Extensive video-game experience alters cortical networks for complex visuomotor transformations

Cortex

Volumn 46, Issue 9, 2010, Pages 1165-1177

  Granek, Joshua A ^a,b   Gorbet, Diana J ^c   Sergio, Lauren E ^a,b  

^a YORK UNIVERSITY   (Canada)

^b YORK UNIVERSITY   (Canada)

^c UNIVERSITY OF WATERLOO   (Canada)

Author keywords

Eye hand coordination; FMRI; Human cortex; Reaching; Skill

Indexed keywords

ADULT; ARTICLE; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; MALE; NERVE CELL NETWORK; NORMAL HUMAN; PARIETAL LOBE; PREFRONTAL CORTEX; PREMOTOR CORTEX; RECREATION; SENSORIMOTOR CORTEX; VISUAL SYSTEM FUNCTION; VISUOMOTOR COORDINATION;

ADAPTATION, PHYSIOLOGICAL; ADULT; ATTENTION; CASE-CONTROL STUDIES; CEREBRAL CORTEX; HUMANS; LEARNING; MAGNETIC RESONANCE IMAGING; MALE; MOTOR SKILLS; NEUROPSYCHOLOGICAL TESTS; PSYCHOMOTOR PERFORMANCE; REACTION TIME; VIDEO GAMES; VISUAL PERCEPTION;

EID: 77956474733     PISSN: 00109452     EISSN: 00109452     Source Type: Journal    
DOI: 10.1016/j.cortex.2009.10.009     Document Type: Article

References (79)

1. Barberi E.A., Gati J.S., Rutt B.K., Menon R.S. A transmit-only/receive-only (TORO) RF system for high-field MRI/MRS applications. Magnetic Resonance in Medicine 2000, 43:284-289.
2. Batista A.P., Buneo C.A., Snyder L.H., Andersen R.A. Reach plans in eye-centered coordinates. Science 1999, 285:257-260.
3. Battaglia-Mayer A., Ferraina S., Genovesio A., Marconi B., Squatrito S., Molinari M., et al. Eye-hand coordination during reaching. II. An analysis of the relationships between visuomanual signals in parietal cortex and parieto-frontal association projections. Cerebral Cortex 2001, 11:528-544.
4. Bertolino A., Fazio L., Di Giorgio A., Blasi G., Romano R., Taurisano P., et al. Genetically determined interaction between the dopamine transporter and the D2 receptor on prefronto-striatal activity and volume in humans. Journal of Neuroscience 2009, 29:1224-1234.
5. Beurze S.M., de Lange F.P., Toni I., Medendorp W.P. Integration of target and effector information in the human brain during reach planning. Journal of Neurophysiology 2007, 97:188-199.
6. Blangero A., Ota H., Rossetti Y., Fujii T., Ohtake H., Tabuchi M., et al. Systematic retinotopic reaching error vectors in unilateral optic ataxia. Cortex 2010, 46(1):77-93.
7. Bo J., Contreras-Vidal J.L., Kagerer F.A., Clark J.E. Effects of increased complexity of visuo-motor transformations on children's arm movements. Human Movement Science 2006, 25:553-567.
8. Boussaoud D., Jouffrais C., Bremmer F. Eye position effects on the neuronal activity of dorsal premotor cortex in the macaque monkey. Journal of Neurophysiology 1998, 80:1132-1150.
9. Brass M., von Cramon D.Y. The role of the frontal cortex in task preparation. Cerebral Cortex 2002, 12:908-914.
10. Buckner R.L., Sepulcre J., Talukdar T., Krienen F.M., Liu H., Hedden T., et al. Cortical hubs revealed by intrinsic functional connectivity: Mapping, assessment of stability, and relation to Alzheimer's disease. Journal of Neuroscience 2009, 29:1860-1873.
11. Buxbaum L.J., Kyle K., Grossman M., Coslett H.B. Left inferior parietal representations for skilled hand-object interactions: Evidence from stroke and corticobasal degeneration. Cortex 2007, 43:411-423.
12. Caminiti R., Ferraina S., Johnson P.B. The sources of visual information to the primate frontal lobe: A novel role for the superior parietal lobule. Cerebral Cortex 1996, 6:319-328.
13. Cavina-Pratesi C., Valyear K.F., Culham J.C., Kohler S., Obhi S.S., Marzi C.A., et al. Dissociating arbitrary stimulus-response mapping from movement planning during preparatory period: Evidence from event-related functional magnetic resonance imaging. Journal of Neuroscience 2006, 26:2704-2713.
14. Carey D.P., Coleman R.J., Della Sala S. Magnetic misreaching. Cortex 1997, 33:639-652.
15. Clavagnier S., Prado J., Kennedy H., Perenin M.T. How humans reach: Distinct cortical systems for central and peripheral vision. Neuroscientist 2007, 13:22-27.
16. Connolly J.D., Goodale M.A., Desouza J.F., Menon R.S., Vilis T. A comparison of frontoparietal fMRI activation during anti-saccades and anti-pointing. Journal of Neurophysiology 2000, 84:1645-1655.
17. Crammond D.J., Kalaska J.F. Modulation of preparatory neuronal activity in dorsal premotor cortex due to stimulus-response compatibility. Journal of Neurophysiology 1994, 71:1281-1284.
18. Debaere F., Wenderoth N., Sunaert S., Van Hecke P., Swinnen S.P. Changes in brain activation during the acquisition of a new bimanual coordination task. Neuropsychologia 2004, 42:855-867.
19. Derrfuss J., Brass M., von Cramon D.Y. Cognitive control in the posterior frontolateral cortex: Evidence from common activations in task coordination, interference control, and working memory. NeuroImage 2004, 23:604-612.
20. Doyon J., Laforce R., Bouchard G., Gaudreau D., Roy J., Poirier M., et al. Role of the striatum, cerebellum and frontal lobes in the automatization of a repeated visuomotor sequence of movements. Neuropsychologia 1998, 36:625-641.
21. Durston S., Fossella J.A., Casey B.J., Hulshoff Pol H.E., Galvan A., Schnack H.G., et al. Differential effects of DRD4 and DAT1 genotype on fronto-striatal gray matter volumes in a sample of subjects with attention deficit hyperactivity disorder, their unaffected siblings, and controls. Molecular Psychiatry 2005, 10:678-685.
22. Gallivan J.P., Cavina-Pratesi C., Culham J.C. Is that within reach? fMRI reveals that the human superior parieto-occipital cortex encodes objects reachable by the hand. Journal of Neuroscience 2009, 29:4381-4391.
23. Ghilardi M.F., Alberoni M., Marelli S., Rossi M., Franceschi M., Ghez C., et al. Impaired movement control in Alzheimer's disease. Neuroscience Letters 1999, 260:45-48.
24. Gielen C.C., van den Heuvel P.J., van Gisbergen J.A. Coordination of fast eye and arm movements in a tracking task. Experimental Brain Research 1984, 56:154-161.
25. Gorbet D.J., Sergio L.E. Preliminary sex differences in human cortical BOLD fMRI activity during the preparation of increasingly complex visually guided movements. European Journal of Neuroscience 2007, 25:1228-1239.
26. Gorbet D.J., Staines W.R., Sergio L.E. Brain mechanisms for preparing increasingly complex sensory to motor transformations. NeuroImage 2004, 23:1100-1111.
27. Hagmann P., Cammoun L., Gigandet X., Meuli R., Honey C.J., Wedeen V.J., et al. Mapping the structural core of human cerebral cortex. PLoS Biology 2008, 6:e159.
28. Haier R.J., Siegel B.V., MacLachlan A., Soderling E., Lottenberg S., Buchsbaum M.S. Regional glucose metabolic changes after learning a complex visuospatial/motor task: A positron emission tomographic study. Brain Research 1992, 570:134-143.
29. Haslinger B., Erhard P., Altenmuller E., Hennenlotter A., Schwaiger M., Grafin von Einsiedel H., et al. Reduced recruitment of motor association areas during bimanual coordination in concert pianists. Human Brain Mapping 2004, 22:206-215.
30. Hoeft F., Watson C.L., Kesler S.R., Bettinger K.E., Reiss A.L. Gender differences in the mesocorticolimbic system during computer game-play. Journal of Psychiatric Research 2008, 42:253-258.
31. Hornak J., O'Doherty J., Bramham J., Rolls E.T., Morris R.G., Bullock P.R., et al. Reward-related reversal learning after surgical excisions in orbito-frontal or dorsolateral prefrontal cortex in humans. Journal of Cognitive Neuroscience 2004, 16:463-478.
32. Hoshi E., Tanji J. Differential involvement of neurons in the dorsal and ventral premotor cortex during processing of visual signals for action planning. Journal of Neurophysiology 2006, 95:3596-3616.
33. Jackson S.R., Newport R., Mort D., Husain M. Where the eye looks, the hand follows; limb-dependent magnetic misreaching in optic ataxia. Current Biology 2005, 15:42-46.
34. Jancke L., Shah N.J., Peters M. Cortical activations in primary and secondary motor areas for complex bimanual movements in professional pianists. Cognitive Brain Research 2000, 10:177-183.
35. Jenkins I.H., Brooks D.J., Nixon P.D., Frackowiak R.S., Passingham R.E. Motor sequence learning: A study with positron emission tomography. Journal of Neuroscience 1994, 14:3775-3790.
36. Johnson M.T., Coltz J.D., Ebner T.J. Encoding of target direction and speed during visual instruction and arm tracking in dorsal premotor and primary motor cortical neurons. European Journal of Neuroscience 1999, 11:4433-4445.
37. Johnson-Frey S.H., Newman-Norlund R., Grafton S.T. A distributed left hemisphere network active during planning of everyday tool use skills. Cerebral Cortex 2005, 15:681-695.
38. Karnath H.O., Ferber S., Himmelbach M. Spatial awareness is a function of the temporal not the posterior parietal lobe. Nature 2001, 411:950-953.
39. Khan A.Z., Crawford J.D., Blohm G., Urquizar C., Rossetti Y., Pisella L. Influence of initial hand and target position on reach errors in optic ataxic and normal subjects. Journal of Vision 2007, 7:1-16.
40. Koch G., Franca M., Del Olmo M.F., Cheeran B., Milton R., Alvarez Sauco M., et al. Time course of functional connectivity between dorsal premotor and contralateral motor cortex during movement selection. Journal of Neuroscience 2006, 26:7452-7459.
41. Krings T., Topper R., Foltys H., Erberich S., Sparing R., Willmes K., et al. Cortical activation patterns during complex motor tasks in piano players and control subjects. A functional magnetic resonance imaging study. Neuroscience Letters 2000, 278:189-193.
42. Kurata K. Site of origin of projections from the thalamus to dorsal versus ventral aspects of the premotor cortex of monkeys. Neuroscience Research 1994, 21:71-76.
43. Lacquaniti F., Perani D., Guigon E., Bettinardi V., Carrozzo M., Grassi F., et al. Visuomotor transformations for reaching to memorized targets: A PET study. NeuroImage 1997, 5:129-146.
44. Leung H.C., Cai W. Common and differential ventrolateral prefrontal activity during inhibition of hand and eye movements. Journal of Neuroscience 2007, 27:9893-9900.
45. Lewis J.W., Van Essen D.C. Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey. Journal of Comparative Neurology 2000, 428:112-137.
46. Lewis J.W., Van Essen D.C. Mapping of architectonic subdivisions in the macaque monkey, with emphasis on parieto-occipital cortex. Journal of Comparative Neurology 2000, 428:79-111.
47. Luber B., Kinnunen L.H., Rakitin B.C., Ellsasser R., Stern Y., Lisanby S.H. Facilitation of performance in a working memory task with rTMS stimulation of the precuneus: Frequency- and time-dependent effects. Brain Research 2007, 1128:120-129.
48. Marzocchi N., Breveglieri R., Galletti C., Fattori P. Reaching activity in parietal area V6A of macaque: Eye influence on arm activity or retinocentric coding of reaching movements?. European Journal of Neuroscience 2008, 27:775-789.
49. Matsuda G., Hiraki K. Sustained decrease in oxygenated hemoglobin during video games in the dorsal prefrontal cortex: A NIRS study of children. NeuroImage 2006, 29:706-711.
50. Moll J., de Oliveira-Souza R., Passman L.J., Cunha F.C., Souza-Lima F., Andreiuolo P.A. Functional MRI correlates of real and imagined tool-use pantomimes. Neurology 2000, 54:1331-1336.
51. Murray E.A., Bussey T.J., Wise S.P. Role of prefrontal cortex in a network for arbitrary visuomotor mapping. Experimental Brain Research 2000, 133:114-129.
52. Nagamitsu S., Nagano M., Yamashita Y., Takashima S., Matsuishi T. Prefrontal cerebral blood volume patterns while playing video games - a near-infrared spectroscopy study. Brain Development 2006, 28:315-321.
53. Neggers S.F., Bekkering H. Gaze anchoring to a pointing target is present during the entire pointing movement and is driven by a non-visual signal. Journal of Neurophysiology 2001, 86:961-970.
54. Neggers S.F., Bekkering H. Ocular gaze is anchored to the target of an ongoing pointing movement. Journal of Neurophysiology 2000, 83:639-651.
55. Norton A., Winner E., Cronin K., Overy K., Lee D.J., Schlaug G. Are there pre-existing neural, cognitive, or motoric markers for musical ability?. Brain and Cognition 2005, 59:124-134.
56. Obayashi S., Suhara T., Kawabe K., Okauchi T., Maeda J., Akine Y., et al. Functional brain mapping of monkey tool use. NeuroImage 2001, 14:853-861.
57. Ogiso T., Kobayashi K., Sugishita M. The precuneus in motor imagery: A magnetoencephalographic study. NeuroReport 2000, 11:1345-1349.
58. Oldfield R.C. The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia 1971, 9:97-113.
59. Petrides M., Pandya D.N. Dorsolateral prefrontal cortex: Comparative cytoarchitectonic analysis in the human and macaque brain and corticocortical connection patterns. European Journal of Neuroscience 1999, 11:1011-1036.
60. Piaget J. The Construction of Reality in the Child 1965, Basic Books, Inc., New York.
61. Picard N., Strick P.L. Imaging the premotor areas. Current Opinion in Neurobiology 2001, 11:663-672.
62. Pisella L., Binkofski F., Lasek K., Toni I., Rossetti Y. No double-dissociation between optic ataxia and visual agnosia: Multiple sub-streams for multiple visuo-manual integrations. Neuropsychologia 2006, 44:2734-2748.
63. Prado J., Clavagnier S., Otzenberger H., Scheiber C., Kennedy H., Perenin M.T. Two cortical systems for reaching in central and peripheral vision. Neuron 2005, 48:849-858.
64. Rowe J., Hughes L., Eckstein D., Owen A.M. Rule-selection and action-selection have a shared neuroanatomical basis in the human prefrontal and parietal cortex. Cerebral Cortex 2008, 18:2275-2285.
65. Rushworth M.F., Buckley M.J., Gough P.M., Alexander I.H., Kyriazis D., McDonald K.R., et al. Attentional selection and action selection in the ventral and orbital prefrontal cortex. Journal of Neuroscience 2005, 25:11628-11636.
66. Saito N., Mushiake H., Sakamoto K., Itoyama Y., Tanji J. Representation of immediate and final behavioral goals in the monkey prefrontal cortex during an instructed delay period. Cerebral Cortex 2005, 15:1535-1546.
67. Sakai K., Hikosaka O., Miyauchi S., Takino R., Sasaki Y., Putz B. Transition of brain activation from frontal to parietal areas in visuomotor sequence learning. Journal of Neuroscience 1998, 18:1827-1840.
68. Shadmehr R., Holcomb H.H. Neural correlates of motor memory consolidation. Science 1997, 277:821-825.
69. Shen L., Alexander G.E. Preferential representation of instructed target location versus limb trajectory in dorsal premotor area. Journal of Neurophysiology 1997, 77:1195-1212.
70. Smith M.E., McEvoy L.K., Gevins A. Neurophysiological indices of strategy development and skill acquisition. Cognitive Brain Research 1999, 7:389-404.
71. Snyder L.H., Batista A.P., Andersen R.A. Saccade-related activity in the parietal reach region. Journal of Neurophysiology 2000, 83:1099-1102.
72. Tachibana Y., Nambu A., Hatanaka N., Miyachi S., Takada M. Input-output organization of the rostral part of the dorsal premotor cortex, with special reference to its corticostriatal projection. Neuroscience Research 2004, 48:45-57.
73. Tippett W.J., Sergio L.E. Visuomotor integration is impaired in early stage Alzheimer's disease. Brain Research 2006, 1102:92-102.
74. Tippett W.J., Krajewski A., Sergio L.E. Visuomotor integration is compromised in Alzheimer's disease patients reaching for remembered targets. European Neurology 2007, 58:1-11.
75. Tomassini V., Jbabdi S., Klein J.C., Behrens T.E., Pozzilli C., Matthews P.M., et al. 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 2007, 27:10259-10269.
76. Toni I., Thoenissen D., Zilles K. Movement preparation and motor intention. NeuroImage 2001, 14:S110-S117.
77. Trillenberg P., Sprenger A., Petersen D., Kompf D., Heide W., Helmchen C. Functional dissociation of saccade and hand reaching control with bilateral lesions of the medial wall of the intraparietal sulcus: Implications for optic ataxia. NeuroImage 2007, 36:T69-T76.
78. Weinrich M., Wise S.P. The premotor cortex of the monkey. Journal of Neuroscience 1982, 2:1329-1345.
79. Wise S.P., di Pellegrino G., Boussaoud D. The premotor cortex and nonstandard sensorimotor mapping. Canadian Journal of Physiology and Pharmacology 1996, 74:469-482.