Cerebral functional imaging using near-infrared spectroscopy during repeated performances of motor rehabilitation tasks tested on healthy subjects

Frontiers in Human Neuroscience

Volumn 8, Issue MAY, 2014, Pages

  Ishikuro, Koji ^a   Urakawa, Susumu ^a   Takamoto, Kouich ^a   Ishikawa, Akihiro ^b   Ono, Taketoshi ^a   Nishijo, Hisao ^a  

^a UNIVERSITY OF TOYAMA   (Japan)

^b SHIMADZU CORPORATION   (Japan)

Author keywords

Frontal pole; Motor skill; NIRS; Rehabilitation; tDCS

Indexed keywords

OXYHEMOGLOBIN;

ADULT; ARTICLE; FEMALE; FUNCTIONAL NEUROIMAGING; FUNCTIONAL TRAINING; HAND FUNCTION; HEMODYNAMICS; HUMAN; HUMAN EXPERIMENT; LATENT PERIOD; MALE; MOTOR PERFORMANCE; MOTOR REHABILITATION; NEAR INFRARED SPECTROSCOPY; NORMAL HUMAN; PREFRONTAL CORTEX; PRIMARY MOTOR CORTEX; REHABILITATION; SKIN BLOOD FLOW; SUPPLEMENTARY MOTOR AREA; TASK PERFORMANCE; TRANSCRANIAL DIRECT CURRENT STIMULATION;

EID: 84901373570     PISSN: None     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2014.00292     Document Type: Article

References (82)

1. Antal, A., Nitsche, M. A., Kincses, T. Z., Kruse, W., Hoffmann, K. P., and Paulus, W. (2004). Facilitation of visuo-motor learning by transcranial direct current stimulation of the motor and extrastriate visual areas in humans. Eur. J. Neurosci. 19, 2888-2892. doi: 10.1111/j.1460-9568.2004.03367.x
2. Banados, M., Teitelboim, C., and Zanelli, J. (1994). Black hole entropy and the dimensional continuation of the Gauss-Bonnet theorem. Phys. Rev. Lett. 14, 957-960. doi: 10.1103/PhysRevLett.72.957
3. Bliss, T. V., and Collingridge, G. L. (1993). A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39. doi: 10.1038/361031a0
4. Boettiger, C. A., and D'Esposito, M. (2005). Frontal networks for learning and executing arbitrary stimulus-response associations. J. Neurosci. 25, 2723-2732. doi: 10.1523/JNEUROSCI.3697-04.2005
5. Boros, K., Poreisz, C., Münchau, A., Paulus, W., and Nitsche, M. A. (2008). Premotor transcranial direct current stimulation (tDCS) affects primary motor excitability in humans. Eur. J. Neurosci. 27, 1292-1300. doi: 10.1111/j.1460-9568.2008.06090.x
6. Brunoni, A. R., Nitsche, M. A., Bolognini, N., Bikson, M., Wagner, T., Merabet, L., et al. (2012). Clinical research with transcranial direct current stimulation (tDCS): challenges and future directions. Brain Stimul. 5, 75-195. doi: 10.1016/j.brs.2011.03.002
7. Butler, A. J., Shuster, M., O'Hara, E., Hurley, K., Middlebrooks, D., and Guilkey, K. (2013). A meta-analysis of the efficacy of anodal transcranial direct current stimulation for upper limb motor recovery in stroke survivors. J. Hand Ther. 26, 162-170. doi: 10.1016/j.jht.2012.07.002.
8. Carmichael, S. T., and Price, J. L. (1996). Connectional networks within the orbital and medial prefrontal cortex of macaque monkeys. J. Comp. Neurol. 371, 179-207. doi: 10.1002/(SICI)1096-9861(19960722)371:2%3C179::AID-CNE1%3E3.0.CO;2-%23
9. Chance, B., Zhuang, Z., UnAh, C., Alter, C., and Lipton, L. (1993). Cognition-activated low-frequency modulation to light absorption in human brain. Proc. Natl. Acad. Sci. 90, 3770-3774. doi: 10.1073/pnas.90.8.3770
10. Clark, V. P., Coffman, B. A., Trumbo, M. C., and Gasparovic, C. (2011). Transcranial direct current stimulation (tDCS) produces localized and specific alterations in neurochemistry: A 1H magnetic resonance spectroscopy study. Neurosci. Lett. 500, 67-71. doi: 10.1016/j.neulet.2011.05.244
11. Critchley, H. D., Elliott, R., Mathias, C. J., and Dolan, R. J. (2000). Neuronal activity relating to generation and representation of Galvanic skin conductance responses: a functional magnetic resonance imaging study. J. Neurosci. 20, 3033-3040.
12. Cummings, F. W. (2001). The interaction of surface geometry with morphogens. J. Theor. Biol. 212, 303-313. doi: 10.1006/jtbi.2001.2377
13. Decety, J., Sjoholm, H., Ryding, E., Stenberg, G., and Ingvar, D. H. (1990). The cerebellum participates in mental activity: tomographic measurement of regional cerebral blood flow. Brain Res. 535, 313-317. doi: 10.1016/0006-8993(90)91615-N
14. de Guise, E., del Pesce, M., Foschi, N., Quattrini, A., Papo, I., and Lassonde, M. (1999). Callosal and cortical contribution to procedural learning. Brain 122, 1049-1062. doi: 10.1093/brain/122.6.1049
15. Deiber, M. P., Passingham, R. E., Colebatch, J. G., Friston, K. J., Nixon, P. D., and Frackowiak, R. S. (1991). Cortical areas and the selection of movement: a study with positron emission tomography. Exp. Brain Res. 84, 393-402. doi: 10.1007/BF00231461
16. Duncan, A., Meek, J. H., Clemence, M., Elwell, C. E., Fallon, P., Tyszczuk, L., et al. (1996). Measurement of cranial optical path length as a function of age using phase resolved near infrared spectroscopy. Periatr. Res. 39, 889-894. doi: 10.1203/00006450-199605000-00025
17. Floyer-Lea, A., and Matthews, P. M. (2004). Changing brain networks for visuomotor control with increased movement automaticity. J. Neurophysiol. 92, 2405-2412. doi: 10.1152/jn.01092.2003
18. Fox, P. T., and Raichle, M. E. (1986). Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory simulation in human subjects. Proc. Natl. Acad. Sci. U.S.A. 83, 1140-1144. doi: 10.1073/pnas.83.4.1140
19. Fox, P. T., Raichle, M. E., Mintun, M. A., and Dence, C. (1988). Nonoxidative glucose consumption during focal physiologic neural activity. Science 241, 462-464. doi: 10.1126/science.3260686
20. Friston, K. J., Frith, C. D., Passingham, R. E., Liddle, P. F., and Frackowiak, R. S. (1992). Motor practice and neurophysiological adaptation in the cerebellum: a positron tomography study. Proc. Biol. Sci. 248, 223-228. doi: 10.1098/rspb.1992.0065
21. Fritsch, B., Reis, J., Martinowich, K., Schambra, H. M., Ji, Y., Cohen, L. G., et al. (2010). Direct current stimulation promotes BDNF-dependent synaptic plasticity: potential implications for motor learning. Neuron 66, 198-204. doi: 10.1016/j.neuron.2010.03.035
22. Fukui, Y., Ajichi, Y., and Okada, E. (2003). Monte Carlo prediction of near-infrared light propagation in realistic adult and neonatal head models. Appl Opt. 42, 2881-2887. doi: 10.1364/AO.42.002881
23. Gagnon, L., Perdue, K., Greve, D. N., Goldenholz, D., Kaskhedikar, G., and Boas, D. A. (2011). Improved recovery of the hemodynamic response in diffuse optical imaging using short optode separations and state-space modeling. Neuroimage 56, 1362-1371. doi: 10.1016/j.neuroimage.2011.03.001
24. Geisler, S., Derst, C., Veh, R. W., and Zahm, D. S. (2007). Glutamatergic afferents of the ventral tegmental area in the rat. J. Neurosci. 27, 5730-5743. doi: 10.1523/JNEUROSCI.0012-07.2007
25. Germon, T. J., Evans, P. D., Barnett, N. J., Wall, P., Manara, A. R., and Nelson, R. J. (1999). Cerebral near infrared spectroscopy: emitter-detector separation must be increased. Br. J. Anaesthesia 82, 831-837. doi: 10.1093/bja/82.6.831
26. Haggard, P. (2008). Human volition: towards a neuroscience of will. Nat. Rev. Neurosci. 9, 934-946. doi: 10.1038/nrn2497
27. Halsband, U., and Lange, R. K. (2006). Motor learning in man: a review of functional and clinical studies. J. Physiol. Paris. 99, 414-424. doi: 10.1016/j.jphysparis.2006.03.007
28. Hanlon, R. E. (1996). Motor learning following unilateral stroke. Arch. Phys. Med. Rehabil. 77, 811-815. doi: 10.1016/S0003-9993(96)90262-2
29. Hatakenaka, M., Miyai, I., Mihara, M., Sakoda, S., and Kubota, K. (2007). Frontal regions involved in learning of motor skill-a functional NIRS study. Neuroimage 34, 109-116. doi: 10.1016/j.neuroimage.2006.08.014
30. Hoshi, Y. (2003). Functional near-infrared optical imaging: utility and limitations in human brain mapping. Psychophysiology 40, 511-520. doi: 10.1111/1469-8986.00053
31. Hoshi, Y., Kobayashi, N., and Tamura, M. (2001). Interpretation of near-infrared spectroscopy signals: a study with a newly developed perfused rat brain model. J. Appl. Physiol. 90, 1622-1657.
32. Hoshi, Y., and Tamura, M. (1993). Detection of dynamic changes in cerebral oxygenation coupled to neuronal function during mental work in human. Neurosci. Lett. 150, 5-8. doi: 10.1016/0304-3940(93)90094-2
33. Hosp, J. A., Pekanovic, A., Rioult-Pedotti, M. S., and Luft, A. R. (2011). Dopaminergic projections from midbrain to primary motor cortex mediate motor skill learning. J. Neurosci. 31, 2481-2487. doi: 10.1523/JNEUROSCI.5411-10.2011
34. Jenkins, I. H., Brooks, D. J., Nixon, P. D., Frackowiak, R. S., and Passingham, R. E. (1994). Motor sequence learning: a study with positron emission tomography. J. Neurosci. 14, 3775-3790.
35. Jobsis, F. F. (1977). Noninvasive infrared monitoring of cerebral and myocardial oxygen sufficiency and circulatory parameters. Science 198, 1264-1267. doi: 10.1126/science.929199
36. Jueptner, M., Stephan, K. M., Frith, C. D., Brooks, D. J., Frackowiak, R. S. J., and Passingham, R. E. (1997). Anatomy of motor learning. I. Frontal cortex and attention to action. J. Neurophysiol. 77, 1313-1324.
37. Kato, T., Kamei, A., Takashima, S., and Ozaki, T. (1993). Human visual cortical function during photic stimulation monitoring by means of near-infrared spectroscopy. J. Cereb. Blood Flow Metab. 13, 516-520. doi: 10.1038/jcbfm.1993.66
38. Kawahira, K., Noma, T., Iiyama, J., Etoh, S., Ogata, A., and Shimodozono, M. (2009). Improvements in limb kinetic apraxia by repetition of a newly designed facilitation exercise in a patient with corticobasal degeneration. Int. J. Rehabil. Res. 32, 178-183. doi: 10.1097/MRR.0b013e32831e4546
39. Kohri, S., Hoshi, Y., Tamura, M., Kato, C., Kuge, Y., and Tamaki, N. (2002). Quantitative evaluation of the relative contribution ratio of cerebral tissue to near-infrared signals in the adult human head: a preliminary study. Physiol. Meas. 23, 301-312. doi: 10.1088/0967-3334/23/2/306
40. Lewis, B. L., and O'Donnell, P. (2000). Ventral tegmental area afferents to the prefrontal cortex maintain membrane potential 'up' states in pyramidal neurons via D1 dopamine receptors. Cereb. Cortex 10, 1168-1175. doi: 10.1093/cercor/10.12.1168
41. Liberzon, I., King, A. P., Britton, J. C., Phan, K. L., Abelson, J. L., and Taylor, S. F. (2007). Paralimbic and medical prefrontal cortical involvement in neuroendocrine responses to traumatic stimuli. Am. J. Psychiatry 164, 1250-1258. doi: 10.1176/appi.ajp.2007.06081367
42. Liebetanz, D., Nitsche, M. A, Tergau, F., and Paulus, W. (2002). Pharmacological approach to the mechanisms of transcranial DC-stimulation-induced after-effects of human motor cortex excitability. Brain 125, 2238-2247. doi: 10.1093/brain/awf238
43. Mansouri, C., L'Huillier, J. P., Kashou, N. H., and Humeau, A. (2010). Depth sensitivity analysis of functional near-infrared spectroscopy measurement using three-dimensional Monte Carlo modelling-based magnetic resonance imaging. Lasers Med. Sci. 25, 431-438. doi: 10.1007/s10103-010-0754-4
44. Martin, S. J., Grimwood, P. D., and Morris, R. G. (2000). Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci. 23, 649-711. doi: 10.1146/annurev.neuro.23.1.649
45. Molgedey, L., and Schuster, H. G. (1994). Separation of a mixture of independent signals using time delayed correlations. Phys. Rev. Lett. 72, 3634-3637. doi: 10.1103/PhysRevLett.72.3634
46. Molina-Luna, K., Pekanovic, A., Röhrich, S., Hertler, B., Schubring-Giese, M., Rioult-Pedotti, M. S., et al. (2009). Dopamine in motor cortex is necessary for skill learning and synaptic plasticity. PLoS ONE 4:e7082. doi: 10.1371/journal.pone.0007082
47. Moody, M., Panerai, R. B., Eames, P. J., and Potter, J. F. (2005). Cerebral and systemic hemodynamic changes during cognitive and motor activation paradigms. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, R1581-R1588. doi: 10.1152/ajpregu.00837.2004
48. Nitsche, M. A., Fricke, K., Henschke, U., Schlitterlau, A., Liebetanz, D., Lang, N., et al. (2003a). Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans. J. Physiol. 553, 293-301. doi: 10.1113/jphysiol.2003.049916
49. Nitsche, M. A, Jakoubkova, M., Thirugnanasambandam, N., Schmalfuss, L., Hullemann, S., Sonka, K., et al. (2010). Contribution of the premotor cortex to consolidation of motor sequence learning in humans during sleep. J. Neurophysiol. 104, 2603-2614. doi: 10.1152/jn.00611.2010
50. Nitsche, M. A., Liebetanz, D., Lang, N., Antal, A., Tergau, F., and Paulus, W. (2003b). Safety criteria for transcranial direct current stimulation (tDCS) in humans. Clin. Neurophysiol. 114, 2220-2222. doi: 10.1016/S1388-2457(03)00235-9
51. Nitsche, M. A., Liebetanz, D., Schlitterlau, A., Henschke, U., Fricke, K., Frommann, K., et al. (2004). GABAergic modulation of DC stimulation-induced motor cortex excitability shifts in humans. Eur. J. Neurosci. 19, 2720-2726. doi: 10.1111/j.0953-816X.2004.03398.x
52. Nitsche, M. A., Schauenburg, A., Lang, N., Liebetanz, D., Exner, C., Paulus, W., et al. (2003c). Facilitation of implicit motor learning by weak transcranial direct current stimulation of the primary motor cortex in the human. J. Cogn. Neurosci. 15, 619-626. doi: 10.1162/089892903321662994
53. Ogawa, S., Menon, R. S., Tank, D. W., Kin, S. G., Merkle, H., Ellermann, J. M., et al. (1993). Functional brain mapping by blood oxygenation level-dependent contrast magnetic resonance imaging. A comparison of signal characteristics with a biophysical model. Biophys. J. 64, 803-812. doi: 10.1016/S0006-3495(93)81441-3
54. Ohmae, E., Ouchi, Y., Oda, M., Suzuki, T., Nobesawa, S., Kanno, T., et al. (2006). Cerebral hemodynamics evaluation by near-infrared time-resolved spectroscopy: correlation with simultaneous positron emission tomography measurements. Neuroimage 29, 697-705. doi: 10.1016/j.neuroimage.2005.08.008
55. Okamoto, M., Dan, H., Shimizu, K., Takeo, K., Amita, T., Oda, I., et al. (2004). Multimodal assessment of cortical activation during apple peeling by NIRS and fMRI. Neuroimage 21, 1275-1288. doi: 10.1016/j.neuroimage.2003.12.003
56. Petrides, M. (2005). Lateral prefrontal cortex: architectonic and functional organization. Philos. Trans. R Soc. Lond. B Biol. Sci. 360, 781-95. doi: 10.1098/rstb.2005.1631
57. Petrides, M., and Pandya, D. N. (2007). Efferent association pathways from the rostral prefrontal cortex in the macaque monkey. J. Neurosci. 27, 11573-11586. doi: 10.1523/JNEUROSCI.2419-07.2007
58. Reis, J., and Fritsch, B. (2011). Modulation of motor performance and motor learning by transcranial direct current stimulation. Curr. Opin. Neurol. 24, 590-596. doi: 10.1097/WCO.0b013e32834c3db0
59. Reis, J., Schambra, H. M., Cohen, L. G., Buch, E. R., Fritsch, B., Zarahn, E., et al. (2009). Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. Proc. Natl. Acad. Sci. U.S.A. 106, 1590-5. doi: 10.1073/pnas.0805413106
60. Richer, F., Chouinard, M. J., and Rouleau, I. (1999). Frontal lesions impair the attentional control of movements during motor learning. Neuropsychologia 37, 1427-1435. doi: 10.1016/S0028-3932(99)00029-9
61. Rioult-Pedotti, M. S., Friedman, D., and Donoghue, J. P. (2000). Learning-induced LTP in neocortex. Science 290, 533-536. doi: 10.1126/science.290.5491.533
62. Roland, P. E., and Seitz, R. J. (1989). "Mapping of learning and memory functions of the brain, " in Visualization of Brain Functions, ed D. Ottoson (London: Stockton), 141-151.
63. Roy, C. S., and Sherrington, C. S. (1890). On the regulation of the blood-supply of the brain. J. Physiol. 11, 85-108.
64. Saager, R., and Berger, A. (2008). Measurement of layer-like hemodynamic trends in scalp and cortex: implications for physiological baseline suppression in functional near-infrared spectroscopy. J. Biomed. Opt. 13:034017. doi: 10.1117/1.2940587
65. Schlaug, G., Renga, V., and Nair, D. (2008). Transcranial direct current stimulation in stroke recovery. Arch. Neurol. 65, 1571-1576. doi: 10.1001/archneur.65.12.1571
66. Seiyama, A., Hazeki, O., and Tamura, M. (1988). Noninvasive quantitative analysis of blood oxygenation in rat skeletal muscle. J. Biochem. 103, 419-424.
67. Smielewski, P., Czosnyka, M., Pickard, J. D., and Kirkpatrick, P. (1997). Clinical evaluation of near-infrared spectroscopy for testing cerebrovascular reactivity in patients with carotid artery disease. Stroke 28, 331-338. doi: 10.1161/01.STR.28.2.331
68. Stagg, C. J., Bachtiar, V., and Johansen-Berg, H. (2011). The role of GABA in human motor learning. Curr. Biol. 21, 480-484. doi: 10.1016/j.cub.2011.01.069
69. Strangman, G., Culver, J. P., Thompson, J. H., and Boas, D. A. (2002). A quantitative comparison of simultaneous BOLD fMRI and NIRS recordings during functional brain activation. Neuroimage 17, 719-731. doi: 10.1006/nimg.2002.1227
70. Takahashi, T., Takikawa, Y., Kawagoe, R., Shibuya, S., Iwano, T., and Kitazawa, S. (2011). Influence of skin blood flow on near-infrared spectroscopy signals measured on the forehead during a verbal fluency task. Neuroimage 57, 991-1002. doi: 10.1016/j.neuroimage.2011.05.012
71. Takamoto, K., Hori, E., Urakawa, S., Katayama, M., Nagashima, Y., Yada, Y., et al. (2013). Thermotherapy to the facial region in and around the eyelids altered prefrontal hemodynamic responses and autonomic nervous activity during mental arithmetic. Psychophysiology 50, 35-47. doi: 10.1111/j.1469-8986.2012.01488.x
72. Takeuchi, M., Hori, E., Takamoto, K., Tran, A. H., Kohno, S., Ishikawa, A., et al. (2009). Brain cortical mapping by simultaneous recording of functional near infrared spectroscopy and electroencephalograms from the whole brain during right median nerve stimulation. Brain Topogr. 22, 197-214. doi: 10.1007/s10548-009-0109-2
73. van Mier, H., Tempel, L. W., Perlmutter, J. S., Raichle, M. E., and Petersen, S. E. (1998). Changes in brain activity during motor learning measured with PET: effects of hand of performance and practice. J. Neurophysiol. 80, 2177-2199.
74. Villringer, A., Planck, J., Hock, C., Schleinkofer, L., and Dirnagl, U. (1993). Near-infrared spectroscopy (NIRS): a new tool to study hemodynamic changes during activation of brain function in human adults. Neurosci. Lett. 154, 101-104. doi: 10.1016/0304-3940(93)90181-J
75. Vollmann, H., Conde, V., Sewerin, S., Taubert, M., Sehm, B., Witte, O. W, et al. (2012). Anodal transcranial direct current stimulation (tDCS) over supplementary motor area (SMA) but not pre-SMA promotes short-term visuomotor learning. Brain Stimul. 6, 101-107. doi: 10.1016/j.brs.2012.03.018
76. Wray, S., Cope, M., Delpy, D. T., Wyatt, J. S., and Reynolds, E. O. (1988). Characterization of the near infrared absorption spectra of cytochrome aa3 and haemoglobin for the non-invasive monitoring of cerebral oxygenation. Biochim. Biophys. Acta 30, 184-192. doi: 10.1016/0005-2728(88)90069-2
77. Yamada, T., Umeyama, S., and Matsuda, K. (2009). Multidistance probe arrangement to eliminate artifacts in functional near-infrared spectroscopy. J. Biomed. Opt. 14:064034. doi: 10.1117/1.3275469
78. Yamamoto, T., and Kato, T. (2002). Paradoxical correlation between signal in functional magnetic resonance imaging and deoxygenated hemoglobin content in capillaries: a new theoretical explanation. Phys. Med. Biol. 47, 1121-1141. doi: 10.1088/0031-9155/47/7/309
79. Yamanaka, H., Kawahira, K., Arima, M., Shimodozono, M., Etoh, S., Tanaka, N., et al. (2005). Evaluation of skilled arm movements in patients with stroke using a computerized motor-skill analyzer for the arm. Int. J. Rehabil. Res. 28, 277-283. doi: 10.1097/00004356-200509000-00013
80. Yasui, H., Takamoto, K., Hori, E., Urakawa, S., Nagashima, Y., Yada, Y., et al. (2010). Significantly correlation between autonomic nervous activity and cerebral hemodynamics during thermotherapy on the neck. Auton. Neurosci. 156, 96-103. doi: 10.1016/j.autneu.2010.03.011
81. Ye, J. C., Tak, S., Jang, K. E., Jung, J., and Jang, J. (2009). NIRS-SPM: statistical parametric mapping for near-infrared spectroscopy. Neuroimage 44, 428-447. doi: 10.1016/j.neuroimage.2008.08.036
82. Zysset, S., Huber, O., Ferstl, E., and von Cramon, D. Y. (2002). The anterior frontomedian cortex and evaluative judgment: an fMRI study. Neuroimage 15, 983-991. doi: 10.1006/nimg.2001.1008