Cortical effects of user training in a motor imagery based brain-computer interface measured by fNIRS and EEG

NeuroImage

Volumn 85, Issue , 2014, Pages 432-444

  Kaiser, Vera ^a   Bauernfeind, Günther ^a   Kreilinger, Alex ^a   Kaufmann, Tobias ^b   Kübler, Andrea ^b   Neuper, Christa ^a,c   Müller Putz, Gernot R ^a  

^a GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c UNIVERSITY OF GRAZ   (Austria)

Author keywords

BCI training; Brain computer interface (BCI); Cortical training effects; Electroencephalography (EEG); Functional near infrared spectroscopy (fNIRS); Motor imagery (MI)

Indexed keywords

OXYHEMOGLOBIN;

ACCURACY; ARTICLE; BETA RHYTHM; BRAIN COMPUTER INTERFACE; BRAIN REGION; CONTROLLED STUDY; ELECTROENCEPHALOGRAPHY; ELECTROENCEPHALOGRAPHY PHASE SYNCHRONIZATION; EVOKED BRAIN STEM RESPONSE; FEMALE; FUNCTIONAL NEAR INFRARED SPECTROSCOPY; HUMAN; HUMAN EXPERIMENT; IMAGE ENHANCEMENT; IMAGERY; MALE; MENTAL TASK; MOTOR IMAGERY; NEAR INFRARED SPECTROSCOPY; NERVE CELL PLASTICITY; NORMAL HUMAN; PRIORITY JOURNAL; SENSORIMOTOR CORTEX; TASK PERFORMANCE; TRAINING; YOUNG ADULT;

BCI TRAINING; BRAIN-COMPUTER INTERFACE (BCI); CORTICAL TRAINING EFFECTS; ELECTROENCEPHALOGRAPHY (EEG); FUNCTIONAL NEAR-INFRARED SPECTROSCOPY (FNIRS); MOTOR IMAGERY (MI);

ADULT; BRAIN MAPPING; BRAIN-COMPUTER INTERFACES; CEREBRAL CORTEX; DATA INTERPRETATION, STATISTICAL; ELECTROENCEPHALOGRAPHY; FEMALE; HUMANS; MALE; MOTOR CORTEX; SIGNAL PROCESSING, COMPUTER-ASSISTED; SOMATOSENSORY CORTEX; SPECTROSCOPY, NEAR-INFRARED; YOUNG ADULT;

EID: 84889647244     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.04.097     Document Type: Article

References (72)

1. Afonso V., Tompkins W., Nguyen T., Luo S. Ecg beat detection using filter banks. IEEE Trans. Biomed. Eng. 1999, 46(2):192-202.
2. Alegre M., Labarga A., Gurtubay I.G., Iriarte J., Malanda A., Artieda J. Beta electroencephalograph changes during passive movements: sensory afferences contribute to beta event-related desynchronization in humans. Neurosci. Lett. 2002, 331:29-32.
3. Arenth P.M., Ricker J.H., Schultheis M.T. Applications of functional near-infrared spectroscopy (fNIRS) to Neurorehabilitation of cognitive disabilities. Clin. Neuropsychol. 2007, 21(1):38-57.
4. Bauernfeind G. Using Functional Near-infrared Spectroscopy (fNIRS) for Optical Brain-Computer Interface (oBCI) Applications 2012, (Ph.D. thesis), Graz University of Technology, Austria.
5. Bauernfeind G., Leeb R., Wriessnegger S., Pfurtscheller G. Development, set-up and first results of a one-channel near-infrared spectroscopy system. Biomed. Tech. (Berl.) 2008, 53(1):36-43.
6. Bauernfeind G., Daly I., Müller-Putz G.R. On the removal of physiological artifacts from fNIRS. Proceedings of the 3rd TOBI Workshop 2012 2012, 24-25.
7. Birbaumer N. Breaking the silence: brain-computer interfaces (BCI) for communication and motor control. Psychophysiology 2006, 43:517-532.
8. Birbaumer N., Ghanayim N., Hinterberger T., Iversen I., Kotchoubey B., Kübler A., Perelmouter J., Taub E., Flor H. A spelling device for the paralysed. Nature 1999, 398:297-298.
9. Buch E., Weber C., Cohen L., Braun C., Dimyan M., Ard T., Mellinger J., Caria A., Soekadar S., Fourkas A., Birbaumer N. Think to move: a neuromagnetic brain-computer interface (BCI) system for chronic stroke. Stroke 2008, 39:910-917.
10. Cannestra A.F., Wartenburger I., Obrig H., Villringer A., Toga A.W. Functional assessment of Broca's area using near infrared spectroscopy in humans. Neuroreport 2003, 14(15):1961-1965.
11. Cunha M., Machado D., Bastos V.H., Ferreira C., Cagy M., Basile L., Piedade R., Ribeiro P. Neuromodulatory effect of bromazepam on motor learning: an electroencephalographic approach. Neurosci. Lett. 2006, 407:166-170.
12. Cutini S., Moro S.B., Bisconti S. Functional near infrared optical imaging in cognitive neuroscience: an introductory review. J. Near Infrared Spectrosc. 2012, 20:75-92.
13. Davison A.C., Hinkley D.V. Bootstrap Methods and Their Application 1997, Cambridge University Press.
14. Dieler A.C., Tupak S.V., Fallgatter A.J. Functional near-infrared spectroscopy for the assessment of speech related tasks. Brain Lang. 2012, 121:90-109.
15. Duncan A., Meek J.H., Clemence M., Elwell C.E., Tyszczuk L., Cope M., Delpy D.T. Optical pathlength measurements on adult head, calf and forearm and the head of the newborn infant using phase resolved optical spectroscopy. Phys. Med. Biol. 1995, 49:295-304.
16. Elwell C.E., Springett R., Hillman E. Oscillations in cerebral haemodynamics - implications for functional activation studies. Adv. Exp. Med. Biol. 1999, 471:57-65.
17. Enzinger C., Ropele S., Fazekas F., Loitfelder M., Gorani F., Seifert T., Reiter G., Neuper C., Pfurtscheller G., Müller-Putz G. Brain motor system function in a patient with complete spinal cord injury following extensive brain-computer interface training. Exp. Brain Res. 2008, 190:215-223.
18. Farwell L.A., Donchin E. Talking off the top of your head: toward a mental prosthesis utilizing event-related brain potentials. Electroencephalogr. Clin. Neurophysiol. 1988, 70:510-523.
19. Ferrari M., Quaresima V. A brief review on the history of human functional near-infrared spectroscopy (fnirs) development and fields of application. Neuroimage 2012, 63(2):921-935.
20. Florian G., Stancak A., Pfurtscheller G. Cardiac response induced by voluntary self-paced finger movement. Int. J. Psychophysiol. 1998, 28(3):273-283.
21. Gentili R., Han C.E., Schweighofer N., Papaxanthis C. Motor learning without doing: trial-by-trial improvement in motor performance during mental training. J. Neurophysiol. 2010, 104:774-783.
22. Graimann B., Huggins J.E., Levine S.P., Pfurtscheller G. Visualization of significant ERD/ERS patterns in multichannel EEG and ECoG datas. Clin. Neurophysiol. 2002, 113:43-47.
23. Halder S., Agorastos D., Veit R., Hammer E.M., Lee S., Varkuti B., Bogdan M., Rosenstiel W., Birbaumer N., Kübler A. Neural mechanisms of brain-computer interface control. Neuroimage 2011, 55:1779-1790.
24. Herdener M., Esposito F., di Salle F., Boller C., Hilti C.C., Habermeyer B., Scheffler K., Wetzel S., Seifritz E., Cattapan-Ludewig K. Musical training induces functional plasticity in human hippocampus. J. Neurosci. 2010, 30:1377-1384.
25. Hirth C. Nichtinvasives optisches Mapping und Spektroskopie zur funktionellen Untersuchung des Gehirns 1999, (Ph.D. thesis), Humboldt-Universität zu, Berlin, Germany.
26. Hirth C., Obrig H., Villringer K., Thiel A., Bernarding J., Mühlnickel W., Flor H., Dirnagl U., Villringer A. Non-invasive functional mapping of the human motor cortex using near-infrared spectroscopy. Neuroreport 1996, 7(12):1977-1981.
27. Hobi V., Dubach U.C., Skreta M., Forgo J., Riggenbach H. The effect of bromazepam on psychomotor activity and subjective mood. J. Int. Med. Res. 1981, 9:89-97.
28. Homan R.W., Herman J., Purdy P. Cerebral location of international 10-20 system electrode placement. Electroencephalogr. Clin. Neurophysiol. 1987, 66(4):376-382.
29. Kaufmann T., Williamson J., Hammer E., Murray-Smith R., Kübler A. Visually multimodal vs. classic unimodal feedback approach for SMR-BCI: a comparison study. Int. J. Bioelectromagn. 2011, 13:80-81.
30. Kelly A.M.C., Garavan H. Human functional neuroimaging of brain changes associated with practice. Cereb. Cortex 2005, 15:1089-1102.
31. Kleih S., Kaufmann T., Zickler C., Halder S., Leotta F., Cincotti F., Aloise F., Riccio A., Herbert C., Mattia D., Kübler A. Out of the frying pan into the fire-the p300-based bci faces real-world challenges. Prog. Brain Res. 2011, 194:27-46.
32. Kleinschmidt A., Obrig H., Requardt M., Merboldt K.D., Dirnagl U., Villringer A., Frahm J. Simultaneous recording of cerebral blood oxygenation changes during human brain activation by magnetic resonance imaging and near-infrared spectroscopy. J. Cereb. Blood Flow Metab. 1996, 16(5):817-826.
33. Kübler A., Kotchoubey B., Kaiser J., Wolpaw J.R., Birbaumer N. Brain-computer communication: unlocking the locked in. Psychol. Bull. 2001, 127:358-375.
34. Kübler A., Nijboer F., Mellinger J., Vaughan T.M., Pawelzik H., Schalk G., McFarland D.J., Birbaumer N., Wolpaw J.R. Patients with ALS can use sensorimotor rhythms to operate a braincomputer interface. Neurology 2005, 64:1775-1777.
35. Leff D.R., Orihuela-Espina F., Elwell C.E., Athanasiou T., Delpy D.T., Darzi A.W., Yang G.Z. Assessment of the cerebral cortex during motor task behaviours in adults: a systematic review of functional near infrared spectroscopy (fnirs) studies. Neuroimage 2011, 54(4):2922-2936.
36. Malonek D., Grinvald A. Interactions between electrical activity and cortical microcirculation revealed by imaging spectroscopy: implications for functional brain mapping. Science 1996, 272(5261):551-554.
37. Malonek D., Dirnagl U., Lindauer U., Yamada K., Kanno I., Grinvald A. Vascular imprints of neuronal activity: relationships between the dynamics of cortical blood flow, oxygenation, and volume changes following sensory stimulation. Proc. Natl. Acad. Sci. U. S. A. 1997, 94(26):14826-14831.
38. Mihara M., Yagura H., Hatakenaka M., Hattori N., Miyai I. Clinical application of functional near-infrared spectroscopy in rehabilitation medicine. Brain Nerve 2010, 62(2):125-132.
39. Mihara M., Miyai I., Hattori N., Hatakenaka M., Yagura H., Kawano T., Okibayashi M., Danjo N., Ishikawa A., Inoue Y., Kubota K. Neurofeedback using real-time near-infrared spectroscopy enhances motor imagery related cortical activation. PLoS One 2012, 7(3):e32234.
40. Miyai I., Tanabe H., Sase I., Eda H., Oda I., Konishi I., Tsunazawa Y., Suzuki T., Yanagida T., Kubota K. Cortical mapping of gait in humans: a near-infrared spectroscopic topography study. Neuroimage 2001, 14(5):1186-1192.
41. Müller-Putz G.R., Scherer R., Pfurtscheller G., Rupp R. Brain-computer interfaces for control of neuroprostheses: from synchronous to asynchronous mode of operation. Biomed. Tech. (Berl.) 2006, 51:57-63.
42. Munzert J., Lorey B., Zentgraf K. Cognitive motor processes: the role of motor imagery in the study of motor representations. Brain Res. Rev. 2009, 60:306-326.
43. Neuper C., Müller-Putz G.R., Scherer R., Pfurtscheller G. Motor imagery and EEG-based control of spelling devices and neuroprostheses. Event-related dynamics of brain oscillations 2006, 393-409. Elsevier. C. Neuper, W. Klimesch (Eds.).
44. Neuper C., Wörtz M., Pfurtscheller G. ERD/ERS patterns reflecting sensorimotor activation and deactivation. Vol. 159 of Progress in Brain Research 2006, 211-222. Elsevier, (Ch. 14). C. Neuper, W. Klimesch (Eds.).
45. Nyberg L., Eriksson J., Larsson A., Marklund P. Learning by doing versus learning by thinking: an fMRI study of motor and mental training. Neuropsychologia 2006, 44:711-717.
46. Obrig H., Villringer A. Beyond the visible: imaging the human brain with light. J. Cereb. Blood Flow Metab. 2003, 23(1):1-18.
47. Okada E., Firbank M., Schweiger M., Arridge S.R., Cope M., Delpy D.T. Theoretical and experimental investigation of near-infrared light propagation in a model of the adult head. Appl. Opt. 1997, 36(1):21-31.
48. Okamoto M., Dan H., Sakamoto K., Takeo K., Shimizu K., Kohno S., Oda I., Isobe S., Suzuki T., Kohyama K., Dan I. Three-dimensional probabilistic anatomical cranio-cerebral correlation via the international 10-20 system oriented for transcranial functional brain mapping. Neuroimage 2004, 21(1):99-111.
49. Pfurtscheller G., Lopes da Silva F.H. Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin. Neurophysiol. 1999, 110:1842-1857.
50. Pfurtscheller G., McFarland D. BCIs that use sensorimotor rhythms. Brain Computer Interfaces: Principles and Practice 2012, Oxford University Press.
51. Pfurtscheller G., Neuper C. Motor imagery activates primary sensorimotor area in humans. Neurosci. Lett. 1997, 239:65-68.
52. Pfurtscheller G., Neuper C. Motor imagery and direct brain-computer communication. Proc. IEEE 2001, 89:1123-1134.
53. Pfurtscheller G., Pregenzer M., Neuper C. Visualization of sensorimotor areas involved in preparation for hand movement based on classification of mu and central beta rhythms in single EEG trials in man. Neurosci. Lett. 1994, 181:43-46.
54. Pfurtscheller G., Neuper C., Flotzinger D., Pregenzer M. EEG-based discrimination between imagination of right and left hand movement. Electroencephalogr. Clin. Neurophysiol. 1997, 103:642-651.
55. Pfurtscheller G., Brunner C., Schlögl A., da Silva F.H.L. Mu rhythm (de)synchronization and EEG single-trial classification of different motor imagery tasks. Neuroimage 2006, 31:153-159.
56. Pfurtscheller G., Müller-Putz G.R., Schlögl A., Graimann B., Scherer R., Leeb R., Brunner C., Keinrath C., Townsend G., Vidaurre C., Naeem M., Lee F.Y., Wriessnegger S., Zimmermann D., Höfler E., Neuper C. Graz-brain-computer Interface: State of Research. Toward brain-computer interfacing 2007, 65-84. MIT Press. G. Dornhege, J. Millan, T. Hinterberger, D.J. McFarland, K.-R. Müller (Eds.).
57. Pfurtscheller G., Linortner P., Winkler R., Korisek G., Müller-Putz G. Discrimination of motor imagery-induced EEG patterns in patients with complete spinal cord injury. Comput. Intell. Neurosci. 2009, 104180.
58. Pichiorri F., Cincotti F., Fallani F.D.V., Pisotta I., Morone G., Molinari M., Mattia D. Towards a brain computer interface-based rehabilitation: from bench to bedside. Proceedings of the 5th International Brain-Computer Interface Conference 2011, 268-271.
59. Pichiorri F., Fallani F.D.V., Cincotti F., Babiloni F., Molinari M.C., Kleih S., Neuper C., Kübler A., Mattia D. Sensorimotor rhythm-based brain-computer interface training: the impact on motor cortical responsiveness. J. Neural Eng. 2011, 8:25020-25029.
60. Pregenzer M., Pfurtscheller G., Flotzinger D. Automated feature selection with a distinction sensitive learning vector quantizer. Neurocomputing 1996, 11:19-29.
61. Rossi S., Telkemeyer S., Wartenburger I., Obrig H. Shedding light on words and sentences: near-infrared spectroscopy in language research. Brain Lang. 2012, 121:152-163.
62. Sellers E., Arbel Y., Donchin E. Bcis that use p300 event-related potentials. Brain Computer Interfaces: Principles and Practice 2012, Oxford University Press.
63. Singh A.K., Okamoto M., Dan H., Jurcak V., Dan I. Spatial registration of multichannel multi-subject fNIRS data to MNI space without MRI. Neuroimage 2005, 27(4):842-851.
64. Sitaram R., Zhang H., Guan C., Thulasidas M., Hoshi Y., Ishikawa A., Shimizu K., Birbaumer N. Temporal classification of multichannel near-infrared spectroscopy signals of motor imagery for developing a brain-computer interface. Neuroimage 2007, 34(4):1416-1427.
65. Stancák A., Pfurtscheller G. Desynchronization and recovery of β rhythms during brisk and slow self-paced finger movements in man. Neurosci. Lett. 1995, 196:21-24.
66. Steinbrink J., Villringer A., Kempf F., Haux D., Boden S., Obrig H. Illuminating the BOLD signal: combined fMRI-fNIRS studies. Magn. Reson. Imaging 2006, 24(4):495-505.
67. Steingrüber H., Lienert G. Hand-Dominanz-Test 1971, Hofgrefe, Göttingen.
68. Strangman G., Culver J.P., Thompson J.H., Boas D.A. A quantitative comparison of simultaneous BOLD fMRI and NIRS recordings during functional brain activation. Neuroimage 2002, 17(2):719-731.
69. van Raalten T.R., Ramsey N.F., Duyn J., Jansma J.M. Practice induces function-specific changes in brain activity. PLoS One 2008, 3:3270.
70. Vanzetta I., Grinvald A. Coupling between neuronal activity and microcirculation: implications for functional brain imaging. HFSP J. 2008, 2(2):79-98.
71. Wriessnegger S.C., Kurzmann J., Neuper C. Spatio-temporal differences in brain oxygenation between movement execution and imagery: a multichannel near-infrared spectroscopy study. Int. J. Psychophysiol. 2008, 67(1):54-63.
72. Zhang H., Xu L., Wang S., Xie B., Guo J., Long Z., Yao L. Behavioral improvements and brain functional alterations by motor imagery training. Brain Res. 2011, 1407:38-46.