ERPs differentially reflect automatic and deliberate processing of the functional manipulability of objects

Frontiers in Human Neuroscience

Volumn 10, Issue , 2016, Pages

  Madan, Christopher R ^a,b   Chen, Yvonne Y ^a   Singhal, Anthony ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b BOSTON COLLEGE   (United States)

Author keywords

Embodied cognition; Manipulability; Motor processing; Semantic knowledge; Tool use

Indexed keywords

ADULT; ARTICLE; ATTENTION; COGNITION; CONTROLLED STUDY; DECISION MAKING; ELECTROENCEPHALOGRAPHY; EVENT RELATED POTENTIAL; FEMALE; GENERAL DEVICE; HAMMER; HUMAN; HUMAN EXPERIMENT; LADDER; MALE; MOTOR PERFORMANCE; NORMAL HUMAN; PERSONAL EXPERIENCE; SLOW BRAIN WAVE; STIMULUS RESPONSE; TOOL USE; VISUAL STIMULATION;

EID: 84983761005     PISSN: None     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2016.00360     Document Type: Article

References (90)

1. Almeida, J., Fintzi, A. R., and Mahon, B. Z. (2013). Tool manipulation knowledge is retrieved by way of the ventral visual object processing pathway. Cortex 49, 2334-2344. doi: 10.1016/j.cortex.2013.05.004
2. Amsel, B. D., Urbach, T. P., and Kutas, M. (2013). Alive and grasping: stable and rapid semantic access to an object category but not object graspability. Neuroimage 77, 1-13. doi: 10.1016/j.neuroimage.2013.03.058
3. Arévalo, A., Perani, D., Cappa, S. F., Butler, A., Bates, E., and Dronkers, N. (2007). Action and object processing in aphasia: from nouns and verbs to the effect of manipulability. Brain Lang. 100, 79-94. doi: 10.1016/j.bandl.2006.06.012
4. Armstrong, G. A. B., and Singhal, A. (2011). Neural markers of automatic and controlled attention during immediate and delayed action. Exp. Brain Res. 213, 35-48. doi: 10.1007/s00221-011-2774-0
5. Bi, Y., Han, Z., Zhong, S., Ma, Y., Gong, G., Huang, R., et al. (2015). The white matter structural network underlying human tool use and tool understanding. J. Neurosci. 35, 6822-6835. doi: 10.1523/JNEUROSCI.3709-14.2015
6. Binkofski, F., Buccino, G., Posse, S., Seitz, R. J., Rizzolatti, G., and Freund, H. J. (1999). A fronto-parietal circuit for object manipulation in man: evidence from an fMRI-study. Eur. J. Neurosci. 11, 3276-3286. doi: 10.1046/j.1460-9568.1999.00753.x
7. Borghi, A. M., Bonfiglioli, C., Ricciardelli, P., Rubichi, S., and Nicoletti, R. (2007). “Do we access object manipulability while we categorize? Evidence from reaction times studies,” in Mental States: Evolution, Function, Nature, eds A. C. Schalley and D. Khlentzos (Philadelphia: John Benjamins), 153-170.
8. Boronat, C. B., Buxbaum, L. J., Coslett, H. B., Tang, K., Saffran, E. M., Kimberg, D. Y., et al. (2005). Distinctions between manipulation and function knowledge of objects: evidence from functional magnetic resonance imaging. Brain Res. Cogn. Brain Res. 23, 361-373. doi: 10.1016/j.cogbrainres.2004.11.001
9. Buccino, G., Sato, M., Cattaneo, L., Rodà, F., and Riggio, L. (2009). Broken affordances, broken objects: a TMS study. Neuropsychologia 47, 3074-3078. doi: 10.1016/j.neuropsychologia.2009.07.003
10. Buxbaum, L. J., and Saffran, E. M. (2002). Knowledge of object manipulation and object function: dissociations in apraxic and nonapraxic subjects. Brain Lang. 82, 179-199. doi: 10.1016/s0093-934x(02)00014-7
11. Campanella, F., and Shallice, T. (2011). Manipulability and object recognition: is manipulability a semantic feature? Exp. Brain Res. 208, 369-383. doi: 10.1007/s00221-010-2489-7
12. Canessa, N., Borgo, F., Cappa, S. F., Perani, D., Falini, A., Buccino, G., et al. (2008). The different neural correlates of action and functional knowledge in semantic memory: an fMRI study. Cereb. Cortex 18, 740-751. doi: 10.1093/cercor/bhm110
13. Capitani, E., Laiacona, M., Mahon, B., and Caramazza, A. (2003). What are the facts of semantic category-specific deficits? A critical review of the clinical evidence. Cogn. Neuropsychol. 20, 213-261. doi: 10.1080/02643290244000266
14. 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
15. Chen, Q., Garcea, F. E., and Mahon, B. Z. (2016). The representation of object-directed action and function knowledge in the human brain. Cereb. Cortex 26, 1609-1618. doi: 10.1093/cercor/bhu328
16. Chen, Y. Y., Lithgow, K., Hemmerich, J. A., and Caplan, J. B. (2014). Is what goes in what comes out? Encoding and retrieval event-related potentials together determine memory outcome. Exp. Brain Res. 232, 3175-3190. doi: 10.1007/s00221-014-4002-1
17. Codispoti, M., Ferrari, V., De Cesarei, A., and Cardinale, R. (2006). Implicit and explicit categorization of natural scenes. Prog. Brain Res. 156, 53-65. doi: 10.1016/s0079-6123(06)56003-0
18. Coles, M. G. (1989). Modern mind-brain reading: psychophysiology, physiology and cognition. Psychophysiology 26, 251-269. doi: 10.1111/j.1469-8986.1989.tb01916.x
19. Coles, M. G. H., Henderikus, G. O., Smid, M., Scheffers, M. K., and Otten, L. J. (1995). “Mental chronometry and the study of human information processing,” in Electrophysiology of Mind: Event-Related Brain Potentials and Cognition, eds M. D. Rugg and M. G. H. Coles (New York, NY: Oxford University Press), 86-131.
20. Delorme, A., and Makeig, S. (2004). EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J. Neurosci. Methods 134, 9-21. doi: 10.1016/j.jneumeth.2003.10.009
21. Donchin, E., Kubovy, M., Kutas, M., Johnson, R., and Herning, R. I. (1973). Graded changes in evoked response (P300) amplitude as a function of cognitive activity. Percept. Psychophys. 14, 319-324. doi: 10.3758/bf03212398
22. Fabiani, M., Karis, D., and Donchin, E. (1990). Effect mnemonic strategy manipulation in a Von Restorff paradigm. Electroencephalogr. Clin. Neurophysiol. 75, 22-35. doi: 10.1016/0013-4694(90)90149-e
23. Garcea, F. E., Dombovy, M., and Mahon, B. Z. (2013). Preserved tool knowledge in the context of impaired action knowledge: implications for models of semantic memory. Front. Hum. Neurosci. 7:120. doi: 10.3389/fnhum.2013.00120
24. Gentilucci, M., and Gangitano, M. (1998). Influence of automatic word reading on motor control. Eur. J. Neurosci. 10, 752-756. doi: 10.1046/j.1460-9568.1998.00060.x
25. Gibson, J. J. (1971). The information available in pictures. Leonardo 4, 27-35. doi: 10.2307/1572228
26. Gibson, J. J. (1977). “The theory of affordances,” in Perceiving, Acting and Knowing: Toward an Ecological Psychology, eds R. Shaw and J. Bransford (Hillsdale, NJ: Lawrence Erlbaum Associates), 67-82.
27. Gibson, J. J. (1979). The Ecological Approach to Visual Perception. Boston, MA: Houghton Mifflin.
28. Glover, S., Rosenbaum, D. A., Graham, J., and Dixon, P. (2004). Grasping the meaning of words. Exp. Brain Res. 154, 103-108. doi: 10.1007/s00221-003-1659-2
29. Green, J. B., Bialy, Y., Sora, E., and Thatcher, R. W. (1997). An electroencephalographic study of imagined movement. Arch. Phys. Med. Rehabil. 78, 578-581. doi: 10.1016/s0003-9993(97)90421-4
30. Handy, T. C., Grafton, S. T., Shroff, N. M., Ketay, S., and Gazzaniga, M. S. (2003). Graspable objects grab attention when the potential for action is recognized. Nat. Neurosci. 6, 421-427. doi: 10.1038/nn1031
31. Johnson-Frey, S. H. (2004). The neural bases of complex tool use in humans. Trends Cogn. Sci. 8, 71-78. doi: 10.1016/j.tics.2003.12.002
32. Jung, T.-P., Makeig, S., Humphries, C., Lee, T.-W., McKeown, M. J., Iragui, V., et al. (2000). Removing electroencephalographic artifacts by blind source separation. Psychophysiology 37, 163-178. doi: 10.1111/1469-8986.3720163
33. Just, M. A., Cherkassky, V. L., Aryal, S., and Mitchell, T. M. (2010). The neurosemantic theory of concrete noun representations based on the underlying brain codes. PLoS One 5:e8622. doi: 10.1371/journal.pone.0008622
34. 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
35. Kappenman, E. S., and Luck, S. J. (2010). The effects of electrode impedance on data quality and statistical significance in ERP recordings. Psychophysiology 47, 888-904. doi: 10.1111/j.1469-8986.2010.01009.x
36. Karis, D., Fabiani, M., and Donchin, E. (1984). “P300” and memory: individual differences in the von Restorff effect. Cogn. Psychol. 16, 177-216. doi: 10.1016/0010-0285(84)90007-0
37. Kellenbach, M. L., Brett, M., and Patterson, K. (2003). Actions speak louder than functions: the importance of manipulability and action in tool representation. J. Cogn. Neurosci. 15, 30-46. doi: 10.1162/089892903321107800
38. Kennedy, J. M. (1974). A Psychology of Picture Perception. San Francisco, CA: Jossey-Bass Publishers.
39. Kok, A. (2001). On the utility of P3 amplitude as a measure of processing capacity. Psychophysiology 38, 557-577. doi: 10.1017/s0048577201990559
40. Kutas, M., and Donchin, E. (1974). Studies of squeezing: handedness, responding hand, response force and asymmetry of readiness potential. Science 186, 545-548. doi: 10.1126/science.186.4163.545
41. Kutas, M., McCarthy, G., and Donchin, E. (1977). Augmenting mental chronometry: the P300 as a measure of stimulus evaluation time. Science 197, 792-795. doi: 10.1126/science.887923
42. 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
43. Luu, P., and Ferree, T. (2005). Determination of the Hydrocel Geodesic Sensor Nets’ Average Electrode Positions and their 10-10 International Equivalents (Technical Report). Eugene, OR: Electrical Geodesics, Inc.
44. Madan, C. R., and Singhal, A. (2012a). Motor imagery and higher-level cognition: four hurdles before research can sprint forward. Cogn. Process. 13, 211-229. doi: 10.1007/s10339-012-0438-z
45. Madan, C. R., and Singhal, A. (2012b). Encoding the world around us: motor-related processing influences verbal memory. Conscious. Cogn. 21, 1563-1570. doi: 10.1016/j.concog.2012.07.006
46. Mahon, B. Z., and Caramazza, A. (2009). Concepts and categories: a cognitive neuropsychological perspective. Annu. Rev. Psychol. 60, 27-51. doi: 10.1146/annurev.psych.60.110707.163532
47. Makris, S. (2015). A commentary: viewing photos and reading nouns of natural graspable objects similarly modulate motor responses. Front. Hum. Neurosci. 9:337. doi: 10.3389/fnhum.2015.00337
48. Marino, B. F., Sirianni, M., Dalla Volta, R., Magliocco, F., Silipo, F., Quattrone, A., et al. (2014). Viewing photos and reading nouns of natural graspable objects similarly modulate motor responses. Front. Hum. Neurosci. 8:968. doi: 10.3389/fnhum.2014.00968
49. Matheson, H. E., White, N. C., and McMullen, P. A. (2014a). A test of the embodied simulation theory of object perception: potentiation of responses to artifacts and animals. Psychol. Res. 78, 465-482. doi: 10.1007/s00426-013-0502-z
50. Matheson, H. E., White, N., and McMullen, P. A. (2014b). Testing the embodied account of object naming: a concurrent motor task affects naming artifacts and animals. Acta Psychol. (Amst) 145, 33-43. doi: 10.1016/j.actpsy.2013.10.012
51. McCarthy, G., and Donchin, E. (1976). The effects of temporal and event uncertainty in determining the waveforms of the auditory event related potential (ERP). Psychophysiology 13, 581-590. doi: 10.1111/j.1469-8986.1976.tb00885.x
52. McCarthy, G., and Wood, C. C. (1985). Scalp distributions of event-related potentials: an ambiguity associated with analysis of variance models. Electroencephalogr. Clin. Neurophysiol. 62, 203-208. doi: 10.1016/0168-5597(85)90015-2
53. Mengotti, P., Corradi-Dell’Acqua, C., Negri, G. A., Ukmar, M., Pesavento, V., and Rumiati, R. I. (2013). Selective imitation impairments differentially interact with language processing. Brain 136, 2602-2618. doi: 10.1093/brain/awt194
54. Mon-Williams, M., and Bingham, G. P. (2011). Discovering affordances that determine the spatial structure of reach-to-grasp movements. Exp. Brain Res. 211, 145-160. doi: 10.1007/s00221-011-2659-2
55. Oldfield, R. C. (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97-113. doi: 10.1016/0028-3932(71)90067-4
56. Osiurak, F. (2014). What neuropsychology tells us about human tool use? The four constraints theory (4CT): mechanics, space, time and effort. Neuropsychol. Rev. 24, 88-115. doi: 10.1007/s11065-014-9260-y
57. Palombo, D. J., and Madan, C. R. (2015). Making memories that last. J. Neurosci. 35, 10643-10644. doi: 10.1523/JNEUROSCI.1882-15.2015
58. Papeo, L., Lingnau, A., Agosta, S., Pascual-Leone, A., Battelli, L., and Caramazza, A. (2015). The origin of word-related motor activity. Cereb. Cortex 25, 1668-1675. doi: 10.1093/cercor/bht423
59. Polich, J. (2012). “Neuropsychology of P300,” in Oxford Handbook of Event-Related Potential Components, eds S. J. Luck and E. S. Kappenman (New York, NY: Oxford University Press), 159-188.
60. Prinzel, L. J., Freeman, F. G., Scerbo, M. W., Mikulka, P. J., and Pope, A. T. (2003). Effects of a psychophysiological system for adaptive automation on performance, workload and the event-related potential P300 component. Hum. Factors 45, 601-613. doi: 10.1518/hfes.45.4.601.27092
61. Proverbio, A. M., Adorni, R., and D’Aniello, G. E. (2011). 250 ms to code for action affordance during observation of manipulable objects. Neuropsychologia 49, 2711-2717. doi: 10.1016/j.neuropsychologia.2011.05.019
62. Proverbio, A. M., Del Zotto, M., and Zani, A. (2007). The emergence of semantic categorization in early visual processing: ERP indices of animal vs. artifact recognition. BMC Neurosci. 8:24. doi: 10.1186/1471-2202-8-24
63. Pulvermüller, F., Hauk, O., Nikulin, V. V., and Ilmoniemi, R. J. (2005). Functional links between motor and language systems. Eur. J. Neurosci. 21, 793-797. doi: 10.1111/j.1460-9568.2005.03900.x
64. Ramoser, H., Müller-Gerking, J., and Pfurtscheller, G. (2000). Optimal spatial filtering of single trial EEG during imagined hand movement. IEEE Trans. Rehabil. Eng. 8, 441-446. doi: 10.1109/86.895946
65. Reilly, J., Harnish, S., Garcia, A., Hung, J., Rodriguez, A. D., and Crosson, B. (2014). Lesion symptom mapping of manipulable object naming in nonfluent aphasia: can a brain be both embodied and disembodied? Cogn. Neuropsychol. 31, 287-312. doi: 10.1080/02643294.2014.914022
66. Righi, S., Orlando, V., and Marzi, T. (2014). Attractiveness and affordance shape tools neural coding: insight from ERPs. Int. J. Psychophysiol. 91, 240-253. doi: 10.1016/j.ijpsycho.2014.01.003
67. Ruchkin, D. S., Johnson, R. Jr., Mahaffey, D., and Sutton, S. (1988). Towards a functional categorization of slow waves. Psychophysiology 25, 339-353. doi: 10.1111/j.1469-8986.1988.tb01253.x
68. Ruchkin, D. S., Sutton, S., Kietzman, M. L., and Silver, K. (1980). Slow wave and P300 in signal detection. Electroencephalogr. Clin. Neurophysiol. 50, 35-47. doi: 10.1016/0013-4694(80)90321-1
69. Rueschemeyer, S.-A., van Rooij, D., Lindemann, O., Willems, R. M., and Bekkering, H. (2010). The function of words: distinct neural correlates for words denoting differently manipulable objects. J. Cogn. Neurosci. 22, 1844-1851. doi: 10.1162/jocn.2009.21310
70. Saccuman, M. C., Cappa, S. F., Bates, E. A., Arévalo, A., Della Rosa, P., Danna, M., et al. (2006). The impact of semantic reference on word class: an fMRI study of action and object naming. Neuroimage 32, 1865-1878. doi: 10.1016/j.neuroimage.2006.04.179
71. Salmon, J. P., Matheson, H. E., and McMullen, P. A. (2014a). Slow categorization but fast naming for photographs of manipulable objects. Vis. Cogn. 22, 141-172. doi: 10.1080/13506285.2014.887042
72. Salmon, J. P., Matheson, H. E., and McMullen, P. A. (2014b). Photographs of manipulable objects are named more quickly than the same objects depicted as line-drawings: evidence that photographs engage embodiment more than line-drawings. Front. Psychol. 5:1187. doi: 10.3389/fpsyg.2014.01187
73. Salmon, J. P., McMullen, P. A., and Filliter, J. H. (2010). Norms for two types of manipulability (graspability and functional usage), familiarity and age of acquisition for 320 photographs of objects. Behav. Res. Methods 42, 82-95. doi: 10.3758/brm.42.1.82
74. Schupp, H. T., Flaisch, T., Stockburger, J., and Junghöfer, M. (2006). Emotion and attention: event-related brain potential studies. Prog. Brain Res. 156, 31-51. doi: 10.1016/s0079-6123(06)56002-9
75. Schwartz, M. F., Kimberg, D. Y., Walker, G. M., Brecher, A., Faseyitan, O. K., Dell, G. S., et al. (2011). Neuroanatomical dissociation for taxonomic and thematic knowledge in the human brain. Proc. Natl. Acad. Sci. U S A 108, 8520-8524. doi: 10.1073/pnas.1014935108
76. Shebani, Z., and Pulvermüller, F. (2013). Moving the hands and feet specifically impairs working memory for arm-and leg-related action words. Cortex 49, 222-231. doi: 10.1016/j.cortex.2011.10.005
77. Sim, E. J., and Kiefer, M. (2005). Category-related brain activity to natural categories is associated with the retrieval of visual features: evidence from repetition effects during visual and functional judgments. Brain Res. Cogn. Brain Res. 24, 260-273. doi: 10.1016/j.cogbrainres.2005.02.006
78. Smulders, F. T., and Miller, J. O. (2012). “The lateralized readiness potential,” in Oxford Handbook of Event-Related Potential Components, eds S. J. Luck and E. S. Kappenman (New York, NY: Oxford University Press), 209-229.
79. Snow, J. C., Pettypiece, C. E., McAdam, T. D., McLean, A. D., Stroman, P. W., Goodale, M. A., et al. (2011). Bringing the real world into the fMRI scanner: repetition effects for pictures versus real objects. Sci. Rep. 1:130. doi: 10.1038/srep00130
80. Soltani, M., and Knight, R. T. (2000). Neural origins of the P300. Crit. Rev. Neurobiol. 14, 199-224. doi: 10.1615/CritRevNeurobiol.v14.i3-4.20
81. Spunt, R. P., Satpute, A. B., and Lieberman, M. D. (2011). Identifying the what, why and how of an observed action: an fMRI study of mentalizing and mechanizing during action observation. J. Cogn. Neurosci. 23, 63-74. doi: 10.1162/jocn.2010.21446
82. Squires, S. D., Macdonald, S. N., Culham, J. C., and Snow, J. C. (2016). Priming tool actions: are real objects more effective primes than pictures? Exp. Brain Res. 234, 963-976. doi: 10.1007/s00221-015-4518-z
83. Squires, N. K., Squires, K. C., and Hillyard, S. A. (1975). Two varieties of long-latency positive waves evoked by unpredictable auditory stimuli in man. Electroencephalogr. Clin. Neurophysiol. 38, 387-401. doi: 10.1016/0013-4694(75)90263-1
84. Tsagkaridis, K., Watson, C., Jax, S., and Buxbaum, L. (2014). The role of action representations in thematic object relations. Front. Hum. Neurosci. 8:140. doi: 10.3389/fnhum.2014.00140
85. Tucker, M., and Ellis, R. (1998). On the relations between seen objects and components of potential actions. J. Exp. Psychol. Hum. Percept. Perform. 24, 830-846. doi: 10.1037/0096-1523.24.3.830
86. Wamain, Y., Pluciennicka, E., and Kalénine, S. (2014). Temporal dynamics of action perception: differences on ERP evoked by object-related and non-object-related actions. Neuropsychologia 63, 249-258. doi: 10.1016/j.neuropsychologia.2014.08.034
87. Williams, L. M., Kemp, A. H., Felmingham, K., Liddell, B. J., Palmer, D. M., and Bryant, R. A. (2007). Neural biases to covert and overt signals of fear: dissociation by trait anxiety and depression. J. Cogn. Neurosci. 19, 1595-1608. doi: 10.1162/jocn.2007.19.10.1595
88. Wilson, A. D., and Golonka, S. (2013). Embodied cognition is not what you think it is. Front. Psychol. 4:58. doi: 10.3389/fpsyg.2013.00058
89. Witt, J. K., Kemmerer, D., Linkenauger, S. A., and Culham, J. (2010). A functional role for motor simulation in identifying tools. Psychol. Sci. 21, 1215-1219. doi: 10.1177/0956797610378307
90. Wolk, D. A., Coslett, H. B., and Glosser, G. (2005). The role of sensory-motor information in object recognition: evidence from category-specific visual agnosia. Brain Lang. 94, 131-146. doi: 10.1016/j.bandl.2004.10.015