Damage to fronto-parietal networks impairs motor imagery ability after stroke: A voxel-based lesion symptom mapping study

Frontiers in Behavioral Neuroscience

Volumn 10, Issue FEB, 2016, Pages

  Oostra, Kristine M ^a   Van Bladel, Anke ^b   Vanhoonacker, Ann C L ^a   Vingerhoets, Guy ^b  

^a GHENT UNIVERSITY HOSPITAL   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

Basal ganglia; Lesion symptom mapping; Motor imagery; Stroke; White matter

Indexed keywords

ADOLESCENT; ADULT; AGED; ARTICLE; BRAIN DAMAGE; BRAIN FUNCTION; BRAIN MAPPING; BRAIN REGION; CEREBROVASCULAR ACCIDENT; CLINICAL ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; CORONA RADIATA (BRAIN); DISEASE ASSOCIATION; FEMALE; FRONTAL LOBE; HEMIPLEGIA; HUMAN; IMAGERY; MALE; MOTOR IMAGERY; MOTOR IMAGERY IMPAIRMENT; NERVE CELL NETWORK; NEUROIMAGING; PARIETAL LOBE; PREFRONTAL CORTEX; PREMOTOR CORTEX; PUTAMEN; QUESTIONNAIRE; VOXEL BASED MORPHOMETRY; WHITE MATTER; WHITE MATTER LESION;

EID: 84960074737     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2016.00005     Document Type: Article

References (62)

1. Baier, B., Karnath, H. O., Dieterich, M., Birklein, F., Heinze, C., and Müller, N. (2010). Keeping memory clear and stable-the contribution of human basal ganglia and prefrontal cortex to working memory. J. Neurosci. 30, 9788-9792. doi: 10.1523/JNEUROSCI.1513-10.2010
2. Bakker, M., De Lange, F. P., Helmich, R., Scheeringa, R., Bloem, B., and Toni, I. (2008). Cerebral correlates of motor imagery of normal and precision gait. Neuroimage 41, 998-1010. doi: 10.1016/j.neuroimage.2008.03.020
3. Bates, E., Wilson, S., Saygin, A., Dick, F., Sereno, M., Knight, R. T., et al. (2003).Voxel-based lesion-symptom mapping. Neurosci 6, 448-450. doi: 10.1038/nn1050
4. Binkofski, F., Amunts, K., Stephan, K., Posse, S., Schormann, T., Freund, H.-J., et al. (2000). Broca’s region subserves imagery of motion: a combined cytoarchitectonic and fMRI study. Hum. Brain. Mapp. 11, 273-285. doi: 10.1002/1097-0193
5. Burianová, H., Marstaller, L., Sowman, P., Tesan, G., Rich, A., Williams, M., et al. (2013). Multimodal functional imaging of motor imagery using a novel paradigm. Neuroimage 71, 50-58. doi: 10.1016/j.neuroimage.2013.01.001
6. Butler, A. (2006). Mental practice with motor imagery: evidence for motor recovery and cortical reorganization after stroke. Arch. Phys. Med. Rehabil. 87(Suppl. 2), S2-S11. doi: 10.1016/j.apmr.2006.08.326
7. Butler, A. J., Cazeaux, J., Fidler, A., Jansen, J., Lefkove, N., Gregg, M., et al. (2012). The movement imagery questionnaire-revised second edition (miq-rs) is a reliable and valid tool for evaluating motor imagery in stroke populations. J. Evid. Based Compl. Alternat. Med. 2012:497289. doi: 10.1155/2012/497289
8. Cho, H., Kim, J., and Lee, G. (2012). Effects of motor imagery training on balance and gait abilities in post-stroke patients: a randomized controlled trial. Clin. Rehabil. 27, 675-680. doi: 10.1177/0269215512464702
9. Confalonieri, L., Pagnoni, G., Barsalou, L. W., Rajendra, J., Eickhoff, S., and Butler, A. (2012). Brain activation in primary motor and somatosensory cortices during motor imagery: correlates with motor imagery ability in stroke patients. ISRN Neurol. 2012:613595. doi: 10.5402/2012/613595
10. Decety, J., and Jeannerod, M. (1996). Mentally simulated movements in virtual reality: does Fitts’s law hold in motor imagery. Behav. Brain Res. 72, 127-134. doi: 10.1016/0166-4328(96)00141-6
11. de Vries, S., Tepper, M., Feenstra, W., Oosterveld, H., Boonstra, A. M., and Otten, B. (2013). Motor imagery ability in stroke patients: the relationship between implicit and explicit motor imagery measures. Front. Hum. Neurosci. 7:790. doi: 10.3389/fnhum.2013.00790
12. Di Rienzo, F., Collet, C., Hoyek, N., and Guillot, A. (2014). Impact of neurologic deficits on motor imagery: a systematic review of clinical evaluations. Neuropsychol. Rev. 24, 116-147. doi: 10.1007/s11065-014-9257-6
13. Doyon, J., Bellec, P., Amsel, R., Penhune, V., Monchi, O., Carrier, J., et al. (2009). Contributions of the basal ganglia and functionally related brain structures to motor learning. Behav. Brain Res. 199, 61-75. doi: 10.1016/j.bbr.2008.11.012
14. Forkel, S., Thiebaut de Schotten, M., Kawadler, J., Dell’Aqua, F., Danek, A., and Catani, M. (2014). The anatomy of fronto-occipital connections from early blunt dissections to contemporary tractography. Cortex 56, 73-84. doi: 10.1016/j.cortex.2012.09.005
15. Fugl-Meyer, A. R., Jääskö, L., Leyman, I., Olsson, S., and Steglind, S. (1975). The post-stroke hemiplegic patient: a method for evaluation of physical performance. Scand. J. Rehabil. Med. 7, 13-31.
16. Gerardin, E., Sirigu, A., Lehérichy, S., Poline, J., Gaymard, B., Marsault, C. (2000). Partially overlapping neural networks for real and imagined hand movements. Cereb. Cortex 10, 1093-1104. doi: 10.1093/cercor/10.11.1093
17. Goebel, R. (2012). BrainVoyager-past, present, future. Neuroimage 62, 748-756. doi: 10.1016/j.neuroimage.2012.01.083
18. Gregg, M., Hall, C., and Butler, A. (2010). The MIQ-RS: a suitable option for examining movement imagery ability. J. Evid. Based Compl. Alternat. Med. 7, 249-257. doi: 10.1093/ecam/nem170
19. Grouios, G. (1992). Mental practice: a review. J. Sport Behav. 15, 42-54
20. Guillot, A., and Collet, C. (2005). Contribution from neurophysiological and psychological methods to the study of motor imagery. Brain Res. Rev. 50, 387-397. doi: 10.1016/j.brainresrev.2005.09.004
21. Guillot, A., Collet, C., Nguyen, V., Malouin, F., Richards, C., and Doyon, J. (2008). Functional neuroanatomical networks associated with expertise in motor imagery. Neuroimage 41, 1471-1483. doi: 10.1016/j.neuroimage.2008.03.042
22. Hall, C. (1997). Measuring Movement imagery abilities: a revision of the movement Imagery questionnaire. J. Mental Image 21, 143-154
23. Heremans, E., Nieuwboer, A., Spildooren, J., De Bondt, S., D’Hooge, A., Helsen, P., et al. (2012). Cued motor imagery in patients with multiple sclerosis. Neuroscience 206, 115-121. doi: 10.1016/j.neuroscience.2011.12.060
24. Hétu, S., Grégoire, M., Saimpont, A., Coll, M.-P., Eugène, F., Michon, P.-E., et al. (2013).The neural network of motor imagery: an ALE meta-analysis. Neurosci. Biobehav. Rev. 37, 930-949. doi: 10.1016/j.neubiorev.2013.03.017
25. Ietswaart, M., Johnston, M., Dijkerman, C., Joice, S., Scott, C., MacWalter, R., et al. (2011). Mental practice with motor imagery in stroke recovery: randomized controlled trial of efficacy. Brain 134, 1373-1386. doi: 10.1093/brain/awr077
26. Kraeutner, S., Gionfriddo, A., Bardouille, T., and Boe, S. (2014). Motor imagery-based brain activity parallels that of motor execution: evidence from magnetic source imaging of cortical oscillations. Brain Res. 1588, 81-91. doi: 10.1016/j.brainres.2014.09.001
27. Kraeutner, S., Keeler, L., and Boe, S. (2015a). Motor imagery-based skill acquisition disrupted following rTMS of the inferior parietal lobe. Exp. Brain Res. doi: 10.1007/s00221-015-4472-9. [Epub ahead of print].
28. Kraeutner, S., MacKenzie, L., Westwood, D., and Boe, S. (2015b). Characterizing skill acquisition through motor imagery with no prior physical practice. J. Exp. Psychol. Hum. Percept. Perform. doi: 10.1037/xhp0000148. [Epub ahead of print].
29. Lacourse, M., Orr, E., Cramer, S., and Cohen, M. (2005). Brain activation during execution and motor imagery of novel and skilled sequential hand movements. Neuroimage 27, 505-519. doi: 10.1016/j.neuroimage.2005.04.025
30. Li, C. (2000). Impairment of motor imagery in putamen lesions in humans. Neurosci. Lett. 287, 13-16. doi: 10.1016/S0304-3940(00)01164-2
31. Liepert, J., Greiner, J., Nedelko, V., and Dettmers, C. (2012). Reduced upper limb sensation impairs mental chronometry for motor imagery after stroke: clinical and electrophysiological findings. Neurorehabil. Neural Repair 26, 470-478. doi: 10.1177/1545968311425924
32. Liu, K. (2004). Mental imagery for promoting relearning for people after stroke: a randomized controlled trial. Arch. Phys. Med. Rehabil. 85, 1403-1408. doi: 10.1016/j.apmr.2003.12.035
33. Lo, R., Gitelman, D., Levy, R., Hulvershorn, J., and Parrish, T. (2010). Identification of critical areas for motor function recovery in chronic stroke subjects using voxel-based lesion symptom mapping. Neuroimage 49, 9-18. doi: 10.1016/j.neuroimage.2009.08.044
34. Lorey, B., Pilgramm, S., Bischoff, M., Stark, R., Vaitl, R., Kindermann, S., et al. (2011). Activation of the parieto-premotor network is associated with vivid motor imagery- a parametric fMRI study. PLoS ONE 6:e20368. doi: 10.1371/journal.pone.0020368
35. Lotze, M., and Cohen, L. (2006). Volition and imagery in neurorehabilitation. Cogn. Behav. Neurol. 19, 135-140. doi: 10.1097/01.wnn.0000209875.56060.06
36. Lotze, M., and Halsband, U. (2006). Motor imagery. J. Physiol. 99, 386-395. doi: 10.1016/j.jphysparis.2006.03.012
37. Makris, N., Papadimitrtriou, G., Sorg, S., Kennedy, D., Caviness, V., and Pandya, D. (2007).The occipitofrontal fascicle in humans: a quantitive in vivo, DT-MRI study. Neuroimage 37, 1100-1111. doi: 10.1016/j.neuroimage.2007.05.042
38. Malouin, F. (2004). Working memory and mental practice outcomes after stroke. Arch. Phys. Med. Rehabil. 85, 177-183. doi: 10.1016/S0003-9993(03)00771-8
39. Malouin, F. (2008). Reliability of mental chronometry for assessing motor imagery ability after stroke. Arch. Phys. Med. Rehabil. 89, 311-319. doi: 10.1016/j.apmr.2007.11.006
40. Malouin, F., and Richards, C. (2010). Mental practice for relearning lokomotor skills. Phys. Ther. 90, 240-251. doi: 10.2522/ptj.20090029
41. Malouin, F., Richards, C., Durand, A., and Doyon, J. (2008). Clinical assessment of motor imagery after stroke. Neurorehabil. Neural Repair 22, 330-340. doi: 10.1177/1545968307313499
42. McAvinue, L. (2008). Measuring motor imagery ability: a review. Eur. J. Cogn. Psychol. 20, 232-251. doi: 10.1080/09541440701394624
43. McInnes, K., Friesen, C., and Boe, S. (2015). Specific Brain lesions impair explicit motor imagery ability: a systematic review of the evidence. Arch. Phys. Med. Rehabil. doi: 10.1016/j.apmr.2015.07.012. [Epub ahead of print]
44. Monchi, O., Petrides, M., Strafella, A., Worsley, K., and Doyon, J. (2006). Functional role of the basal ganglia in the planning and execution of actions. Ann. Neurol. 59, 257-264. doi: 10.1002/ana.20742
45. Munzert, J., Lorey, B., and Zentgraf, K. (2009). Cognitive motor processes: the role of motor imagery in the study of motor presentations. Brain Res. Rev. 60, 306-326. doi: 10.1016/j.brainresrev.2008.12.024
46. Oishi, K., Faria, A., van Zijl, P., and Mori, S. (2011). MRI Atlas of Human White Matter, 2nd Edn. London: Academic Press.
47. Oostra, K. M., Oomen, A., Vanderstraeten, G., and Vingerhoets, G. (2015). Influence of motor imagery training on gait rehabilitation in sub-acute stroke: a randomized controlled trial. J. Rehabil. Med. 47, 204-209. doi: 10.2340/16501977-1908
48. Page, S., Levine, P., and Leonard, A. (2007). Mental practice in chronic stroke. Results of a randomized, placebo-controlled trial. Stroke 38, 1293-1297. doi: 10.1161/01.STR.0000260205.67348.2b
49. Page, S., Szaflarski, J., Eliassen, J., Pan, H., and Cramer, S. (2009). Cortical plasticity following motor skill learning during mental practice in stroke. Neurorehabil. Neural Repair 23, 382-388. doi: 10.1177/1545968308326427
50. Rorden, C., and Brett, M. (2000). Stereotaxic display of brain lesions. Behav. Neurol. 12, 191-200. doi: 10.1155/2000/421719
51. Rorden, C., Karnath, H. O., and Bonilha, L. (2007). Improving lesion-symptom mapping. J. Cogn. Neurosci. 19, 1081-1088. doi: 10.1162/jocn.2007.19.7.1081
52. Sabaté, M., Gonzáles, B., and Rodrígues, M. (2004). Brain lateralization of motor imagery: motor planning asymmetry as a cause of movement lateralization. Neuropsychologia 42, 1041-1049. doi: 10.1016/j.neuropsychologia.2003.12.015
53. Schuster, C., Hilfiker, R., Amft, O., Scheidhauer, A., Andrews, B., Butler, J. (2011). Best Practice for motor imagery: a systematic literature review on motor imagery training elements in five different disciplines. BMC Med 9:75. doi: 10.1186/1741-7015-9-75
54. Sharma, N., Baron, J. C., and Rowe, J. (2009). Motor imagery after stroke: relating outcome to motor network connectivity. Ann. Neurol. 66, 604-616. doi: 10.1002/ana.21810
55. Sharma, N., Pomeroy, V., and Baron, J. C. (2006). Motor Imagery, a backdoor to the motor system after stroke? Stroke 37, 1941-1952. doi: 10.1161/01.STR.0000226902.43357.fc
56. Sirigu, A., Cohen, L., Duhamel, R., Pillon, B., Dubois, B., Agid, Y., et al. (1995). Congruent unilateral impairments for real and imagined hand movements. Neuroreport 6, 997-1001. doi: 10.1097/00001756-199505090-00012
57. Sirigu, A., Duhamel, J. R., Cohen, L., Pillon, B., Dubois, B., and Agid, Y. (1996). The mental representation of hand movements after parietal cortex damage. Science 273, 1564-1568. doi: 10.1126/science.273.5281.1564
58. Stinear, C., Fleming, M., Barber, P., and Byblow, W. (2007). Lateralization of motor imagery following stroke. Clin. Neurophysiol. 118, 1794-1801. doi: 10.1016/j.clinph.2007.05.008
59. Szameitat, A. J., Shen, S., Conforto, A., and Sterr, A. (2012). Cortical activation during executed, imagined, observed, and passive wrist movements in healthy volunteers and stroke patients. Neuroimage 62, 266-280. doi: 10.1016/j.neuroimage.2012.05.009
60. Timmermans, A., Verbunt, J. A., van Woerden, R., Moennekens, M., Pernot, D. H., and Seelen, H. A. (2013). Effect of mental practice on the improvement of function and daily activity performance of the upper extremity in patients with subacute stroke: a randomized clinical trial. J. Am. Med. Dir. Assoc. 14, 204-212. doi: 10.1016/j.jamda.2012.10.010
61. Vry, M. S., Saur, D., Rijntjes, M., Umarova, R., Kellmeyer, P., Schnell, S., et al. (2012). Ventral and dorsal fiber systems for imagined and executed movement. Exp. Brain Res. 219, 203-216. doi: 10.1007/s00221-012-3079-7
62. Zimmermann, P., Fimm, B., and Vera Fimm. (2012). Test of Attentional Performance Version 2.3. Herzogenrath: Psychologisches Testsysteme.