Experimental Brain Research

, Volume 229, Issue 4, pp 561–570 | Cite as

Imagined actions in multiple sclerosis patients: evidence of decline in motor cognitive prediction

  • Andrea Tacchino
  • Marco Bove
  • Ludovico Pedullà
  • Mario Alberto Battaglia
  • Charalambos Papaxanthis
  • Giampaolo Brichetto
Research Article

Abstract

Motor imagery is a mental process during which subjects internally simulate a movement without any motor output. Mental and actual movement durations are similar in healthy adults (isochrony) while temporal discrepancies (anisochrony) could be an expression of neurological deficits on action representation. It is unclear whether patients with multiple sclerosis (PwMS) preserve the capacity to simulate their own movements. This study investigates the ability of PwMS to predict their own actions by comparing temporal features of dominant and non-dominant actual and mental actions. Fourteen PwMS and nineteen healthy subjects (HS) were asked to execute and to imagine pointing arm movements among four pairs of targets of different sizes. Task duration was calculated for both actual and mental movements by an optoelectronic device. Results showed temporal consistency and target-by-target size modulation in actual movements through the four cycles for both groups with significantly longer actual and mental movement durations in PwMS with respect to HS. An index of performance (IP) was used to examine actual/mental isochrony properties in the two groups. Statistical analysis on IP showed in PwMS significantly longer actual movement durations with respect to mental movement durations (anisochrony), more relevant for the non-dominant than dominant arm. Mental prediction of motor actions is not well preserved in MS where motor and cognitive functional changes are present. Differences in performing imagined task with dominant and non-dominant arm could be related to increased cognitive effort required for performing non-dominant movements.

Keywords

Multiple sclerosis Motor imagery Forward internal model Isochrony Motor cognition 

References

  1. Arrondo G, Alegre M, Sepulcre J, Iriarte J, Artieda J, Villoslada P (2009) Abnormalities in brain synchronization are correlated with cognitive impairment in multiple sclerosis. Mult Scler 15(4):509–516PubMedCrossRefGoogle Scholar
  2. Avanzino L, Giannini A, Tacchino A, Pelosin E, Ruggeri P, Bove M (2009) Motor imagery influences the execution of repetitive finger opposition movements. Neurosci Lett 466(1):11–15PubMedCrossRefGoogle Scholar
  3. Baeck JS, Kim YT, Seo JH, Ryeom HK, Lee J, Choi SM, Woo M, Kim W, Kim JG, Chang Y (2012) Brain activation patterns of motor imagery reflect plastic changes associated with intensive shooting training. Behav Brain Res 234(1):26–32PubMedCrossRefGoogle Scholar
  4. Bakker M, de Lange FP, Stevens JA, Toni I, Bloem BR (2007) Motor imagery of gait: a quantitative approach. Exp Brain Res 179(3):497–504PubMedCrossRefGoogle Scholar
  5. Benedict RH, Carone DA, Bakshi R (2004a) Correlating brain atrophy with cognitive dysfunction, mood disturbances, and personality disorder in multiple sclerosis. J Neuroimaging 14(3 Suppl):36S–45SPubMedCrossRefGoogle Scholar
  6. Benedict RH, Weinstock-Guttman B, Fishman I, Sharma J, Tjoa CW, Bakshi R (2004b) Prediction of neuropsychological impairment in multiple sclerosis: comparison of conventional magnetic resonance imaging measures of atrophy and lesion burden. Arch Neurol 61(2):226–230PubMedCrossRefGoogle Scholar
  7. Benedict RH, Holtzer R, Motl RW, Foley FW, Kaur S, Hojnacki D, Weinstock-Guttman B (2011) Upper and lower extremity motor function and cognitive impairment in multiple sclerosis. J Int Neuropsychol Soc 17(4):643–653PubMedCrossRefGoogle Scholar
  8. Bergendal G, Fredrikson S, Almkvist O (2007) Selective decline in information processing in subgroups of multiple sclerosis: an 8-year longitudinal study. Eur Neurol 57(4):193–202PubMedCrossRefGoogle Scholar
  9. Bodling AM, Denney DR, Lynch SG (2009) Cognitive aging in patients with multiple sclerosis: a cross-sectional analysis of speeded processing. Arch Clin Neuropsychol 24(8):761–767PubMedCrossRefGoogle Scholar
  10. Bohannon RW, Smith MB (1987) Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther 67(2):206–207PubMedGoogle Scholar
  11. Bonzano L, Tacchino A, Roccatagliata L, Abbruzzese G, Mancardi GL, Bove M (2008) Callosal contributions to simultaneous bimanual finger movements. J Neurosci 28(12):3227–3233PubMedCrossRefGoogle Scholar
  12. Bonzano L, Tacchino A, Roccatagliata L, Mancardi GL, Abbruzzese G, Bove M (2011) Structural integrity of callosal midbody influences intermanual transfer in a motor reaction-time task. Hum Brain Mapp 32(2):218–228PubMedCrossRefGoogle Scholar
  13. Caeyenberghs K, Tsoupas J, Wilson PH, Smits-Engelsman BC (2009) Motor imagery development in primary school children. Dev Neuropsychol 34(1):103–121PubMedCrossRefGoogle Scholar
  14. Casadio M, Sanguineti V, Morasso P, Solaro C (2008) Abnormal sensorimotor control, but intact force field adaptation, in multiple sclerosis subjects with no clinical disability. Mult Scler 14(3):330–342PubMedCrossRefGoogle Scholar
  15. Chiaravalloti ND, DeLuca J (2008) Cognitive impairment in multiple sclerosis. The Lancet Neurology 7(12):1139–1151CrossRefGoogle Scholar
  16. Cho HY, Kim JS, Lee GC (2012) Effects of motor imagery training on balance and gait abilities in post-stroke patients: a randomized controlled trial. Clin Rehabil [Epub ahead of print]Google Scholar
  17. Choudhury S, Charman T, Bird V, Blakemore SJ (2007) Development of action representation during adolescence. Neuropsychologia 45(2):255–262PubMedCrossRefGoogle Scholar
  18. Colorado RA, Shukla K, Zhou Y, Wolinsky JS, Narayana PA (2012) Multi-task functional MRI in multiple sclerosis patients without clinical disability. Neuroimage 59(1):573–581PubMedCrossRefGoogle Scholar
  19. Compston A, Coles A (2008) Multiple sclerosis. Lancet 372(9648):1502–1517PubMedCrossRefGoogle Scholar
  20. Courtine G, Papaxanthis C, Gentili R, Pozzo T (2004) Gait-dependent motor memory facilitation in covert movement execution. Brain Res Cogn Brain Res 22(1):67–75PubMedCrossRefGoogle Scholar
  21. Danckert J, Ferber S, Doherty T, Steinmetz H, Nicolle D, Goodale MA (2002) Selective, non-lateralized impairment of motor imagery following right parietal damage. Neurocase 8(3):194–204PubMedCrossRefGoogle Scholar
  22. Decety J (1996) Do imagined and executed actions share the same neural substrate? Brain Res Cogn Brain Res 3(2):87–93PubMedCrossRefGoogle Scholar
  23. Decety J, Jeannerod M (1995) Mentally simulated movements in virtual reality: does Fitts’s law hold in motor imagery? Behav Brain Res 72(1–2):127–134PubMedCrossRefGoogle Scholar
  24. Decety J, Jeannerod M, Prablanc C (1989) The timing of mentally represented actions. Behav Brain Res 34(1–2):35–42PubMedCrossRefGoogle Scholar
  25. DeLuca J, Chelune GJ, Tulsky DS, Lengenfelder J, Chiaravalloti ND (2004) Is speed of processing or working memory the primary information processing deficit in multiple sclerosis? J Clin Exp Neuropsychol 26(4):550–562PubMedCrossRefGoogle Scholar
  26. Demougeot L, Papaxanthis C (2011) Muscle fatigue affects mental simulation of action. J Neurosci 31(29):10712–10720PubMedCrossRefGoogle Scholar
  27. Denney DR, Lynch SG, Parmenter BA, Horne N (2004) Cognitive impairment in relapsing and primary progressive multiple sclerosis: mostly a matter of speed. J Int Neuropsychol Soc 10(7):948–956PubMedCrossRefGoogle Scholar
  28. Dominey P, Decety J, Broussolle E, Chazot G, Jeannerod M (1995) Motor imagery of a lateralized sequential task is asymmetrically slowed in hemi-Parkinson’s patients. Neuropsychologia 33(6):727–741PubMedCrossRefGoogle Scholar
  29. Fadiga L, Craighero L (2004) Electrophysiology of action representation. J Clin Neurophysiol 21(3):157–169PubMedCrossRefGoogle Scholar
  30. Fischer JS, Rudick RA, Cutter GR, Reingold SC (1999) The multiple sclerosis functional composite measure (MSFC): an integrated approach to MS clinical outcome assessment. National MS Society Clinical Outcomes Assessment Task Force. Mult Scler 5(4):244–250PubMedGoogle Scholar
  31. Flachenecker P, Kumpfel T, Kallmann B, Gottschalk M, Grauer O, Rieckmann P, Trenkwalder C, Toyka KV (2002) Fatigue in multiple sclerosis: a comparison of different rating scales and correlation to clinical parameters. Mult Scler 8(6):523–526PubMedCrossRefGoogle Scholar
  32. Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12(3):189–198PubMedCrossRefGoogle Scholar
  33. Frak V, Paulignan Y, Jeannerod M (2001) Orientation of the opposition axis in mentally simulated grasping. Exp Brain Res 136(1):120–127PubMedCrossRefGoogle Scholar
  34. Gentili R, Cahouet V, Ballay Y, Papaxanthis C (2004) Inertial properties of the arm are accurately predicted during motor imagery. Behav Brain Res 155(2):231–239PubMedCrossRefGoogle Scholar
  35. Gentili R, Papaxanthis C, Pozzo T (2006) Improvement and generalization of arm motor performance through motor imagery practice. Neuroscience 137(3):761–772PubMedCrossRefGoogle Scholar
  36. Gentili R, Han CE, Schweighofer N, Papaxanthis C (2010) Motor learning without doing: trial-by-trial improvement in motor performance during mental training. J Neurophysiol 104(2):774–783PubMedCrossRefGoogle Scholar
  37. Gueugneau N, Mauvieux B, Papaxanthis C (2009) Circadian modulation of mentally simulated motor actions: implications for the potential use of motor imagery in rehabilitation. Neurorehabil Neural Repair 23(3):237–245PubMedGoogle Scholar
  38. Helmich RC, de Lange FP, Bloem BR, Toni I (2007) Cerebral compensation during motor imagery in Parkinson’s disease. Neuropsychologia 45(10):2201–2215PubMedCrossRefGoogle Scholar
  39. Heremans E, Feys P, Nieuwboer A, Vercruysse S, Vandenberghe W, Sharma N, Helsen W (2011) Motor imagery ability in patients with early- and mid-stage Parkinson disease. Neurorehabil Neural Repair 25(2):168–177PubMedCrossRefGoogle Scholar
  40. Heremans E, D’Hooge A M, De Bondt S, Helsen W, Feys P (2012) The relation between cognitive and motor dysfunction and motor imagery ability in patients with multiple sclerosis. Mult Scler 18(3):1303–1309Google Scholar
  41. Hong IK, Choi JB, Lee JH (2012) Cortical changes after mental imagery training combined with electromyography-triggered electrical stimulation in patients with chronic stroke. Stroke J Cereb Circ 43(9):2506–2509CrossRefGoogle Scholar
  42. Human Experimentation: Code of Ethics of the World Medical Association (Declaration of Helsinki) (1964) Can Med Assoc J 91(11):619Google Scholar
  43. Jackson PL, Lafleur MF, Malouin F, Richards CL, Doyon J (2003) Functional cerebral reorganization following motor sequence learning through mental practice with motor imagery. Neuroimage 20(2):1171–1180PubMedCrossRefGoogle Scholar
  44. Janculjak D, Mubrin Z, Brinar V, Spilich G (2002) Changes of attention and memory in a group of patients with multiple sclerosis. Clin Neurol Neurosurg 104(3):221–227PubMedCrossRefGoogle Scholar
  45. Jeannerod M (2001) Neural simulation of action: a unifying mechanism for motor cognition. Neuroimage 14(1 Pt 2):S103–S109PubMedCrossRefGoogle Scholar
  46. Jeannerod M, Decety J (1995) Mental motor imagery: a window into the representational stages of action. Curr Opin Neurobiol 5(6):727–732PubMedCrossRefGoogle Scholar
  47. Johnson SH (2000) Imagining the impossible: intact motor representations in hemiplegics. NeuroReport 11(4):729–732PubMedCrossRefGoogle Scholar
  48. Johnson SH, Sprehn G, Saykin AJ (2002) Intact motor imagery in chronic upper limb hemiplegics: evidence for activity-independent action representations. J Cogn Neurosci 14(6):841–852PubMedCrossRefGoogle Scholar
  49. Kagerer FA, Bracha V, Wunderlich DA, Stelmach GE, Bloedel JR (1998) Ataxia reflected in the simulated movements of patients with cerebellar lesions. Exp Brain Res 121(2):125–134PubMedCrossRefGoogle Scholar
  50. Lee M, Reddy H, Johansen-Berg H, Pendlebury S, Jenkinson M, Smith S, Palace J, Matthews PM (2000) The motor cortex shows adaptive functional changes to brain injury from multiple sclerosis. Ann Neurol 47(5):606–613PubMedCrossRefGoogle Scholar
  51. Mainero C, Caramia F, Pozzilli C, Pisani A, Pestalozza I, Borriello G, Bozzao L, Pantano P (2004) fMRI evidence of brain reorganization during attention and memory tasks in multiple sclerosis. Neuroimage 21(3):858–867PubMedCrossRefGoogle Scholar
  52. Maruff P, Wilson PH, De Fazio J, Cerritelli B, Hedt A, Currie J (1999) Asymmetries between dominant and non-dominant hands in real and imagined motor task performance. Neuropsychologia 37(3):379–384PubMedCrossRefGoogle Scholar
  53. McDonald WI, Compston A, Edan G, Goodkin D, Hartung HP, Lublin FD, McFarland HF, Paty DW, Polman CH, Reingold SC, Sandberg-Wollheim M, Sibley W, Thompson A, van den Noort S, Weinshenker BY, Wolinsky JS (2001) Recommended diagnostic criteria for multiple sclerosis: guidelines from the international panel on the diagnosis of multiple sclerosis. Ann Neurol 50(1):121–127PubMedCrossRefGoogle Scholar
  54. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113PubMedCrossRefGoogle Scholar
  55. Page SJ, Levine P, Leonard A (2007) Mental practice in chronic stroke: results of a randomized, placebo-controlled trial. Stroke J Cereb Circ 38(4):1293–1297CrossRefGoogle Scholar
  56. Papaxanthis C, Pozzo T, Skoura X, Schieppati M (2002) Does order and timing in performance of imagined and actual movements affect the motor imagery process? The duration of walking and writing task. Behav Brain Res 134(1–2):209–215PubMedCrossRefGoogle Scholar
  57. Papaxanthis C, Pozzo T, Kasprinski R, Berthoz A (2003) Comparison of actual and imagined execution of whole-body movements after a long exposure to microgravity. Neurosci Lett 339(1):41–44PubMedCrossRefGoogle Scholar
  58. Papaxanthis C, Paizis C, White O, Pozzo T, Stucchi N (2012) The relation between geometry and time in mental actions. PLoS ONE 7(11):e51191PubMedCrossRefGoogle Scholar
  59. Penner IK, Rausch M, Kappos L, Opwis K, Radu EW (2003) Analysis of impairment related functional architecture in MS patients during performance of different attention tasks. J Neurol 250(4):461–472PubMedCrossRefGoogle Scholar
  60. Personnier P, Paizis C, Ballay Y, Papaxanthis C (2008) Mentally represented motor actions in normal aging II. The influence of the gravito-inertial context on the duration of overt and covert arm movements. Behav Brain Res 186(2):273–283PubMedCrossRefGoogle Scholar
  61. Personnier P, Ballay Y, Papaxanthis C (2010a) Mentally represented motor actions in normal aging: III. Electromyographic features of imagined arm movements. Behav Brain Res 206(2):184–191PubMedCrossRefGoogle Scholar
  62. Personnier P, Kubicki A, Laroche D, Papaxanthis C (2010b) Temporal features of imagined locomotion in normal aging. Neurosci Lett 476(3):146–149PubMedCrossRefGoogle Scholar
  63. Ranganathan VK, Siemionow V, Liu JZ, Sahgal V, Yue GH (2004) From mental power to muscle power–gaining strength by using the mind. Neuropsychologia 42(7):944–956PubMedCrossRefGoogle Scholar
  64. Reddy H, Narayanan S, Arnoutelis R, Jenkinson M, Antel J, Matthews PM, Arnold DL (2000) Evidence for adaptive functional changes in the cerebral cortex with axonal injury from multiple sclerosis. Brain 123(Pt 11):2314–2320PubMedCrossRefGoogle Scholar
  65. Reicker LI, Tombaugh TN, Walker L, Freedman MS (2007) Reaction time: an alternative method for assessing the effects of multiple sclerosis on information processing speed. Arch Clin Neuropsychol 22(5):655–664PubMedCrossRefGoogle Scholar
  66. Rizzo MA, Hadjimichael OC, Preiningerova J, Vollmer TL (2004) Prevalence and treatment of spasticity reported by multiple sclerosis patients. Mult Scler 10(5):589–595PubMedCrossRefGoogle Scholar
  67. Rocca MA, Pagani E, Ghezzi A, Falini A, Zaffaroni M, Colombo B, Scotti G, Comi G, Filippi M (2003) Functional cortical changes in patients with multiple sclerosis and nonspecific findings on conventional magnetic resonance imaging scans of the brain. Neuroimage 19(3):826–836PubMedCrossRefGoogle Scholar
  68. Sharma N, Pomeroy VM, Baron JC (2006) Motor imagery: a backdoor to the motor system after stroke? Stroke J Cereb Circ 37(7):1941–1952CrossRefGoogle Scholar
  69. Simmons L, Sharma N, Baron JC, Pomeroy VM (2008) Motor imagery to enhance recovery after subcortical stroke: who might benefit, daily dose, and potential effects. Neurorehabil Neural Repair 22(5):458–467PubMedCrossRefGoogle Scholar
  70. Sirigu A, Duhamel JR, Cohen L, Pillon B, Dubois B, Agid Y (1996) The mental representation of hand movements after parietal cortex damage. Science 273(5281):1564–1568PubMedCrossRefGoogle Scholar
  71. Sirigu A, Cohen L, Zalla T, Pradat-Diehl P, Van Eeckhout P, Grafman J, Agid Y (1998) Distinct frontal regions for processing sentence syntax and story grammar. Cortex J Devot Study Nerv Syst Behav 34(5):771–778CrossRefGoogle Scholar
  72. Skoura X, Papaxanthis C, Vinter A, Pozzo T (2005) Mentally represented motor actions in normal aging. I. Age effects on the temporal features of overt and covert execution of actions. Behav Brain Res 165(2):229–239PubMedCrossRefGoogle Scholar
  73. Skoura X, Personnier P, Vinter A, Pozzo T, Papaxanthis C (2008) Decline in motor prediction in elderly subjects: right versus left arm differences in mentally simulated motor actions. Cortex J Devot Study Nerv Syst Behav 44(9):1271–1278CrossRefGoogle Scholar
  74. Skoura X, Vinter A, Papaxanthis C (2009) Mentally simulated motor actions in children. Dev Neuropsychol 34(3):356–367PubMedCrossRefGoogle Scholar
  75. Solaro C, Brichetto G, Casadio M, Roccatagliata L, Ruggiu P, Mancardi GL, Morasso PG, Tanganelli P, Sanguineti V (2007) Subtle upper limb impairment in asymptomatic multiple sclerosis subjects. Mult Scler 13(3):428–432PubMedCrossRefGoogle Scholar
  76. Staffen W, Mair A, Zauner H, Unterrainer J, Niederhofer H, Kutzelnigg A, Ritter S, Golaszewski S, Iglseder B, Ladurner G (2002) Cognitive function and fMRI in patients with multiple sclerosis: evidence for compensatory cortical activation during an attention task. Brain 125(Pt 6):1275–1282PubMedCrossRefGoogle Scholar
  77. Steens A, de Vries A, Hemmen J, Heersema T, Heerings M, Maurits N, Zijdewind I (2012a) Fatigue perceived by multiple sclerosis patients is associated with muscle fatigue. Neurorehabil Neural Repair 26(1):48–57PubMedCrossRefGoogle Scholar
  78. Steens A, Heersema DJ, Maurits NM, Renken RJ, Zijdewind I (2012b) Mechanisms underlying muscle fatigue differ between multiple sclerosis patients and controls: a combined electrophysiological and neuroimaging study. Neuroimage 59(4):3110–3118PubMedCrossRefGoogle Scholar
  79. Stinear CM, Byblow WD, Steyvers M, Levin O, Swinnen SP (2006) Kinesthetic, but not visual, motor imagery modulates corticomotor excitability. Exp Brain Res 168(1–2):157–164PubMedCrossRefGoogle Scholar
  80. Sweet LH, Rao SM, Primeau M, Mayer AR, Cohen RA (2004) Functional magnetic resonance imaging of working memory among multiple sclerosis patients. J Neuroimaging 14(2):150–157PubMedGoogle Scholar
  81. Tamir R, Dickstein R, Huberman M (2007) Integration of motor imagery and physical practice in group treatment applied to subjects with Parkinson’s disease. Neurorehabil Neural Repair 21(1):68–75PubMedCrossRefGoogle Scholar
  82. Wishart HA, Saykin AJ, McDonald BC, Mamourian AC, Flashman LA, Schuschu KR, Ryan KA, Fadul CE, Kasper LH (2004) Brain activation patterns associated with working memory in relapsing-remitting MS. Neurology 62(2):234–238PubMedCrossRefGoogle Scholar
  83. Wolpert DM, Flanagan JR (2001) Motor prediction. Curr Biol 11(18):R729–R732PubMedCrossRefGoogle Scholar
  84. Wolpert DM, Miall RC (1996) Forward models for physiological motor control. Neural Netw 9(8):1265–1279PubMedCrossRefGoogle Scholar
  85. Wolpert DM, Ghahramani Z, Flanagan JR (2001) Perspectives and problems in motor learning. Trends Cogn Sci 5(11):487–494PubMedCrossRefGoogle Scholar
  86. Zhang H, Xu L, Wang S, Xie B, Guo J, Long Z, Yao L (2011) Behavioral improvements and brain functional alterations by motor imagery training. Brain Res 1407:38–46PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Andrea Tacchino
    • 1
  • Marco Bove
    • 2
  • Ludovico Pedullà
    • 1
  • Mario Alberto Battaglia
    • 3
  • Charalambos Papaxanthis
    • 4
    • 5
  • Giampaolo Brichetto
    • 1
  1. 1.Scientific Research AreaItalian Multiple Sclerosis Foundation (FISM)GenoaItaly
  2. 2.Section of Human Physiology, Department of Experimental MedicineUniversity of GenoaGenoaItaly
  3. 3.Department of Physiopathology, Experimental Medicine and Public HealthUniversity of SienaSienaItaly
  4. 4.UFR STAPS, INSERM U1093 Cognition, Action, et Plasticité SensorimotriceUniversité de BourgogneDijonFrance
  5. 5.UFR STAPSUniversité de BourgogneDijonFrance

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