Enhanced frontoparietal network architectures following "gaze-contingent" versus "free-hand" motor learning

NeuroImage

Volumn 64, Issue 1, 2013, Pages 267-276

  James, David R C ^a   Leff, Daniel R ^a   Orihuela Espina, Felipe ^a   Kwok, Ka Wai ^a   Mylonas, George P ^a   Athanasiou, Thanos ^a   Darzi, Ara W ^a   Yang, Guang Zhong ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Gaze contingent; Graph theory; Longitudinal motor skill learning; Near infrared spectroscopy; Rehabilitation; Surgery

Indexed keywords

ADULT; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN FUNCTION; CEREBELLUM; CONTROLLED STUDY; FEMALE; FREE HAND MOTOR LEARNING; FRONTAL CORTEX; GAZE; GAZE CONTINGENT MOTOR LEARNING; HUMAN; INFRARED SPECTROSCOPY; LEARNING; MALE; MOTOR CORTEX; MOTOR PERFORMANCE; NERVE CELL PLASTICITY; NEUROANATOMY; POSTERIOR PARIETAL CORTEX; PRIORITY JOURNAL; TASK PERFORMANCE;

ADULT; ATTENTION; FEMALE; FIXATION, OCULAR; FRONTAL LOBE; HUMANS; LEARNING; MALE; MOTOR SKILLS; NERVE NET; NEURAL PATHWAYS; PARIETAL LOBE; VOLITION;

EID: 84867453036     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2012.08.056     Document Type: Article

References (64)

1. Achard S., Bullmore E. Efficiency and cost of economical brain functional networks. PLoS Comput. Biol. 2007, 3:174-183.
2. Achard S., Salvador R., Whitcher B., Suckling J., Bullmore E. A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. J. Neurosci. 2006, 26:63-72.
3. Bahrami P., Schweizer T.A., Tam F., Grantcharov T.P., Cusimano M.D., Graham S.J. Functional MRI-compatible laparoscopic surgery training simulator. Magn. Reson. Med. 2011, 65:873-881.
4. Bassett D.S., Bullmore E. Small-world brain networks. Neuroscientist 2006, 12:512-523.
5. Bassett D.S., Bullmore E., Verchinski B.A., Mattay V.S., Weinberger D.R., Meyer-Lindenberg A. Hierarchical organization of human cortical networks in health and schizophrenia. J. Neurosci. 2008, 28:9239-9248.
6. Bassett D.S., Bullmore E.T., Meyer-Lindenberg A., Apud J.A., Wienberger D.R., Coppola R. Cognitive fitness of cost-efficient functional networks. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:11747-11752.
7. Bassett D.S., Wymbs N.F., Porter M.A., Mucha P.J., Carlson J.M., Grafton S.T. Dynamic reconfiguration of human brain networks during learning. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:7641-7646.
8. Bullmore E.T., Bassett D.S. Brain graphs: graphical models of the human brain connectome. Annu. Rev. Clin. Psychol. 2011, 7:113-140.
9. Bullmore E., Sporns O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat. Rev. Neurosci. 2009, 10:186-198.
10. Buneo C.A., Andersen R.A. The posterior parietal cortex: sensorimotor interface for the planning and online control of visually guided movements. Neuropsychologia 2006, 44:2594-2606.
11. Buneo C.A., Jarvis M.R., Batista A.P., Andersen R.A. Direct visuomotor transformations for reaching. Nature 2002, 416:632-636.
12. Chen Z.J., He Y., Rosa-Neto P., Germann J., Evans A.C. Revealing a modular architecture of human brain structural networks by using cortical thickness from MRI. Cereb. Cortex 2008, 18:2374-2381.
13. Coynel D., Marrelec G., Perlbarg V., Pelegrini-Issac M., Van de Moortele P.F., Ugurbil K., Doyon J., Benali H., Lehericy S. Dynamics of motor-related functional integration during motor sequence learning. NeuroImage 2010, 49:759-766.
14. 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.
15. Floyer-Lea A., Matthews P.M. Distinguishable brain activation networks for short- and long-term motor skill learning. J. Neurophysiol. 2005, 94. (5r12-18).
16. Friston K.J., Frith C.D., Liddle P.F., Frackowiak R.S.J. Functional connectivity: the principal-component analysis of large (PET) data sets. J. Cereb. Blood Flow Metab. 1993, 13:5-14.
17. Halsband U., Lange R.K. Motor learning in man: a review of functional and clinical studies. J. Physiol. Paris 2006, 99:414-424.
18. He Y., Chen Z.J., Evans A.C. Small-world anatomical networks in the human brain revealed by cortical thickness from fMRI. Cereb. Cortex 2007, 17:2407-2419.
19. Hitchcock E.M., Warm J.S., Matthews G., Dember W.N., Shear P.K., Tripp L.D., Mayleben D.W., Parasuraman R. Automation cueing modulates cerebral blood flow and vigilance in a simulated air traffic control task. Theor. Issues Ergon. Sci. 2003, 4:89-112.
20. Hoshi Y., Shimada M., Sato C., Iguchi Y. Reevaluation of near-infrared light propagation in the adult human head: implications for functional near-infrared spectroscopy. J. Biomed. Opt. 2005, 10:064032.
21. James D.R.C., Orihuela-Espina F., Leff D.R., Mylonas G.P., Kwok K.W., Darzi A.W., Yang G.Z. Cognitive burden estimation for visuomotor learning with fNIRS. Med. Image Comput. Comput. Assist. Interv. 2010, 13:319-326.
22. James D.R.C., Orihuela-Espina F., Leff D.R., Sodergren M.H., Athanasiou T., Darzi A.W., Yang G.Z. The ergonomics of Natural Orifice Translumenal Endoscopic Surgery (NOTES) in terms of performance, stress and cognitive behaviour. Surgery 2011, 149:525-533.
23. Jurcak V., Tsuzuki D., Dan I. 10/20, 10/10, and 10/5 systems revisited: their validity as relative head-surface-based positioning systems. NeuroImage 2007, 34:1600-1611.
24. Kelly A.M., Garavan H. Human functional neuroimaging of brain changes associated with practice. Cereb. Cortex 2005, 15:1089-1102.
25. Latora V., Marchiori M. Economic small-world behavior in weighted networks. Eur. Phys. J. B 2003, 32:249-263.
26. Lee S.L., Lerotic M., Vitiello V., Giannarou S., Kwok K.W., Visentini-Scarzanella M., Yang G.Z. From medical images to minimally invasive intervention: Computer assistance for robotic surgery. Comput. Med. Imaging Graph. 2010, 34:33-45.
27. Leff D.R., Koh P.H., Aggarwal R., Leong J., Deliganni F., Elwell C., Delpy D.T., Darzi A., Yang G.Z. Optical mapping of the frontal cortex during a surgical knot-tying task, a feasibility study. Medical Imaging and Augmented Reality (MIAR) 2006, 140-147. Springer-Verlag, Shanghai. G.Z. Yang (Ed.).
28. Leff D.R., Elwell C.E., Orihuela-Espina F., Atallah L., Delpy D.T., Darzi A.W., Yang G.Z. Changes in prefrontal cortical behaviour depend upon familiarity on a bimanual co-ordination task: an fNIRS study. NeuroImage 2008, 39:805-813.
29. Leff D.R., Orihuela-Espina F., Atallah L., Athanasiou T., Leong J.J., Darzi A.W., Yang G.Z. Functional prefrontal reorganization accompanies learning-associated refinements in surgery: a manifold embedding approach. Comput. Aided Surg. 2008, 13:325-339.
30. Leff D.R., Orihuela-Espina F., Leong J., Darzi A., Yang G.Z. Modelling dynamic fronto-parietal behaviour during minimally invasive surgery-a Markovian trip distribution approach. Med. Image Comput. Comput. Assist. Interv. 2008, 11:595-602.
31. Leff D.R., Orihuela-Espina F., Athanasiou T., Karimyan V., Elwell C., Wong J., Yang G.Z., Darzi A.W. "Circadian cortical compensation": a longitudinal study of brain function during technical and cognitive skills in acutely sleep-deprived surgical residents. Ann. Surg. 2010, 252:1082-1090.
32. Lin C.H., Chiang M.C., Knowlton B.J., Iacoboni M., Udompholkul P., Wu A.D. Interleaved practice enhances skill learning and the functional connectivity of fronto-parietal networks. Hum. Brain Mapp. 2012.
33. Marteau T.M., Bekker H. The development of a six-item short-form of the state scale of the Spielberger State-Trait Anxiety Inventory (STAI). Br. J. Clin. Psychol. 1992, 31(Pt 3):301-306.
34. Moller H.J., Mikulis D.J. Neurocognitive disability, stroke, and surgery: a role for neuroergonomics?. J. Psychosom. Res. 2007, 63:613-615.
35. Mulliken G.H., Musallam S., Anderson R.A. Forward estimation of movement state in posterior parietal cortex. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:8170-8177.
36. Murthy A., Ray S., Shorter S.M., Priddy E.G., Schall J.D., Thompson K.G. Frontal eye field contributions to rapid corrective saccades. J. Neurophysiol. 2007, 97:1457-1469.
37. Mylonas G.P., Kwok K.W., Darzi A., Yang G.Z. Gaze-contingent motor channelling and haptic constraints for minimally invasive robotic surgery. Med. Image Comput. Comput. Assist. Interv. 2008, 11:676-683.
38. Mylonas G.P., Kwok K.W., James D.R.C., Leff D.R., Orihuela-Espina F., Darzi A.W., Yang G.Z. Gaze-Contingent Motor Channelling, Haptic Constraints and associated Cognitive Demand for Robotic MIS. Med. Image Anal. 2012, 16:612-631.
39. Ohuchida K., Kenmotsu H., Yamamoto A., Sawada K., Hayami T., Morooka K., Takasugi S., Konishi K., Ieiri S., Tanoue K., Iwamoto Y., Tanaka M., Hashizume M. The frontal cortex is activated during learning of endoscopic procedures. Surg. Endosc. 2009, 23:2296-2301.
40. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9:97-113.
41. Orihuela-Espina F., Leff D.R., James D.R.C., Darzi A.W., Yang G.Z. Quality control and assurance in functional near infrared spectroscopy (fNIRS) experimentation. Phys. Med. Biol. 2010, 55:1-24.
42. Parasuraman R. Neuroergonomics: research and practice. Theor. Issues Ergon. Sci. 2003, 4:5-20.
43. Petersen S.E., van Mier H., Fiez J.A., Raichle M.E. The effects of practice on the functional anatomy of task performance. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:853-860.
44. Posner M.I. Expanding horizons in ergonomics research. NeuroImage 2012, 59:149-153.
45. Puttemans V., Wenderoth N., Swinnen S.P. Changes in brain activation during the acquisition of a multifrequency bimanual coordination task: from the cognitive stage to advanced levels of automaticity. J. Neurosci. 2005, 25:4270-4278.
46. Rossini L., Izzo D., Summerer L. Brain-machine interfaces for space applications. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2009, 2009:520-523.
47. Rubinov M., Sporns O. Complex network measures of brain connectivity: uses and interpretations. NeuroImage 2010, 52:1059-1069.
48. Saager R., Berger A. Measurement of layer-like hemodynamic trends in scalp and cortex: implications for physiological baseline suppression in functional near-infrared spectroscopy. J. Biomed. Opt. 2008, 13:034017.
49. Schall J.D. The neural selection and control of saccades by the frontal eye field. Philos. Trans. R. Soc. B-Biol. Sci. 2002, 357:1073-1082.
50. Shadmehr R., Holcomb H.H. Neural correlates of motor memory consolidation. Science 1997, 277:821-825.
51. Sporns O., Chialvo D.R., Kaiser M., Hilgetag C.C. Organization, development and function of complex brain networks. Trends Cogn. Sci. 2004, 8:418-425.
52. Steele C.J., Penhune V.B. Specific increases within global decreases: a functional magnetic resonance imaging investigation of five days of motor sequence learning. J. Neurosci. 2010, 30:8332-8341.
53. Sun F.T., Miller L.M., Rao A.A., D'Esposito M. Functional connectivity of cortical networks involved in bimanual motor sequence learning. Cereb. Cortex 2007, 17:1227-1234.
54. Tachtsidis I., Leung T.S., Devoto L., Delpy D.T., Elwell C.E. Measurement of frontal lobe functional activation and related systemic effects: a near-infrared spectroscopy investigation. Adv. Exp. Med. Biol. 2008, 614:397-403.
55. Takahashi T., Takikawa Y., Kawagoe R., Shibuya S., Iwano T., Kitazawa S. Influence of skin blood flow on near-infrared spectroscopy signals measured on the forehead during a verbal fluency task. NeuroImage 2011, 57:991-1002.
56. Taskforce Heart rate variability. Standards of measurement, physiological interpretation, and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Eur. Heart J. 1996, 17:354-381.
57. Tononi G., Edelman G.M., Sporns O. Complexity and coherency: integrating information in the brain. Trends Cogn. Sci. 1998, 2:474-484.
58. Tsunashima H., Yanagisawa K. Measurement of brain function of car driver using functional near-infrared spectroscopy (fNIRS). Comput. Intell. Neurosci. 2009, vol. 2:1-12.
59. van den Heuvel M.P., Stam C.J., Boersma M., Hulshoff Pol H.E. Small-world and scale-free organization of voxel-based resting-state functional connectivity in the human brain. NeuroImage 2008, 43:528-539.
60. van den Heuvel M.P., Stam C.J., Kahn R.S., Hulshoff Pol H.E. Efficiency of functional brain networks and intellectual performance. J. Neurosci. 2009, 29:7619-7624.
61. van Wijk B.C., Stam C.J., Daffertshofer A. Comparing brain networks of different size and connectivity density using graph theory. PLoS One 2010, 5:e13701.
62. Voss M.W., Prakash R.S., Erickson K.I., Boot W.R., Basak C., Neider M.B., Simons D.J., Fabiani M., Gratton G., Kramer A.F. Effects of training strategies implemented in a complex videogame on functional connectivity of attentional networks. NeuroImage 2012, 59:138-148.
63. Watts D.J., Strogatz S.H. Collective dynamics of 'small-world' networks. Nature 1998, 393:440-442.
64. Zhu F.F., Poolton J.M., Wilson M.R., Hu Y., Maxwell J.P., Masters R.S. Implicit motor learning promotes neural efficiency during laparoscopy. Surg. Endosc. 2011, 25(9):2950-2955.