The neural basis of human tool use

Frontiers in Psychology

Volumn 5, Issue APR, 2014, Pages

  Orban, Guy A ^a   Caruana, Fausto ^a,b  

^a UNIVERSITY OF PARMA   (Italy)

^b ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

Author keywords

Affordances; Anterior intraparietal sulcus; Anterior supramarginal gyrus; Mechanical problem solving; Tool use

Indexed keywords

EID: 84899667858     PISSN: None     EISSN: 16641078     Source Type: Journal    
DOI: 10.3389/fpsyg.2014.00310     Document Type: Article

References (105)

1. Ambrose, S. H. (2001). Paleolithic technology and human evolution. Science 291, 1748-1753. doi: 10.1126/science.1059487.
2. Arcaro, M. J., Pinsk, M. A., Li, X., and Kastner, S. (2011). Visuotopic organization of macaque posterior parietal cortex: a functional magnetic resonance imaging study. J. Neurosci. 31, 2064-2078. doi: 10.1523/JNEUROSCI.3334-10.2011.
3. Asfaw, B., Beyene, Y., Suwa, G., Walter, R. C., White, T. D., WoldeGabriel, G., et al. (1992). The earliest Acheulean from Konso-Gardula. Nature 360, 732-735. doi: 10.1038/360732a0.
4. Baber, C. (2003). Cognition and Tool Use: Forms of Engagement in Human and Animal Use of Tools. London: Taylor&Francis. doi: 10.1201/9781420024203.
5. Bach, P., Peelen, M. V., and Tipper, S. P. (2010). On the role of object information in action observation: an fMRI study. Cereb. Cortex 20, 2798-2809. doi: 10.1093/cercor/bhq026.
6. Beauchamp, M. S., Lee, K. E., Haxby, J. V., and Martin, A. (2002). Parallel visual motion processing streams for manipulable objects and human movements. Neuron 34, 149-159. doi: 10.1016/S0896-6273(02)00642-6.
7. Beck, B. B. (1980). Animal Tool Use Behavior: The Use and Manufacture of Tools by Animals. New York: Garland Publishing.
8. Binkofski, F., and Buxbaum, L. J. (2013). Two action systems in the human brain. Brain Lang. 127, 222-229. doi: 10.1016/j.bandl.2012.07.007.
9. Binkofski, F., Dohle, C., Posse, S., Stephan, K. M., Hefter, H., Seitz, R. J., et al. (1998). Human anterior intraparietal area subserves prehension: a combined lesion and functional MRI activation study. Neurology 50, 1253-1259. doi: 10.1212/WNL.50.5.1253.
10. Borra, E., Belmalih, A., Calzavara, R., Gerbella, M., Murata, A., Rozzi, S., et al. (2008). Cortical connections of the macaque anterior intraparietal (AIP) area. Cereb. Cortex 18, 1094-1111. doi: 10.1093/cercor/bhm146.
11. Bunzeck, N., Wuestenberg, T., Lutz, K., Heinze, H. J., and Jancke, L. (2005). Scanning silence: mental imagery of complex sounds. Neuroimage 26, 1119-1127. doi: 10.1016/j.neuroimage.2005.03.013.
12. Carreiras, M., Seghier, M. L., Baquero, S., Estévez, A., Lozano, A., Devlin, J. T., et al. (2009). An anatomical signature for literacy. Nature 461, 983-986. doi: 10.1038/nature08461.
13. Caspers, S., Eickhoff, S. B., Geyer, S., Scheperjans, F., Mohlberg, H., Zilles, K., et al. (2008). The human inferior parietal lobule in stereotaxic space. Brain Struct. Funct. 212, 481-495. doi: 10.1007/s00429-008-0195-z.
14. Cattaneo, L., Caruana, F., Jezzini, A., and Rizzolatti, G. (2009). Representation of goal and movements without overt motor behavior: a TMS study, J. Neurosci. 29, 11134-11138. doi: 10.1523/JNEUROSCI.2605-09.2009.
15. Chao, L. L., Haxby, J. V., and Martin, A. (1999). Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects. Nat. Neurosci. 2, 913-919. doi: 10.1038/13217.
16. Chao, L. L., and Martin, A. (2000). Representation of manipulable man-made objects in the dorsal stream. Neuroimage 12, 478-484. doi: 10.1006/nimg.2000.0635.
17. Claeys, K. G., Lindsey, D. T., De Schutter, E., and Orban, G. A. (2003). A higher order motion region in human inferior parietal lobule: evidence from fMRI. Neuron 40, 631-642. doi: 10.1016/S0896-6273(03)00590-7.
18. Cogan, G. B., Thesen, T., Carlson, C., Doyle, W., Devinsky, O., and Pesaran, B. (2014). Sensory-motor transformations for speech occur bilaterally. Nature 507, 94-98. doi: 10.1038/nature12935.
19. Coqueugniot, H., Hublin, J. J., Veillon, F., Houët, F., and Jacob, T. (2004). Early brain growth in Homo erectus and implications for cognitive ability. Nature 16, 431, 299-302. doi: 10.1038/nature02852.
20. Creem-Regehr, S. H., and Lee, J. N. (2005). Neural representations of graspable objects: are tools special? Brain Res. Cogn. Brain Res. 22, 457-469. doi: 10.1016/j.cogbrainres.2004.10.006.
21. Daprati, E., and Sirigu, A. (2006). How we interact with objects: learning from brain lesions. Trends Cogn. Sci. 10, 265-270. doi: 10.1016/j.tics.2006.04.005.
22. Denys, K., Vanduffel, W., Fize, D., Nelissen, K., Peuskens, H., Van Essen, D., et al. (2004). The processing of visual shape in the cerebral cortex of human and nonhuman primates: a functional magnetic resonance imaging study. J. Neurosci. 24, 2551-2565. doi: 10.1523/JNEUROSCI.3569-03.2004.
23. Devlin, J. T., Russell, R. P., Davis, M. H., Price, C. J., Moss, H. E., Fadili, M. J., et al. (2002). Is there an anatomical basis for category-specificity? Semantic memory studies in PET and fMRI. Neuropsychologia 40, 54-75. doi: 10.1016/S0028-3932(01)00066-5.
24. Durand, J.-B. B., Peeters, R., Norman, J. F., Todd, J. T., and Orban, G. A. (2009). Parietal regions processing visual 3D shape extracted from disparity. Neuroimage 46, 1114-1126. doi: 10.1016/j.neuroimage.2009.03.023.
25. Eickhoff, S. B., Heim, S., Zilles, K., and Amunts, K. (2006). Testing anatomically specified hypotheses in functional imaging using cytoarchitectonic maps. Neuroimage 32, 570-582. doi: 10.1016/j.neuroimage.2006.04.204.
26. Ferri, S., Rizzolatti, G., and Orban, G. A. (2013). Observing three classes of action performed with the upper limb, sfn abstract 824.01/Z16.
27. Freedman, D. J., and Assad, J. A. (2006). Experience-dependent representation of visual categories in parietal cortex. Nature 443, 85-88. doi: 10.1038/nature05078.
28. Gallivan, J. P., McLean, D. A., Valyear, K. F., and Culham, J. C. (2013). Decoding the neural mechanisms of human tool use. Elife 2, e00425. doi: 10.7554/eLife.00425.
29. Georgieva, S., Peeters, R., Kolster, H., Todd, J. T., and Orban, G. A. (2009). The processing of threedimensional shape from disparity in the human brain. J. Neurosci. 29, 727-742. doi: 10.1523/JNEUROSCI.4753-08.2009.
30. Goldenberg, G., and Hagmann, S. (1998). Tool use and mechanical problem solving in apraxia. Neuropsychologia 36, 581-589. doi: 10.1016/S0028-3932(97)00165-6.
31. Goldenberg, G., and Spatt, J. (2009). The neural basis of tool use. Brain 132, 1645-1655. doi: 10.1093/brain/awp080.
32. Goldenberg, G. (2009). Apraxia and the parietal lobes. Neuropsychologia 47, 1449-1559. doi: 10.1016/j.neuropsychologia.2008.07.014.
33. Hecht, E. E., Murphy, L. E., Gutman, D. A., Votaw, J. R., Schuster, D. M., Preuss, T. M., et al. (2013). Differences in neural activation for object-directed grasping in chimpanzees and humans. J. Neurosci. 33, 14117-14134. doi: 10.1523/JNEUROSCI.2172-13.2013.
34. Hegarty, M. (2004). Mechanical reasoning by mental simulation. Trends Cogn. Sci. 8, 280-285. doi: 10.1016/j.tics.2004.04.001.
35. Hickok, G., and Poeppel, D. (2007). The cortical organization of speech processing. Nat. Rev. Neurosci. 8, 393-402. doi: 10.1038/nrn2113.
36. Inoue, K., Kawashima, R., Sugiura, M., Ogawa, A., Schormann, T., Zilles, K., et al. (2001). Activation in the ipsilateral posterior parietal cortex during tool use: a PET study. Neuroimage 14, 1469-1475. doi: 10.1006/nimg.2001.0942.
37. Iriki, A., Tanaka, M., and Iwamura, Y. (1996). Coding of modified body schema during tool use by macaque postcentral neurones. Neuroreport 7, 2325-2330. doi: 10.1097/00001756-199610020-00010.
38. Jacobs, S., Danielmeier, C., and Frey, S. H. (2009). Human anterior intraparietal and ventral premotor cortices support representations of grasping with the hand or a novel tool. J. Cogn. Neurosci. 22, 2594-2608. doi: 10.1162/jocn.2009.21372.
39. Janssens, T., Arsenault, J. T., Polimeni, J. R., and Vanduffel, W. (2013). Definition of the macaque posterior parietal regions using MRI-based measures of retinotopy, connectivity, myelination, and function, sfn abstract 64.04/GG12.
40. Järveläinen, J., Schürmann, M., and Hari, R. (2004). Activation of the human primary motor cortex during observation of tool use. Neuroimage 23, 187-192. doi: 10.1016/j.neuroimage.2004.06.010.
41. Jastorff, J., and Orban, G. A. (2009). Human functional magnetic resonance imaging reveals separation and integration of shape and motion cues in biological motion processing. J. Neurosci. 29, 7315-7329. doi: 10.1523/JNEUROSCI.4870-08.2009.
42. Jastorff, J., Popivanov, I. D., Vogels, R., Vanduffel, W., and Orban, G. A. (2012). Integration of shape and motion cues in biological motion processing in the monkey STS. Neuroimage 60, 911-921. doi: 10.1016/j.neuroimage.2011.12.087.
43. Johnson-Frey, S. H., Newman-Norlund, R., and Grafton, S. T. (2005). A distributed left hemisphere network active during planning of everyday tool use skills. Cereb. Cortex 15, 681-695. doi: 10.1093/cercor/bhh169.
44. Joly, O., Ramus, F., Pressnitzer, D., Vanduffel, W., and Orban, G. A. (2012). Interhemispheric differences in auditory processing revealed by fMRI in awake rhesus monkeys. Cereb. Cortex 22, 838-853. doi: 10.1093/cercor/bhr150.
45. Kalénine, S., Buxbaum, L. J., and Coslett, H. B. (2010). Critical brain regions for action recognition: lesion symptom mapping in left hemisphere stroke. Brain 133, 3269-3280. doi: 10.1093/brain/awq210.
46. Kolster, H., Mandeville, J. B., Arsenault, J. T., Ekstrom, L. B., Wald, L. L., and Vanduffel, W. (2009). Visual field map clusters in macaque extrastriate visual cortex. J. Neurosci. 29, 7031-7039. doi: 10.1523/JNEUROSCI.0518-09.2009.
47. Kolster, H., Peeters, R., and Orban, G. A. (2010). The retinotopic organization of the human middle temporal area MT/V5 and its cortical neighbors. J. Neurosci. 30, 9801-9820. doi: 10.1523/JNEUROSCI.2069-10.2010.
48. Kolster, H., Peeters, R., and Orban, G. A. (2011). Ten retinotopically organized areas in the human parietal cortex, sfn abstract 851.10.
49. Króliczak, G., and Frey, S. H. (2009). A common network in the left cerebral hemisphere represents planning of tool use pantomimes and familiar intransitive gestures at the hand-independent level. Cereb. Cortex 19, 2396-2410. doi: 10.1093/cercor/bhn261.
50. Lewis, J. W., Brefczynski, J. A., Phinney, R. E., Janik, J. J., and DeYoe, E. A. (2005). Distinct cortical pathways for processing tool versus animal sounds. J. Neurosci. 25, 5148-5158. doi: 10.1523/JNEUROSCI.0419-05.2005.
51. Lewis, J. W., Phinney, R. E., Brefczynski-Lewis, J. A., and DeYoe, E. A. (2006). Lefties get it "right" when hearing tool sounds. J. Cogn. Neurosci. 18, 1314-1330. doi: 10.1162/jocn.2006.18.8.1314.
52. Mahon, B. Z., Milleville, S. C., Negri, G. A. L., Rumiati, R. I., Caramazza, A., and Martin, A. (2007). Action-related properties shape object representations in the ventral stream. Neuron 55, 507-520. doi: 10.1016/j.neuron.2007.07.011.
53. Mars, R. B., Jbabdi, S., Sallet, J., O'Reilly, J. X., Croxson, P. L., Olivier, E., et al. (2011). Diffusion-weighted imaging tractography-based parcellation of the human parietal cortex and comparison with human and macaque resting-state functional connectivity. J. Neurosci. 31, 4087-4100. doi: 10.1523/JNEUROSCI.5102-10.2011.
54. Maravita, A., and Iriki, A. (2004). Tools for the body (schema). Trends Cogn. Sci. 8, 79-86. doi: 10.1016/j.tics.2003.12.008.
55. Martin, K., Jacobs, S., and Frey, S. H. (2011). Handedness-dependent and-independent cerebral asymmetries in the anterior intraparietal sulcus and ventral premotor cortex during grasp planning. Neuroimage 57, 502-512. doi: 10.1016/j.neuroimage.2011.04.036.
56. Massen, C., and Prinz, W. (2007). Programming tool-use actions. J. Exp. Psychol. Hum. Percept. Perform. 33, 692-704. doi: 10.1037/0096-1523.33.3.692.
57. Moll, J., de Oliveira-Souza, R., Passman, L. J., Cunha, F. C., Souza-Lima, F., and Andreiuolo, P. A. (2000). Functional MRI correlates of real and imagined tool-use pantomimes. Neurology 54, 1331-1336. doi: 10.1212/WNL.54.6.1331.
58. Mruczek, R. E., von Loga, I. S., and Kastner, S. (2013). The representation of tool, and non-tool object information in the human intraparietal sulcus. J. Neurophysiol. 109, 2883-2896. doi: 10.1152/jn.00658.2012.
59. Murata, A., Gallese, V., Kaseda, M., and Sakata, H. (1996). Parietal neurons related to memory-guided hand manipulation. J. Neurophysiol. 75, 2180-2186.
60. Murata, A., Gallese, V., Luppino, G., Kaseda, M., and Sakata, H. (2000). Selectivity for the shape, size, and orientation of objects for grasping in neurons of monkey parietal area AIP. J Neurophysiol. 83, 2580-2601.
61. Nakamura, H., Kuroda, T., Wakita, M., Kusunoki, M., Kato, A., Mikami, A., et al. (2001). From three-dimensional space vision to prehensile hand movements: the lateral intraparietal area links the area V3A and the anterior intraparietal area in macaques. J. Neurosci. 21, 8174-8187.
62. Nelissen, K., Borra, E., Gerbella, M., Rozzi, S., Luppino, G., Vanduffel, W., et al. (2011). Action observation circuits in the macaque monkey cortex, J. Neurosci. 31, 3743-3756. doi: 10.1523/JNEUROSCI.4803-10.2011.
63. Okada, T., Tanaka, S., Nakai, T., Nishizawa, S., Inui, T., Sadato, N., et al. (2000). Naming of animals and tools: a functional magnetic resonance imaging study of categorical differences in the human brain areas commonly used for naming visually presented objects. Neurosci. Lett. 296, 33-36. doi: 10.1016/S0304-3940(00)01612-8.
64. Orban, G. A., Claeys, K., Nelissen, K., Smans, R., Sunaert, S., Todd, J. T., et al. (2006). Mapping the parietal cortex of human and non-human primates. Neuropsychologia 44, 2647-2667. doi: 10.1016/j.neuropsychologia.2005.11.001.
65. Orban, G. A., Peeters, R., Vanduffel, W., Rizzolatti, G., and Nelissen, K. (2012). Using parallel fMRI in human and nonhuman primates to locate premotor area F5c in humans, sfn abstract 13.10.
66. Osiurak, F. (2013). Apraxia of tool use is not a matter of affordances. Front. Hum. Neurosci. 7:890. doi: 10.3389/fnhum.2013.00890.
67. Osiurak, F., Jarry, C., Allain, P., Aubin, G., Etcharry-Bouyx, F., Richard, I., et al. (2009). Unusual use of objects after unilateral brain damage: the technical reasoning model. Cortex 45, 769-783. doi: 10.1016/j.cortex.2008.06.013.
68. Osiurak, F., Jarry, C., and Le Gall, D. (2010). Grasping the affordances, understanding the reasoning: toward a dialectical theory of human tool use. Psychol. Rev. 117, 517-540. doi: 10.1037/a0019004.
69. Peelen, M. V., Bracci, S., Lu, X., He, C., Caramazza, A., and Bi, Y. (2013). Tool selectivity in left occipitotemporal cortex develops without vision. J. Cogn. Neurosci. 25, 1225-1234. doi: 10.1162/jocn_a_00411.
70. Peeters, R., Simone, L., Nelissen, K., Fabbri-Destro, M., Vanduffel, W., Rizzolatti, G., et al. (2009). The representation of tool use in humans and monkeys: common and uniquely human features. J. Neurosci. 29, 11523-11539. doi: 10.1523/JNEUROSCI.2040-09.2009.
71. Peeters, R. R., Rizzolatti, G., and Orban, G. A. (2013). Functional properties of the left parietal tool use region. Neuroimage 78, 83-93. doi: 10.1016/j.neuroimage.2013.04.023.
72. Povinelli, D. J., Reaux, J. E., Theall, L. A., and Giambrone, S. (2000). Folk Physics for Apes: The Chimpanzee's Theory of How the World Works. Oxford: Oxford University Press.
73. Preston, B. (1998). Cognition and tool use. Mind Lang. 13, 513-547. doi: 10.1111/1468-0017.00090.
74. Ramayya, A. G., Glasser, M. F., and Rilling, J. K. (2010). A DTI investigation of neural substrates supporting tool use. Cereb. Cortex 20, 507-516. doi: 10.1093/cercor/bhp141.
75. Rizzolatti, G., and Craighero, L. (2004). The mirror neuron system. Annu. Rev. Neurosci. 27, 169-192. doi: 10.1146/annurev.neuro.27.070203.144230.
76. Rizzolatti, G., and Matelli, M. (2003). Two different streams form the dorsal visual system: anatomy and functions. Exp. Brain Res. 153, 146-157. doi: 10.1007/s00221-003-1588-0.
77. Rochat, M., Caruana, F., Jezzini, A., Escola, L., Intskirveli, I., Grammont, F., et al. (2010). Responses of mirror neurons in area F5 to hand and tool grasping observation. Exp. Brain Res. 204, 605-616. doi: 10.1007/s00221-010-2329-9.
78. Roche, H., Delagnes, A., Brugal, J. P., Feibel, C., Kibunjia, M., Mourre, V., et al. (1999). Early hominid stone tool production and technical skill 2.34 Myr ago in West Turkana, Kenya. Nature 399, 57-60. doi: 10.1038/19959.
79. Ruff, C. (2009). Relative limb strength and locomotion. Am. J. Phys. Anthropol. 138, 90-100. doi: 10.1002/ajpa.20907.
80. Rumiati, R. I., Weiss, P. H., Shallice, T., Ottoboni, G., Noth, J., Zilles, K., et al. (2004). Neural basis of pantomiming the use of visually presented objects. Neuroimage 21, 1224-1231. doi: 10.1016/j.neuroimage.2003.11.017.
81. Rushworth, M. F., Johansen-Berg, H., Göbel, S. M., and Devlin, J. T. (2003). The left parietal and premotor cortices: motor attention and selection. Neuroimage 20(Suppl. 1), S89-S100. doi: 10.1016/j.neuroimage.2003.09.011.
82. Sawamura, H., Orban, G. A., and Vogels, R. (2006). Selectivity of neuronal adaptation does not match response selectivity: a single-cell study of the FMRI adaptation paradigm. Neuron 49, 307-318. doi: 10.1016/j.neuron.2005.11.028.
83. Silver, M. A., Ress, D., and Heeger, D. J. (2005). Topographic maps of visual spatial attention in human parietal cortex. J. Neurophysiol. 94, 1358-1371. doi: 10.1152/jn.01316.2004.
84. Srivastava, S., Orban, G. A., De Mazière, P. A., and Janssen, P. (2009). A distinct representation of three-dimensional shape in macaque anterior intraparietal area: fast, metric, and coarse. J. Neurosci. 29, 10613-10626. doi: 10.1523/JNEUROSCI.6016-08.2009.
85. Stout, D., and Chaminade, T. (2007). The evolutionary neuroscience of tool making. Neuropsychologia 45, 1091-1100. doi: 10.1016/j.neuropsychologia.2006.09.014.
86. Stout, D., and Chaminade, T. (2012). Stone tools, language and the brain in human evolution. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367, 75-87. doi: 10.1098/rstb.2011.0099.
87. Stout, D., Passingham, R., Frith, C., Apel, J., and Chaminade, T. (2011). Technology, expertise and social cognition in human evolution. Eur. J. Neurosci. 33, 1328-1338. doi: 10.1111/j.1460-9568.2011.07619.x.
88. Stout, D., Toth, N., Schick, K., and Chaminade, T. (2008). Neural correlates of Early Stone Age toolmaking: technology, language and cognition in human evolution. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363, 1939-1949. doi: 10.1098/rstb.2008.0001.
89. Sunaert, S., Van Hecke, P., Marchal, G., and Orban, G. A. (1999). Motion-responsive regions of the human brain. Exp. Brain Res. 127, 355-370. doi: 10.1007/s002210050804.
90. Sunderland, A., Wilkins, L., Dineen, R., and Dawson, S. E. (2013). Tool-use and the left hemisphere: what is lost in ideomotor apraxia? Brain Cogn. 81, 183-192. doi: 10.1016/j.bandc.2012.10.008.
91. Susman, R. L. (1994). Fossil evidence for early hominid tool use. Science 265, 1570-1573. doi: 10.1126/science.8079169.
92. Tomassini, V., Jbabdi, S., Klein, J. C., Behrens, T. E., Pozzilli, C., Matthews, P. M., et al. (2007). Diffusion-weighted imaging tractography-based parcellation of the human lateral premotor cortex identifies dorsal and ventral subregions with anatomical and functional specializations. J. Neurosci. 27, 10259-10269. doi: 10.1523/JNEUROSCI.2144-07.2007.
93. Tootell, R. B., Mendola, J. D., Hadjikhani, N. K., Ledden, P. J., Liu, A. K., Reppas, J. B., et al. (1997). Functional analysis of V3A and related areas in human visual cortex. J. Neurosci. 17, 7060-7078.
94. Tsao, D. Y., and Livingstone, M. S. (2008). Mechanisms of face perception. Annu. Rev. Neurosci. 31, 411-437. doi: 10.1146/annurev.neuro.30.051606.094238.
95. Umiltà, M. A., Escola, L., Intskirveli, I., Grammont, F., Rochat, M., Caruana, F., et al. (2008). When pliers become fingers in the monkey motor system, Proc. Natl. Acad. Sci. U.S.A. 105, 2209-2213. doi: 10.1073/pnas.0705985105.
96. Vaesen, K. (2012). The cognitive bases of human tool use. Behav. Brain Sci. 35, 203-218. doi: 10.1017/S0140525X11001452.
97. Valyear, K. F., Cavina-Pratesi, C., Stiglick, A. J., and Culham, J. C. (2007). Does tool-related fMRI activity within the intraparietal sulcus reflect the plan to grasp? Neuroimage 36(Suppl. 2), T94-T108. doi: 10.1016/j.neuroimage.2007.03.031.
98. Valyear, K. F., Gallivan, J. P., McLean, D. A., and Culham, J. C. (2012). fMRI repetition suppression for familiar but not arbitrary actions with tools. J. Neurosci. 32, 4247-4259. doi: 10.1523/JNEUROSCI.5270-11.2012.
99. Vanduffel, W., Fize, D., Mandeville, J. B., Nelissen, K., Van Hecke, P., Rosen, B. R., et al. (2001). Visual motion processing investigated using contrast agent-enhanced fMRI in awake behaving monkeys. Neuron 32, 565-577. doi: 10.1016/S0896-6273(01)00502-5.
100. Vanduffel, W., Fize, D., Peuskens, H., Denys, K., Sunaert, S., Todd, J. T., et al. (2002). Extracting 3D from motion: differences in human and monkey intraparietal cortex. Science 298, 413-415. doi: 10.1126/science.1073574.
101. Van Essen, D. C. (2005). A population-average, landmark-and surface-based (PALS) atlas of human cerebral cortex. Neuroimage 28, 635-662. doi: 10.1016/j.neuroimage.2005.06.058.
102. Van Essen, D. C., Glasser, M. F., Dierker, D. L., Harwell, J., and Coalson, T. (2012). Parcellations and hemispheric asymmetries of human cerebral cortex analyzed on surface-based atlases. Cereb. Cortex 22, 2241-2262. doi: 10.1093/cercor/bhr291.
103. van Schaik, C. P., Deaner, R. O., and Merrill, M. Y. (1999). The conditions for tool use in primates: implications for the evolution of material culture. J. Hum. Evol. 36, 719-741. doi: 10.1006/jhev.1999.0304.
104. Wood, B., and Baker, J. (2011). Evolution of the Genus Homo. Annu. Rev. Ecol. Evol. Syst. 42, 47-69. doi: 10.1146/annurev-ecolsys-102209-144653.
105. Zhang, S., and Li, C. S. (2013). Functional clustering of the human inferior parietal lobule by whole-brain connectivity mapping of resting-state functional magnetic resonance imaging signals. Brain Connect. 4, 53-69. doi: 10.1089/brain.2013.0191.