., & Rossetti, Y. (2017). Definition: Limb apraxia. Cortex. https://doi.org/10.1016/j.cortex.2017.03.010

    PubMed  Article  PubMed Central  Google Scholar 

  80. Osiurak, F., Rossetti, Y., & Badets, A. (2017). What is an affordance? 40 years later. Neuroscience & Biobehavioral Reviews, 77, 403–417. https://doi.org/10.1016/j.neubiorev.2017.04.014

    Article  Google Scholar 

  81. Peelen, M. V., & Downing, P. E. (2005). Is the extrastriate body area involved in motor actions? Nature Neuroscience, 8(2), 125.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  82. Peeters, R. R., Rizzolatti, G., & Orban, G. A. (2013). Functional properties of the left parietal tool use region. NeuroImage. https://doi.org/10.1016/j.neuroimage.2013.04.023

    PubMed  Article  PubMed Central  Google Scholar 

  83. Peeters, R., Simone, L., Nelissen, K., Fabbri-Destro, M., Vanduffel, W., Rizzolatti, G., & Orban, G. A. (2009). The representation of tool use in humans and Monkeys: Common and uniquely human features. Journal of Neuroscience. https://doi.org/10.1523/JNEUROSCI.2040-09.2009

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  84. Petrides, M. (2005). Lateral prefrontal cortex: Architectonic and functional organization. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. https://doi.org/10.1098/rstb.2005.1631

    Article  Google Scholar 

  85. Rajah, M. N., Ames, B., & D’Esposito, M. (2008). Prefrontal contributions to domain-general executive control processes during temporal context retrieval. Neuropsychologia. https://doi.org/10.1016/j.neuropsychologia.2007.10.023

    PubMed  Article  PubMed Central  Google Scholar 

  86. Reynaud, E., Lesourd, M., Navarro, J., & Osiurak, F. (2016). On the neurocognitive origins of human tool use: A critical review of neuroimaging data. Neuroscience & Biobehavioral Reviews, 64, 421–437. https://doi.org/10.1016/j.neubiorev.2016.03.009

    Article  Google Scholar 

  87. Rizzolatti, G., Fadiga, L., Matelli, M., Bettinardi, V., Paulesu, E., Perani, D., & Fazio, F. (1996). Localization of grasp representations in humans by PET: 1. Observation versus execution. Experimental Brain Research, 111(2). https://doi.org/10.1007/BF00227301

  88. Rumiati, R. I., Zanini, S., Vorano, L., & Shallice, T. (2001). A form of ideational apraxia as a selective deficit of contention scheduling. Cognitive Neuropsychology. https://doi.org/10.1080/02643290126375

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  89. Rumiati, R. I., Weiss, P. H., Shallice, T., Ottoboni, G., Noth, J., Zilles, K., & Fink, G. R. (2004). Neural basis of pantomiming the use of visually presented objects. NeuroImage. https://doi.org/10.1016/j.neuroimage.2003.11.017

    PubMed  Article  PubMed Central  Google Scholar 

  90. Salimi-Khorshidi, G., Smith, S. M., Keltner, J. R., Wager, T. D., & Nichols, T. E. (2009). Meta-analysis of neuroimaging data: A comparison of image-based and coordinate-based pooling of studies. NeuroImage, 45(3), 810–823. https://doi.org/10.1016/j.neuroimage.2008.12.039

    Article  PubMed  PubMed Central  Google Scholar 

  91. Samartsidis, P., Montagna, S., Johnson, T. D., & Nichols, T. E. (2017). The coordinate-based meta-analysis of neuroimaging data. Statistical Science, 32(4), 580–599. https://doi.org/10.1214/17-STS624

    Article  PubMed  PubMed Central  Google Scholar 

  92. Shmuelof, L., & Zohary, E. (2006). A mirror representation of others’ actions in the human anterior parietal cortex. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 26(38), 9736–9742. https://doi.org/10.1523/JNEUROSCI.1836-06.2006

    CAS  Article  Google Scholar 

  93. Stadler, W., Schubotz, R. I., von Cramon, D. Y., Springer, A., Graf, M., & Prinz, W. (2011). Predicting and memorizing observed action: Differential premotor cortex involvement. Human Brain Mapping. https://doi.org/10.1002/hbm.20949

    PubMed  Article  PubMed Central  Google Scholar 

  94. Sunaert, S., Van Hecke, P., Marchal, G., & Orban, G. A. (1999). Motion-responsive regions of the human brain. Experimental Brain Research. https://doi.org/10.1007/s002210050804

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  95. Taylor, J. C., Wiggett, A. J., & Downing, P. E. (2007). Functional MRI analysis of body and body part representations in the extrastriate and fusiform body areas. Journal of Neurophysiology, 98(3), 1626–1633. https://doi.org/10.1152/jn.00012.2007

    Article  PubMed  PubMed Central  Google Scholar 

  96. Tench, C. R., Tanasescu, R., Constantinescu, C. S., Auer, D. P., & Cottam, W. J. (2017). Coordinate based random effect size meta-analysis of neuroimaging studies. NeuroImage, 153, 293–306. https://doi.org/10.1016/J.NEUROIMAGE.2017.04.002

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  97. Tessari, A., Canessa, N., Ukmar, M., & Rumiati, R. I. (2007). Neuropsychological evidence for a strategic control of multiple routes in imitation. Brain. https://doi.org/10.1093/brain/awm003

    Article  Google Scholar 

  98. Thompson-Schill, S. L., D’Esposito, M., Aguirre, G. K., & Farah, M. J. (1997). Role of left inferior prefrontal cortex in retrieval of semantic knowledge: A reevaluation. Proceedings of the National Academy of Sciences. https://doi.org/10.1073/pnas.94.26.14792

    CAS  Article  Google Scholar 

  99. Tomasello, M., Carpenter, M., Call, J., Behne, T., & Moll, H. (2005). Understanding and sharing intentions: The origins of cultural cognition. Behavioral and Brain Sciences, 28(05). https://doi.org/10.1017/S0140525X05000129

    PubMed  Article  PubMed Central  Google Scholar 

  100. Tomassini, V., Jbabdi, S., Klein, J. C., Behrens, T. E. J., Pozzilli, C., Matthews, P. M., … Johansen-Berg, H. (2007). Diffusion-weighted imaging tractography-based parcellation of the human lateral premotor cortex identifies dorsal and ventral subregions with anatomical and functional specializations. Journal of Neuroscience. https://doi.org/10.1523/JNEUROSCI.2144-07.2007

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  101. Tootell, R. B., Reppas, J. B., Kwong, K. K., Malach, R., Born, R. T., Brady, T. J., … Belliveau, J. W. (1995). Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging. The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 15(4), 3215–3230 fmri_Mary M-converted #34; used to be #2162 and #2324.

    CAS  Article  Google Scholar 

  102. Turkeltaub, P. E., Eden, G. F., Jones, K. M., & Zeffiro, T. A. (2002). Meta-analysis of the functional neuroanatomy of single-word reading: Method and validation. Neuroimage, 16(3 Pt 1), 765–780.

    PubMed  PubMed Central  Article  Google Scholar 

  103. Uithol, S., van Rooij, I., Bekkering, H., & Haselager, P. (2011). Understanding motor resonance. Social Neuroscience, 6(4), 388–397. https://doi.org/10.1080/17470919.2011.559129

    Article  PubMed  PubMed Central  Google Scholar 

  104. van Elk, M., van Schie, H., & Bekkering, H. (2014). Action semantics: A unifying conceptual framework for the selective use of multimodal and modality-specific object knowledge. Physics of Life Reviews. https://doi.org/10.1016/j.plrev.2013.11.005

    PubMed  Article  PubMed Central  Google Scholar 

  105. Van Essen, D. C. (2005). A population-average, landmark- and surface-based (PALS) atlas of human cerebral cortex. NeuroImage, 28(3), 635–662. https://doi.org/10.1016/j.neuroimage.2005.06.058

    Article  PubMed  PubMed Central  Google Scholar 

  106. Van Overwalle, F., & Baetens, K. (2009). Understanding others’ actions and goals by mirror and mentalizing systems: A meta-analysis. NeuroImage. https://doi.org/10.1016/j.neuroimage.2009.06.009

    PubMed  Article  PubMed Central  Google Scholar 

  107. Vanduffel, W., Zhu, Q., & Orban, G. A. (2014). Monkey cortex through fMRI glasses. Neuron, 83(3), 533–550. https://doi.org/10.1016/j.neuron.2014.07.015

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  108. Vingerhoets, G. (2014). Contribution of the posterior parietal cortex in reaching, grasping, and using objects and tools. Frontiers in Psychology, 5, 151.

    PubMed  PubMed Central  Article  Google Scholar 

  109. Wager, T. D., Lindquist, M. A., Nichols, T. E., Kober, H., & Van Snellenberg, J. X. (2009). Evaluating the consistency and specificity of neuroimaging data using meta-analysis. NeuroImage. https://doi.org/10.1016/j.neuroimage.2008.10.061

    PubMed  Article  PubMed Central  Google Scholar 

  110. Watson, J. D. G., Myers, R., Frackowiak, R. S. J., Hajnal, J. V., Woods, R. P., Mazziotta, J. C., … Zeki, S. (1993). Area V5 of the human brain: Evidence from a combined study using positron emission tomography and magnetic resonance imaging. Cerebral Cortex, 3(2), 79–94. https://doi.org/10.1093/cercor/3.2.79

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  111. Wolpert, D. M., Ghahramani, Z., & Jordan, M. I. (1995). An internal model for sensorimotor integration. Science-AAAS-weekly paper edition, 269(5232), 1880-1882. Science-AAAS-Weekly Paper Edition.

  112. Yarkoni, T., Poldrack, R. A., Van Essen, D. C., & Wager, T. D. (2010). Cognitive neuroscience 2.0: Building a cumulative science of human brain function. Trends in Cognitive Sciences. https://doi.org/10.1016/j.tics.2010.08.004

    PubMed  PubMed Central  Article  Google Scholar 

  113. Zeki, S., Watson, J. D., Lueck, C. J., Friston, K. J., Kennard, C., & Frackowiak, R. S. (1991). A direct demonstration of functional specialization in human visual cortex. The Journal of Neuroscience, 11(March), 641–649 https://doi.org/10.1523/JNEUROSCI.11-03-00641.1991

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  114. Zhang, Z., Sun, Y., Humphreys, G. W., & Song, Y. (2017). Different activity patterns for action and language within their shared neural areas: An fMRI study on action observation and language phonology. Neuropsychologia. https://doi.org/10.1016/j.neuropsychologia.2017.02.025

    PubMed  Article  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from ANR (Agence Nationale pour la Recherche; Project “Cognition et économie liée à l’outil/Cognition and tool-use economy”, N°ANR-14-C230-0015-01), and was performed within the framework of the LABEX CORTEX (ANR-11-LABX-0042) of Université de Lyon, within the program “Investissements d’Avenir” (ANR-11-IDEX-0007) operated by the French National Research Agency (ANR).

Author Contribution Statement

E.R. and F.O. designed the study. E.R. and F.O. analyzed the data. All authors discussed the results and commented on the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Emanuelle Reynaud.

Ethics declarations

Competing Interests

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Supplementary information accompanies this paper at XXXX.

ESM 1

(PDF 143 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Reynaud, E., Navarro, J., Lesourd, M. et al. To Watch is to Work: a Review of NeuroImaging Data on Tool Use Observation Network. Neuropsychol Rev 29, 484–497 (2019). https://doi.org/10.1007/s11065-019-09418-3

Download citation

Keywords

  • Tool use
  • Action observation
  • Left inferior parietal cortex
  • Meta-analysis