The influence of expertise on brain activation of the action observation network during anticipation of tennis and volleyball serves

Frontiers in Human Neuroscience

Volumn 8, Issue AUG, 2014, Pages

  Balser, Nils ^a   Lorey, Britta ^a   Pilgramm, Sebastian ^a   Naumann, Tim ^a   Kindermann, Stefan ^a   Stark, Rudolf ^a   Zentgraf, Karen ^a,b   Williams, A Mark ^c   Munzert, Jörn ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c BRUNEL UNIVERSITY   (United Kingdom)

Author keywords

Cerebellum; Functional magnetic resonance imaging; Motor expertise; Sports related anticipation; Superior parietal lobe

Indexed keywords

ACTION OBSERVATION NETWORK; ADULT; ANTICIPATION; ARTICLE; CEREBELLUM CORTEX; CONTROLLED STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; MALE; MOTOR CONTROL; MOVEMENT PERCEPTION; NERVE CELL NETWORK; NORMAL HUMAN; SENSORIMOTOR FUNCTION; SUPERIOR PARIETAL LOBULE; SUPPLEMENTARY MOTOR AREA; TASK PERFORMANCE; TENNIS; VOLLEYBALL;

EID: 84905258136     PISSN: None     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2014.00568     Document Type: Article

References (82)

1. Abernethy, B., Gill, D. P., Parks, S. L., and Packer, S. T. (2001). Expertise and the perception of kinematic and situational probability information. Perception 30, 233-252. doi: 10.1068/p2872.
2. Abernethy, B., and Russell, D. G. (1987). The relationship between expertise and visual search strategy in a racquet sport. Hum. Mov. Sci. 6, 283-319.
3. Abreu, A. M., Macaluso, E., Azevedo, R. T., Cesari, P., Urgesi, C., and Aglioti, S. M. (2012). Action anticipation beyond the action observation network: a functional magnetic resonance imaging study in expert basketball players. Eur. J. Neurosci. 35, 1646-1654. doi: 10.1111/j.1460-9568.2012.08104.x
4. Aglioti, S. M., Cesari, P., Romani, M., and Urgesi, C. (2008). Action anticipation and motor resonance in elite basketball players. Nat. Neurosci. 11, 1109-1116. doi: 10.1038/nn.2182
5. Avenanti, A., Annella, L., Candidi, M., Urgesi, C., and Aglioti, S. M. (2013). Compensatory plasticity in the action observation network: virtual lesions of STS enhance anticipatory simulation of seen actions. Cereb. Cortex 23, 570-580 doi: 10.1093/cercor/bhs040
6. Balser, N., Lorey, B., Pilgramm, S., Stark, R., Bischoff, M., Zentgraf, K., et al. (2014). Prediction of human actions: expertise and task-related effects on neural activation of the action observation network. Hum. Brain Mapp. 35, 4016-4034. doi: 10.1002/hbm.22455
7. Bastian, A. J. (2006). Learning to predict the future: the cerebellum adapts feedforward movement control. Curr. Opin. Neurobiol. 16, 645-649. doi: 10.1016/j.conb.2006.08.016
8. Bishop, D. T., Wright, M. J., Jackson, R. C., and Abernethy, B. (2013). Neural bases for anticipation skill in soccer: an FMRI study. J. Sport Exerc. Psychol. 35, 98-109.
9. Bosch, S. E., Neggers, S. F. W., and van der Stigchel, S. (2013). The role of the frontal eye fields in oculomotor competition: image-guided TMS enhances contralateral target selection. Cereb. Cortex 23, 824-832. doi: 10.1093/cercor/bhs075
10. Buccino, G., Vogt, S., Ritzl, A., Fink, G. R., Zilles, K., Freund, H.-J., et al. (2004). Neural circuits underlying imitation learning of hand actions: an event-related fMRI study. Neuron 42, 323-334. doi: 10.1016/S0896-6273(04)00181-3
11. Calvo-Merino, B., Grèzes, J., Glaser, D. E., Passingham, R. E., Haggard, P., and Gre, J. (2006). Seeing or doing? Influence of visual and motor familiarity in action observation. Curr. Biol. 16, 1905-1910. doi: 10.1016/j.cub.2006.07.065
12. Cañal-Bruland, R., van Ginneken, W. F., van der Meer, B. R., and Williams, A. M. (2011). The effect of local kinematic changes on anticipation judgments. Hum. Mov. Sci. 30, 495-503. doi: 10.1016/j.humov.2010.10.001
13. Caspers, S., Zilles, K., Laird, A. R., and Eickhoff, S. B. (2010). ALE meta-analysis of action observation and imitation in the human brain. Neuroimage 50, 1148-1167. doi: 10.1016/j.neuroimage.2009.12.112
14. Cerminara, N. L., Apps, R., and Marple-Horvat, D. E. (2009). An internal model of a moving visual target in the lateral cerebellum. J. Physiol. 587, 429-442. doi: 10.1113/jphysiol.2008.163337
15. Corbetta, M., Miezin, F. M., Shulman, G. L., and Petersen, S. E. (1993). A PET study of visuospatial attention. J. Neurosci. 13, 1202-1226.
16. Corbetta, M., and Shulman, G. L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 3, 201-215. doi: 10.1038/nrn755
17. Corbetta, M., Shulman, G. L., Miezin, F. M., and Petersen, S. E. (1995). Superior parietal cortex activation during spatial attention shifts and visual feature conjunction. Science 270, 802-805.
18. Crognier, L., and Féry, Y.-A. (2005). Effect of tactical initiative on predicting passing shots in tennis. Appl. Cogn. Psychol. 19, 637-649. doi: 10.1002/acp.1100
19. Cross, E. S., Hamilton, A. F. C., de Kraemer, D. J. M., Kelley, W. M., and Grafton, S. T. (2009). Sensitivity of the action observation network to physical and observational learning. Cereb. Cortex 19, 315-326. doi: 10.1093/cercor/bhn083
20. Culham, J. C., and Valyear, K. F. (2006). Human parietal cortex in action. Curr. Opin. Neurobiol. 16, 205-212. doi: 10.1016/j.conb.2006.03.005
21. Diedrichsen, J. (2006). A spatially unbiased atlas template of the human cerebellum. Neuroimage 33, 127-138. doi: 10.1016/j.neuroimage.2006.05.056
22. Diedrichsen, J., Balsters, J. H., Flavell, J., Cussans, E., and Ramnani, N. (2009). A probabilistic MR atlas of the human cerebellum. Neuroimage 46, 39-46. doi: 10.1016/j.neuroimage.2009.01.045
23. Diersch, N., Mueller, K., Cross, E. S., Stadler, W., Rieger, M., Schütz-Bosbach, S., et al. (2013). Action prediction in younger versus older adults: Neural correlates of motor familiarity. PLoS ONE 8:e64195. doi: 10.1371/journal.pone.0064195
24. Dimitrova, A., de Greiff, A., Schoch, B., Gerwig, M., Frings, M., Gizewski, E. R., et al. (2006). Activation of cerebellar nuclei comparing finger, foot and tongue movements as revealed by fMRI. Brain Res. Bull. 71, 233-241. doi: 10.1016/j.brainresbull.2006.09.015
25. Eickhoff, S. B., Stephan, K. E., Mohlberg, H., Grefkes, C., Fink, G. R., Amunts, K., et al. (2005). A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25, 1325-1335. doi: 10.1016/j.neuroimage.2004.12.034
26. Fiehler, K., Burke, M., Engel, A., Bien, S., and Rösler, F. (2008). Kinesthetic working memory and action control within the dorsal stream. Cereb. Cortex 18, 243-253. doi: 10.1093/cercor/bhm071
27. Fogassi, L., and Luppino, G. (2005). Motor functions of the parietal lobe. Curr. Opin. Neurobiol. 15, 626-631. doi: 10.1016/j.conb.2005.10.015
28. Friedrich, F. J., Egly, R., Rafal, R. D., and Beck, D. (1998). Spatial attention deficits in humans: a comparison of superior parietal and temporal-parietal junction lesions. Neuropsychology 12, 193-207.
29. Gallagher, H. L., and Frith, C. D. (2004). Dissociable neural pathways for the perception and recognition of expressive and instrumental gestures. Neuropsychologia 42, 1725-1736. doi: 10.1016/j.neuropsychologia.2004.05.006
30. Gazzola, V., and Keysers, C. (2009). The observation and execution of actions share motor and somatosensory voxels in all tested subjects: single-subject analyses of unsmoothed fMRI data. Cereb. Cortex 19, 1239-1255. doi: 10.1093/cercor/bhn181
31. Gazzola, V., Rizzolatti, G., Wicker, B., and Keysers, C. (2007). The anthropomorphic brain: the mirror neuron system responds to human and robotic actions. Neuroimage 35, 1674-1684. doi: 10.1016/j.neuroimage.2007.02.003
32. Gläscher, J. (2009). Visualization of group inference data in functional neuroimaging. Neuroinformatics 7, 73-82. doi: 10.1007/s12021-008-9042-x
33. Grafton, S. T., Arbib, M. A., Fadiga, L., and Rizzolatti, G. (1996). Localization of grasp representations in humans by positron emission tomography. 2. Observation compared with imagination. Exp. Brain Res. 112, 103-111.
34. Grafton, S. T., Mazziotta, J. C., Woods, R. P., and Phelps, M. E. (1992). Human functional anatomy of visually guided finger movements. Brain 115, 565-587.
35. Halligan, P. W., Fink, G. R., Marshall, J. C., and Vallar, G. (2003). Spatial cognition: evidence from visual neglect. Trends Cogn. Sci. 7, 125-133. doi: 10.1016/S1364-6613(03)00032-9
36. Heinen, K., Feredoes, E., Weiskopf, N., Ruff, C. C., and Driver, J. (2013). Direct evidence for attention-dependent influences of the frontal eye-fields on feature-responsive visual cortex. Cereb. Cortex. doi: 10.1093/cercor/bht157. [Epub ahead of print].
37. Hubert, M., and van der Veeken, S. (2008). Outlier detection for skewed data. J. Chemometr. 22, 235-246. doi: 10.1002/cem.1123
38. Huys, R., Smeeton, N. J., Hodges, N. J., Beek, P. J., and Williams, A. M. (2008). On the dynamic information underlying visual anticipation skill. Percept. Psychophys. 70, 1217-1234. doi: 10.3758/PP.70.7.1217
39. Imamizu, H., and Kawato, M. (2008). Neural correlates of predictive and postdictive switching mechanisms for internal models. J. Neurosci. 28, 10751-10765. doi: 10.1523/JNEUROSCI.1106-08.2008
40. Imamizu, H., Miyauchi, S., Tamada, T., Sasaki, Y., Takino, R., Pütz, B., et al. (2000). Human cerebellar activity reflecting an acquired internal model of a new tool. Nature 403, 192-195. doi: 10.1038/35003194
41. McPherson, S. L., and MacMahon, C. (2008). How baseball players prepare to bat: tactical knowledge as a mediator of expert performance in baseball. J. Sport Exerc. Psychol. 30, 755-778.
42. McRobert, A. P., Ward, P., Eccles, D. W., and Williams, A. M. (2011). The effect of manipulating context-specific information on perceptual-cognitive processes during a simulated anticipation task. Brit. J. Psychol. 102, 519-534. doi: 10.1111/j.2044-8295.2010.02013.x
43. Miall, R. C. (2003). Connecting mirror neurons and forward models. Neuroreport 14, 2135-2137. doi: 10.1097/01.wnr.0000098751.87269.77
44. Miall, R. C., and King, D. (2008). State estimation in the cerebellum. Cerebellum 7, 572-576. doi: 10.1007/s12311-008-0072-6
45. Miall, R. C., and Wolpert, D. M. (1996). Forward models for physiological motor control. Neural Networks 9, 1265-1279.
46. Molenberghs, P., Cunnington, R., and Mattingley, J. B. (2012). Brain regions with mirror properties: a meta-analysis of 125 human fMRI studies. Neurosci. Biobehav. Rev. 36, 341-349. doi: 10.1016/j.neubiorev.2011.07.004
47. Oldfield, R. (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97-113.
48. Pardo, J. V., Fox, P. T., and Raichle, M. E. (1991). Localization of a human system for sustained attention by positron emission tomography. Nature 349, 61-64. doi: 10.1038/349061a0
49. Pilgramm, S., Lorey, B., Stark, R., Munzert, J., Vaitl, D., and Zentgraf, K. (2010). Differential activation of the lateral premotor cortex during action observation. BMC Neurosci. 11:89. doi: 10.1186/1471-2202-11-89
50. Posner, M. I., Walker, J. A., Friedrich, F. J., and Rafal, R. D. (1984). Effects of parietal injury on covert orienting of attention. J. Neurosci. 4, 1863-1874.
51. Rizzolatti, G., Fogassi, L., and Gallese, V. (1997). Parietal cortex: from sight to action. Curr. Opin. Neurobiol. 7, 562-567.
52. 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
53. Ronconi, L., Basso, L., Gori, S., and Facoetti, A. (2014). TMS on right frontal eye fields induces an inflexible focus of attention. Cereb. Cortex 24, 396-402. doi: 10.1093/cercor/bhs319
54. Rowe, R. M., and McKenna, F. P. (2001). Skilled anticipation in real-world tasks: measurement of attentional demands in the domain of tennis. J. Exp. Psychol. Appl. 7, 60-67. doi: 10.1037/1076-898X.7.1.60
55. Rushworth, M. F. S., Johansen-Berg, H., Göbel, S. M., and Devlin, J. T. (2003). The left parietal and premotor cortices: motor attention and selection. Neuroimage 20, S89-100. doi: 10.1016/j.neuroimage.2003.09.011
56. Savelsbergh, G. J. P., Williams, A. M., van der Kamp, J., and Ward, P. (2002). Visual search, anticipation and expertise in soccer goalkeepers. J. Sports Sci. 20, 279-287. doi: 10.1080/026404102317284826
57. Schmahmann, J. D., Macmore, J., and Vangel, M. (2009). Cerebellar stroke without motor deficit: clinical evidence for motor and non-motor domains within the human cerebellum. Neuroscience 162, 852-861. doi: 10.1016/j.neuroscience.2009.06.023
58. Schubotz, R. (2007). Prediction of external events with our motor system: towards a new framework. Trends Cogn. Sci. 11, 211-218. doi: 10.1016/j.tics.2007.02.006
59. Singer, R. N., Cauraugh, J. H., Chen, D., and Steinberg, G. M. (1996). Visual search, anticipation, and reactive comparisons between highly-skilled and beginning tennis players. J. Appl. Sport Psychol. 8, 9-26.
60. Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T. E. J., Johansen-Berg, H., et al. (2004). Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23, 208-219. doi: 10.1016/j.neuroimage.2004.07.051
61. Sokolov, A. A., Gharabaghi, A., Tatagiba, M. S., and Pavlova, M. (2010). Cerebellar engagement in an action observation network. Cereb. Cortex 20, 486-491. doi: 10.1093/cercor/bhp117
62. Squire, R. F., Noudoost, B., Schafer, R. J., and Moore, T. (2013). Prefrontal contributions to visual selective attention. Annu. Rev. Neurosci. 36, 451-466. doi: 10.1146/annurev-neuro-062111-150439.
63. Stadler, W., Ott, D. V. M., Springer, A., Schubotz, R. I., Schütz-Bosbach, S., and Prinz, W. (2012). Repetitive TMS suggests a role of the human dorsal premotor cortex in action prediction. Front. Hum. Neurosci. 6:20. doi: 10.3389/fnhum.2012.00020
64. Stadler, W., Schubotz, R. I., von Cramon, D. Y., von Springer, A., Graf, M., and Prinz, W. (2011). Predicting and memorizing observed action: differential premotor cortex involvement. Hum. Brain Mapp. 32, 677-687. doi: 10.1002/hbm.20949
65. Synofzik, M., Lindner, A., and Thier, P. (2008). The cerebellum updates predictions about the visual consequences of one's behavior. Curr. Biol. 18, 814-818. doi: 10.1016/j.cub.2008.04.071
66. Urgesi, C., Maieron, M., Avenanti, A., Tidoni, E., Fabbro, F., and Aglioti, S. M. (2010). Simulating the future of actions in the human corticospinal system. Cereb. Cortex 20, 2511-2521. doi: 10.1093/cercor/bhp292
67. Urgesi, C., Savonitto, M. M., Fabbro, F., and Aglioti, S. M. (2011). Long-and short-term plastic modeling of action prediction abilities in volleyball. Psychol. Res. 76, 542-560. doi: 10.1007/s00426-011-0383-y
68. Vesia, M., Monteon, J. A., Sergio, L. E., and Crawford, J. D. (2006). Hemispheric asymmetry in memory-guided pointing during single-pulse transcranial magnetic stimulation of human parietal cortex. J. Neurophysiol. 96, 3016-3027. doi: 10.1152/jn.00411.2006
69. Williams, A. M., Ford, P. R., Eccles, D. W., and Ward, P. (2011). Perceptual-cognitive expertise in sport and its acquisition: implications for applied cognitive psychology. Appl. Cogn. Psychol. 25, 432-442. doi: 10.1002/acp.1710
70. Williams, A. M., Huys, R., Cañal-Bruland, R., and Hagemann, N. (2009). The dynamical information underpinning anticipation skill. Hum. Mov. Sci. 28, 362-370. doi: 10.1016/j.humov.2008.10.006
71. Williams, A. M., Ward, P., Knowles, J. M., and Smeeton, N. J. (2002). Anticipation skill in a real-world task: measurement, training, and transfer in tennis. J. Exp. Psychol. Appl. 8, 259-270. doi: 10.1037/1076-898X.8.4.259
72. Winstein, C. J., Grafton, S. T., Pohl, P. S., and Angeles, L. (1997). Motor task difficulty and brain activity: investigation of goal-directed reciprocal aiming using positron emission tomography. J. Neurophysiol. 77, 1581-1594.
73. Wolfensteller, U., Schubotz, R. I., and von Cramon, D. Y. (2004). "What" becoming "where": functional magnetic resonance imaging evidence for pragmatic relevance driving premotor cortex. J. Neurosci. 17, 10431-10439. doi: 10.1523/JNEUROSCI.2641-042004
74. Wolpert, D. M., and Flanagan, J. R. (2001). Motor prediction. Curr. Biol. 11, 729-732. doi: 10.1016/S0960-9822(01)00432-8
75. Wolpert, D. M., Goodbody, S. J., and Husain, M. (1998a). Maintaining internal representations: the role of the human superior parietal lobe. Nat. Neurosci. 1, 529-533. doi: 10.1038/2245
76. Wolpert, D. M., Miall, R. C., and Kawato, M. (1998b). Internal models in the cerebellum. Trends Cogn. Sci. 2, 338-347.
77. Worsley, K. (2007). "Random field theory, Chapter 18, " in Statistical Parametric Mapping: The Analysis of Functional Brain Images, eds K. Friston, J. Ashburner, S. Kiebel, T. Nichols, and W. Penny (Amsterdam: Academic Press), 232-236.
78. Wright, M., Bishop, D., Jackson, R., and Abernethy, B. (2011). Cortical fMRI activation to opponents' body kinematics in sport-related anticipation: expert-novice differences with normal and point-light video. Neurosci. Letters 500, 216-221. doi: 10.1016/j.neulet.2011.06.045
79. Wright, M. J., Bishop, D. T., Jackson, R. C., and Abernethy, B. (2010). Functional MRI reveals expert-novice differences during sport-related anticipation. Neuroreport 21, 94-98. doi: 10.1097/WNR.0b013e328333dff2
80. Wright, M. J., and Jackson, R. C. (2007). Brain regions concerned with perceptual skills in tennis: an fMRI study. Int. J. Psychophysiol. 63, 214-220. doi: 10.1016/j.ijpsycho.2006.03.018
81. Yarrow, K., Brown, P., and Krakauer, J. W. (2009). Inside the brain of an elite athlete: the neural processes that support high achievement in sports. Nat. Rev. Neurosci. 10, 585-596. doi: 10.1038/nrn2672
82. Zentgraf, K., Munzert, J., Bischoff, M., and Newman-Norlund, R. D. (2011). Simulation during observation of human actions-theories, empirical studies, applications. Vision Res. 51, 827-835. doi: 10.1016/j.visres.2011.01.007