Improvement in touch sensation after stroke is associated with resting functional connectivity changes

Frontiers in Neurology

Volumn 6, Issue JUL, 2015, Pages

  Bannister, Louise C ^a,b   Crewther, Sheila G ^b   Gavrilescu, Maria ^a,c   Carey, Leeanne M ^a,b,d  

^a FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

^b LA TROBE UNIVERSITY   (Australia)

^c DEFENCE SCIENCE AND TECHNOLOGY ORGANISATION   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Intrinsic functional connectivity; Magnetic resonance imaging; Neuronal plasticity; Somatosensory disorders; Stroke recovery; Tactile

Indexed keywords

ADULT; AGED; ARTICLE; CEREBELLUM; CEREBROVASCULAR ACCIDENT; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; FRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; IMPAIRED TACTILE DISCRIMINATION; INFERIOR PARIETAL CORTEX; MALE; MIDDLE AGED; MIDDLE TEMPORAL GYRUS; NEUROIMAGING; RESTING STATE NETWORK; SOMATOSENSORY CORTEX; SOMATOSENSORY DISORDER; SOMATOSENSORY SYSTEM; TACTILE DISCRIMINATION; THALAMUS; TOUCH; VISUAL CORTEX; YOUNG ADULT;

EID: 84940033950     PISSN: None     EISSN: 16642295     Source Type: Journal    
DOI: 10.3389/fneur.2015.00165     Document Type: Article

References (89)

1. Kim JS, Choi-Kwon S. Discriminative sensory dysfunction after unilateral stroke. Stroke (1996) 27:677-82. doi: 10.1161/01.STR.27.4.677.
2. Carey LM, Matyas TA. Frequency of discriminative sensory loss in the hand after stroke. J Rehabil Med (2011) 43(3):257-63. doi:10.2340/16501977-0662.
3. Carey LM, Abbott DF, Harvey MR, Puce A, Seitz RJ, Donnan GA. Relationship between touch impairment and brain activation after lesions of subcortical and cortical somatosensory regions. Neurorehabil Neural Repair (2011) 25(5):443-57. doi:10.1177/1545968310395777.
4. Carter AR, Shulman GL, Corbetta M. Why use a connectivity-based approach to study stroke and recovery of function? Neuroimage (2012) 62(4):2271-80. doi:10.1016/j.neuroimage.2012.02.070.
5. Corbetta M, Kincade M, Lewis C, Snyder A, Sapir A. Neural basis and recovery of spatial attention deficits in spatial neglect. Nat Neurosci (2005) 8:1603-10. doi:10.1038/nn1574.
6. Carey L, Seitz R, Parsons M, Levi C, Farquharson S, Tournier J-D, et al. Beyond the lesion - neuroimaging foundations for poststroke recovery. Future Neurol (2013) 8(5):507-24. doi:10.2217/fnl.13.39.
7. Carter AR, Astafiev SV, Lang CE, Connor LT, Rengachary J, Strube MJ, et al. Resting interhemispheric functional magnetic resonance imaging connectivity predicts performance after stroke. Ann Neurol (2010) 67(3):365-75. doi:10.1002/ana.21905.
8. Corbetta M. Functional connectivity and neurological recovery. Dev Psychobiol (2012) 54:239-53. doi:10.1002/dev.20507.
9. Kolb B, Teskey GC, Gibb R. Factors influencing cerebral plasticity in the normal and injured brain. Front Hum Neurosci (2010) 4:204. doi:10.3389/fnhum.2010.00204.
10. Wikström H, Roine RO, Aronen HJ, Salonen O, Sinkkonen J, Ilmoniemi RJ, et al. Specific changes in somatosensory evoked fields during recovery from sensorimotor stroke. Ann Neurol (2000) 47:353-60. doi:10.1002/1531-8249(200003)47:3<353::AID-ANA11>3.3.CO;2-I.
11. Carey LM, Abbott DF, Puce A, Jackson GD, Syngeniotis A, Donnan GA. Reemergence of activation with poststroke somatosensory recovery: a serial fMRI case study. Neurology (2002) 59(5):749-52. doi:10.1212/WNL.59.5.749.
12. Staines WR, Black SE, Graham SJ, McIlroy WE. Somatosensory gating and recovery from stroke involving the thalamus. Stroke (2002) 33(11):2642-51. doi:10.1161/01.STR. 0000032552.40405.40.
13. Rossini PM, Altamura C, Ferreri F, Melgari J-M, Tecchio F, Tombini M, et al. Neuroimaging experimental studies on brain plasticity in recovery from stroke. Eura Medicophys (2007) 43:241-54.
14. Weder B, Knorr U, Herzog H, Nebeling B, Kleinschmidt A, Huang Y, et al. Tactile exploration of shape after subcortical ischaemic infarction studied with PET. Brain (1994) 117(3):593-605. doi:10.1093/brain/117.3.593.
15. Taskin B, Jungehulsing GJ, Ruben J, Brunecker P, Krause T, Blankenburg F, et al. Preserved responsiveness of secondary somatosensory cortex in patients with thalamic stroke. Cereb Cortex (2006) 16(10):1431-9. doi:10.1093/cercor/bhj080.
16. Tecchio F, Zappasodi F, Tombini M, Oliviero A, Pasqualetti P, Vernieri F, et al. Brain plasticity in recovery from stroke: an MEG assessment. Neuroimage (2006) 32(3):1326-34. doi:10.1016/j.neuroimage.2006.05.004.
17. Tecchio F, Zappasodi F, Tombini M, Caulo M, Vernieri F, Rossini PM. Interhemispheric asymmetry of primary hand representation and recovery after stroke: a MEG study. Neuroimage (2007) 36(4):1057-64. doi:10.1016/j.neuroimage.2007.02.058.
18. Price CJ, Friston KJ. Scanning patients with tasks they can perform. Hum Brain Mapp (1999) 8:102-8. doi:10.1002/(SICI)1097-0193(1999)8:2/3<102::AID-HBM6>3.0.CO;2-J.
19. Biswal BB, Mennes M, Zuo XN, Gohel S, Kelly C, Smith SM, et al. Toward discovery science of human brain function. Proc Natl Acad Sci U S A (2010) 107(10):4734-9. doi:10.1073/pnas.0911855107.
20. Friston KJ. Functional and effective connectivity: a review. Brain Connect (2011) 1(1):13-36. doi:10.1089/brain.2011.0008.
21. Sporns O, Chialvo DR, Kaiser M, Hilgetag CC. Organization, development and function of complex brain networks. Trends Cogn Sci (2004) 8(9):418-25. doi:10.1016/j.tics.2004.07.008.
22. Lewis CM, Baldassarre A, Committeri G, Romani GL, Corbetta M. Learning sculpts the spontaneous activity of the resting human brain. Proc Natl Acad Sci U S A (2009) 106(41):17558-63. doi:10.1073/pnas.0902455106.
23. Cohen AL, Fair DA, Dosenbach NU, Miezin FM, Dierker D, Van Essen DC, et al. Defining functional areas in individual human brains using resting functional connectivity MRI. Neuroimage (2008) 41(1):45-57. doi:10.1016/j.neuroimage.2008.01.066.
24. Shirer WR, Ryali S, Rykhlevskaia E, Menon V, Greicius MD. Decoding subject-driven cognitive states with whole-brain connectivity patterns. Cereb Cortex (2012) 22(1):158-65. doi:10.1093/cercor/bhr099.
25. He BJ, Snyder AZ, Vincent JL, Epstein A, Shulman GL, Corbetta M. Breakdown of functional connectivity in frontoparietal networks underlies behavioral deficits in spatial neglect. Neuron (2007) 53(6):905-18. doi:10.1016/j.neuron.2007.02.013.
26. Nomura EM, Gratton C, Visser RM, Kayser A, Perez F, D'Esposito M. Double dissociation of two cognitive control networks in patients with focal brain lesions. Proc Natl Acad Sci U S A (2010) 107(26):12017-22. doi:10.1073/pnas.1002431107.
27. Rehme AK, Grefkes C. Cerebral network disorders after stroke: evidence from imaging-based connectivity analyses of active and resting brain states in humans. J Physiol (2013) 591(1):17-31. doi:10.1113/jphysiol.2012.243469.
28. van Meer MPA, van der Marel K, Wang K, Otte WM, El Bouazati S, Roeling TA, et al. Recovery of sensorimotor function after experimental stroke correlates with restoration of resting-state interhemispheric functional connectivity. J Neurosci (2010) 30(11):3964-72. doi:10.1523/JNEUROSCI. 5709-09.2010.
29. Wang L, Yu CS, Chen H, Qin W, He Y, Fan FM, et al. Dynamic functional reorganization of the motor execution network after stroke. Brain (2010) 133(4):1224-38. doi:10.1093/brain/awq043.
30. Park C-H, Chang WH, Ohn SH, Kim ST, Bang OY, Pascual-Leone A, et al. Longitudinal changes of resting-state functional connectivity during motor recovery after stroke. Stroke (2011) 42:1357-62. doi:10.1161/STROKEAHA.110.596155.
31. Iwamura Y, Taoka M, Iriki A. Bilateral activity and callosal connections in the somatosensory cortex. Neuroscientist (2001) 7(5):419-29. doi:10.1177/107385840100700511.
32. Schulte T, Müller-Oehring EM. Contribution of callosal connections to the interhemispheric integration of visuomotor and cognitive processes. Neuropsychol Rev (2010) 20(2):174-90. doi:10.1007/s11065-010-9130-1.
33. Ward NS, Cohen LG. Mechanisms underlying recovery of motor function after stroke. Arch Neurol (2004) 61(12):1844-8. doi:10.1001/archneur.61.12.1844.
34. Seitz RJ, Bütefisch CM. Recovery from ischemic stroke: a translational research perspective for neurology. Future Neurol (2006) 1:571-86. doi:10.2217/14796708.1.5.571.
35. Carey LM, Seitz R. Functional neuroimaging in stroke recovery and neurorehabilitation: conceptual issues and perspectives. Int J Stroke (2007) 2(4):245-64. doi:10.1111/j.1747-4949.2007.00164.x.
36. Carey LM. Touch and body sensations. In: Carey LM, editor. Stroke Rehabilitation: Insights from Neuroscience and Imaging. New York, NY: Oxford University Press (2012). p. 157-72.
37. Grefkes C, Ward NS. Cortical reorganisation after stroke: how much and how functional? Neuroscientist (2014) 20:56-70. doi:10.1177/1073858413491147.
38. Corbetta M, Shulman GL. Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci (2002) 3:201-15. doi:10.1038/nrn755.
39. Corbetta M, Patel G, Shulman GL. The reorienting system of the human brain: from environment to theory of mind. Neuron (2008) 58(3):306-24. doi:10.1016/j.neuron.2008.04.017.
40. Sathian K. Cross-modal plasticity in sensory systems. In: Selzer M, Clarke S, Cohen LG, Duncan PW, Gage FH, editors. Textbook of Neural Repair and Rehabilitation Neural Repair and Plasticity. Cambridge, IN: Cambridge Uni Press (2006). p. 180-93.
41. Seitz RJ, Knorr U, Azari NP, Herzog H, Freud H-J. Visual network activation in recovery from sensorimotor stroke. Restor Neurol Neurosci (1999) 14:25-33.
42. Crewther SG, Goharpy N, Bannister L, Lamp G. Goal-driven attention in recovery post-stroke. In: Carey LM, editor. Stroke Rehabilitation: Insights from Neuroscience and Neuroimaging. New York, NY: Oxford University Press (2012). p. 191-207.
43. Minati L, Grisoli M, Bruzzone MG. MR spectroscopy, functional MRI, and diffusion-tensor imaging in the aging brain: a conceptual review. J Geriatr Psychiatry Neurol (2007) 20:3-21. doi:10.1177/0891988706297089.
44. Roski C, Caspers S, Langner R, Laird AR, Fox PT, Zilles K, et al. Adult age-dependent differences in resting-state connectivity within and between visual-attention and sensorimotor networks. Front Aging Neurosci (2013) 5:67. doi:10.3389/fnagi.2013.00067.
45. Robertson IH, North N. Active and passive activation of left limbs: influence on visual and sensory neglect. Neuropsychologia (1993) 31:293-300. doi:10.1016/0028-3932(93)90093-F.
46. Johansen-Berg H, Dawes H, Guy C, Smith S, Wade DT, Matthews PM. Correlation between motor improvements and altered fMRI activity after rehabilitative therapy. Brain (2002) 125:2731-42. doi:10.1093/brain/awf282.
47. Loubinoux I, Carel C, Pariente J, Dechaumont S, Albucher J-F, Marque P, et al. Correlation between cerebral reorganization and motor recovery after subcortical infarcts. Neuroimage (2003) 20:2166-80. doi:10.1016/j.neuroimage.2003.08.017.
48. Tombari D, Loubinoux I, Pariente J, Gerdelat A, Albucher J-F, Tardy J, et al. A longitudinal fMRI study: in recovering and then in clinically stable subcortical stroke patients. Neuroimage (2004) 23:827-39. doi:10.1016/j.neuroimage.2004.07.058.
49. Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia (1971) 9:97-113. doi:10.1016/0028-3932(71)90067-4.
50. Brott T, Adams HP, Olinger CP, Marler JR, Barsan WG, Biller J, et al. Measurements of acute cerebral infarction: a clinical examination scale. Stroke (1989) 20(7):864-70. doi:10.1161/01.STR.20.7.871.
51. Mahoney FI, Barthel DW. Functional evaluation - the Barthel index. Md State Med J (1965) 14:61-5.
52. Van der Lee JH, De Groot V, Beckerman H, Wagenaar RC, Lankdorst GJ, Bouter LM. The intra- and interrater reliability of the action research arm test: a practical test of upper extremity function in patients with stroke. Arch Phys Med Rehabil (2001) 82(1):14-9. doi:10.1053/apmr.2001.18668.
53. Carey LM, Oke LE, Matyas TA. Impaired limb position sense after stroke: a quantitative test for clinical use. Arch Phys Med Rehabil (1996) 77(12):1271-8. doi:10.1016/S0003-9993(96)90192-6.
54. Carey LM. Loss of somatic sensation. In: Selzer M, Clarke S, Cohen L, Duncan P, Gage FH, editors. Textbook of Neural Repair and Rehabilitation Vol II Medical Neurorehabilitation. Cambridge, IN: Cambridge Uni Press (2006). p. 231-47.
55. Carey LM, Oke LE, Matyas TA. Impaired touch discrimination after stroke: a quantitative test. Neurorehabil Neural Repair (1997) 11(4):219-32. doi:10.1177/154596839701100404.
56. Weinstein S. Hand instrument. The "Shirt-Pocket Portable" Nerve Tester. Care and Use Manual. San Jose, CA: North Coast Medical Inc (1996).
57. Abbott D, Jackson G. iBrain® - Software for analysis and visualisation of functional MR images. Neuroimage (2001) 13(6):S59. doi:10.1016/S1053-8119(01)91402-8.
58. Cordes D, Haughton VM, Arfanakis K, Carew JD, Turski PA, Moritz CH, et al. Frequencies contributing to functional connectivity in the cerebral cortex in "resting-state" data. AJNR Am J Neuroradiol (2001) 22:1326-33.
59. Carey LM, Abbott A, Harvey M, Puce A, Seitz R. Dynamic texture perception for dominant and non-dominant hands within individuals: an fMRI study in adult healthy volunteers. Neuroimage (2008) 41(Suppl 1):S146. doi:10.1016/j.neuroimage.2008.04.008.
60. EickhoffSB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, et al. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage (2005) 25(4):1325-35. doi:10.1016/j.neuroimage.2004.12.034.
61. Johansen-Berg H, Behrens TEJ, Sillery E, Ciccarelli O, Thompson AJ, Smith SM, et al. Functional-anatomical validation and individual variation of diffusion tractography-based segmentation of the human thalamus. Cereb Cortex (2005) 15(1):31-9. doi:10.1093/cercor/bhh105.
62. Biswal B, Yetkin FZ, Haughton VM, Hyde JS. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med (1995) 34(4):537-41. doi:10.1002/mrm.1910340409.
63. Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci U S A (2005) 102(27):9673-8. doi:10.1073/pnas.0504136102.
64. Rorden C, Brett M. Stereotaxic display of brain lesions. Behav Neurol (2000) 12:191-200. doi:10.1155/2000/421719.
65. Seitz RJ, Hoflich P, Binkofski F, Tellmann L, Herzog H, Freund H-J. Role of the premotor cortex in recovery from middle cerebral artery infarction. Arch Neurol (1998) 55(8):1081-8. doi:10.1001/archneur.55.8.1081.
66. Dijkerman HC, de Haan EH. Somatosensory processes subserving perception and action. Behav Brain Sci (2007) 30(2):189-201. doi:10.1017/S0140525X07001392.
67. Carey LM, Abbott DF, Egan GF, O'Keefe GJ, Jackson GD, Bernhardt J, et al. Evolution of brain activation with good and poor motor recovery after stroke. Neurorehabil Neural Repair (2006) 20:24-41. doi:10.1177/1545968305283053.
68. Ward NS, Brown MM, Thompson AJ, Frackowiak RSJ. Neural correlates of motor recovery after stroke: a longitudinal fMRI study. Brain (2003) 126:2476-96. doi:10.1093/brain/awg145.
69. Petersen SE, Posner MI. The attention system of the human brain: 20 years after. Annu Rev Neurosci (2012) 35:73-89. doi:10.1146/annurev-neuro-062111-150525.
70. Boly M, Balteau E, Schnakers C, Degueldre C, Moonen G, Luxen A, et al. Baseline brain activity fluctuations predict somatosensory perception in humans. Proc Natl Acad Sci U S A (2007) 104(29):12187-92. doi:10.1073/pnas.0611404104.
71. Langner R, EickhoffSB. Sustaining attention to simple tasks: a meta-analytic review of the neural mechanisms of vigilant attention. Psychol Bull (2013) 139(4):870-900. doi:10.1037/a0030694.
72. Buckner RL, Krienen FM, Castellanos A, Diaz JC, Yeo BT. The organization of the human cerebellum estimated by intrinsic functional connectivity. J Neurophysiol (2011) 106:2322-45. doi:10.1152/jn.00339.2011.
73. Staines WR, Graham SJ, Black SE, McIlroy WE. Task-relevant modulation of contralateral and ipsilateral primary somatosensory cortex and the role of prefrontal-cortical sensory gating systems. Neuroimage (2002) 15(1):190-9. doi:10.1006/nimg.2001.0953.
74. Kaas JH. Is most of neural plasticity in the thalamus cortical? Proc Natl Acad Sci U S A (1999) 96(14):7622-3. doi:10.1073/pnas.96.14.7622.
75. Jain N, Qi HX, Collins CE, Kaas JH. Large-scale reorganization in the somatosensory cortex and thalamus after sensory loss in macaque monkeys. J Neurosci (2008) 28(43):11042-60. doi:10.1523/JNEUROSCI. 2334-08.2008.
76. Waites AB, Stanislavsky A, Abbott DF, Jackson GD. Effect of prior cognitive state on resting state networks measured with functional connectivity. Hum Brain Mapp (2005) 24:59-68. doi:10.1002/hbm.20069.
77. New AB, Robin DA, Parkinson AL, Duffy JR, McNeil MR, Piguet O, et al. Altered resting-state network connectivity in stroke patients with and without apraxia of speech. Neuroimage Clin (2015) 8:429-39. doi:10.1016/j.nicl.2015.03.013.
78. Liu TT. Neurovascular factors in resting-state functional MRI. Neuroimage (2013) 80:339-48. doi:10.1016/j.neuroimage.2013.04.071.
79. Veldsman M, Cumming T, Brodtmann A. Beyond BOLD: optimizing functional imaging in stroke populations. Hum Brain Mapp (2015) 36(4):1620-36. doi:10.1002/hbm.22711.
80. de Haan B, Rorden C, Karnath H-O. Abnormal perilesional BOLD signal is not correlated with stroke patients' behaviour. Front Hum Neurosci (2013) 7:669. doi:10.3389/fnhum.2013.00669.
81. Chang C, Thomason ME, Glover GH. Mapping and correction of vascular hemodynamic latency in the BOLD signal. Neuroimage (2008) 43:90-102. doi:10.1016/j.neuroimage.2008.06.030.
82. Carey LM. Sensory loss in stroke patients: effective training of tactile and proprioceptive discrimination. Arch Phys Med Rehabil (1993) 74:602-11. doi:10.1016/0003-9993(93)90158-7.
83. Buch ER, Modir Shanechi A, Fourkas AD, Weber C, Birbaumer N, Cohen LG. Parietofrontal integrity determines neural modulation associated with grasping imagery after stroke. Brain (2012) 135:596-614. doi:10.1093/brain/awr331.
84. EickhoffSB, Jbabdi S, Caspers S, Laird AR, Fox PT, Zilles K, et al. Anatomical and functional connectivity of cytoarchitectonic areas within the human parietal operculum. J Neurosci (2010) 30:6409-21. doi:10.1523/JNEUROSCI. 5664-09.2010.
85. Tame L, Braun C, Lingnau A, Schwarzbach J, Demarchi G, Hegner YL, et al. The contribution of primary and secondary somatosensory cortices to the representation of body parts and body sides: an fMRI adaptation study. J Cogn Neurosci (2012) 24:2306-20. doi:10.1162/jocn_a_00272.
86. Burton H, Sinclair RJ, Wingert JR, Dierker DL. Multiple parietal operculum subdivisions in humans: tactile activation maps. Somatosens Mot Res (2008) 25:149-62. doi:10.1080/08990220802249275.
87. Pleger B, Foerster AF, Ragert P, Dinse HR, Schwenkreis P, Malin J-P, et al. Functional imaging of perceptual learning in human primary and secondary somatosensory cortex. Neuron (2003) 40:643-53. doi:10.1016/S0896-6273(03)00677-9.
88. Romo R, Hernandez A, Zainos A, Lemus L, Brody CD. Neuronal correlates of decision-making in secondary somatosensory cortex. Nat Neurosci (2002) 5:1217-25. doi:10.1038/nn950.
89. Tomasi D, Volkow ND. Association between functional connectivity hubs and brain networks. Cereb Cortex (2011) 21(9):2003-13. doi:10.1093/cercor/bhq268.