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Exploring motor and visual imagery in Amyotrophic Lateral Sclerosis

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An Erratum to this article was published on 02 March 2016

Abstract

Amyotrophic Lateral Sclerosis (ALS) is a motor neuron disease characterized by the progressive atrophy of both the first and the second motor neurons. Although the cognitive profile of ALS patients has already been defined by the occurrence of language dysfunctions and frontal deficit symptoms, it is less clear whether the degeneration of upper and lower motor neurons affects motor imagery abilities. Here, we directly investigated motor imagery in ALS patients by means of an established task that allows to examine the presence of the effects of the biomechanical constraints. Twenty-three ALS patients and 23 neurologically unimpaired participants have been administered with the (1) hand laterality task (HLT) in which participants were asked to judge the laterality of a rotated hand and the (2) mirror letter discrimination task (MLD) in which participants were asked to judge whether a rotated alphanumeric character was in its canonical or mirror-reversed form (i.e. control task). Results show that patients present the same pattern of performance as unimpaired participants at the MLD, while at the HLT, they present only partially with the effects of biomechanical constraints. Taken together, our findings provide evidences that motor imagery abilities, related to the mental simulation of an action, are affected by this progressive disease.

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References

  • Alivisatos B, Petrides M (1997) Functional activation of the human brain during mental rotation. Neuropsychologia 35(2):111–118

    Article  PubMed  CAS  Google Scholar 

  • Arbib MA (1981) Perceptual structures and distributed motor control. In: Brooks VB (ed) Handbook of physiology. Bethesda, American Physiological Society, pp 1449–1480

    Google Scholar 

  • Berlucchi G, Aglioti SM (2010) The body in the brain revisited. Exp Brain Res 200(1):25–35

    Article  PubMed  Google Scholar 

  • Booth JR, MacWhinney B, Thulborn KR, Sacco K, Voyvodic JT, Feldman HM (2000) Developmental and lesion effects in brain activation during sentence comprehension and mental rotation. Dev Neuropsychol 18(2):139–169

    Article  PubMed  CAS  Google Scholar 

  • Brady N, Maguinness C, Ni Choisdealbha A (2011) My hand or yours? Markedly different sensitivity to egocentric and allocentric views in the hand laterality task. PLoS One 6(8):e23316

    Article  PubMed  CAS  Google Scholar 

  • Brooks BR (1994) El Escorial World Federation of Neurology criteria for the diagnosis of amyotrophic lateral sclerosis. Subcommittee on Motor Neuron Diseases/Amyotrophic Lateral Sclerosis of the World Federation of Neurology Research Group on Neuromuscular Diseases and the El Escorial “Clinical limits of amyotrophic lateral sclerosis” workshop contributors. J Neurol Sci 124(Suppl):96–107

    Article  PubMed  Google Scholar 

  • Brooks BR, Miller RG, Swash M, Munsat TL (2000) El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord 1(5):293–299

    Article  PubMed  CAS  Google Scholar 

  • Carlesimo GA, Caltagirone C, Gainotti G, Fadda L, Gallassi R, Lorusso S, Marfia G, Marra C, Nocentini U, Parnetti L (1996) The mental deterioration battery: normative data, diagnostic reliability and qualitative analyses of cognitive impairment. Eur Neurol 36(6):378–384

    Article  PubMed  CAS  Google Scholar 

  • Cavina-Pratesi C, Monaco S, Fattori P, Galletti C, McAdam TD, Quinlan DJ, Goodale MA, Culham JC (2010) Functional magnetic resonance imaging reveals the neural substrates of arm transport and grip formation in reach-to-grasp actions in humans. J Neurosci 30(31):10306–10323

    Article  PubMed  CAS  Google Scholar 

  • Cedarbaum JM, Stambler N (1997) Performance of the Amyotrophic Lateral Sclerosis Functional Rating Scale (ALSFRS) in multicenter clinical trials. J Neurol Sci 152(Suppl 1):S1–S9

    Article  PubMed  Google Scholar 

  • Chevalier-Larsen E, Holzbaur EL (2006) Axonal transport and neurodegenerative disease. Biochim Biophys Acta 1762(11–12):1094–1108

    PubMed  CAS  Google Scholar 

  • Chio A, Calvo A, Moglia C, Mazzini L, Mora G (2011) Phenotypic heterogeneity of amyotrophic lateral sclerosis: a population based study. J Neurol Neurosurg Psychiatry 82(7):740–746

    Article  PubMed  Google Scholar 

  • Conson M, Sacco S, Sara M, Pistoia F, Grossi D, Trojano L (2008) Selective motor imagery defect in patients with locked-in syndrome. Neuropsychologia 46(11):2622–2628

    Article  PubMed  Google Scholar 

  • Conson M, Pistoia F, Sara M, Grossi D, Trojano L (2010) Recognition and mental manipulation of body parts dissociate in locked-in syndrome. Brain Cogn 73(3):189–193

    Article  PubMed  Google Scholar 

  • Cooper LA, Shepard RN (1975) Mental transformations in the identification of left and right hands. J Exp Psychol Hum Percept Perform 104(1):48–56

    PubMed  CAS  Google Scholar 

  • Corradi-Dell’Acqua C, Tomasino B, Fink GR (2009) What is the position of an arm relative to the body? Neural correlates of body schema and body structural description. J Neurosci 29(13):4162–4171

    Article  PubMed  Google Scholar 

  • de Vignemont F (2010) Body schema and body image—pros and cons. Neuropsychologia 48(3):669–680

    Article  PubMed  Google Scholar 

  • 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):127–134

    Article  PubMed  CAS  Google Scholar 

  • Decety J, Perani D, Jeannerod M, Bettinardi V, Tadary B, Woods R, Mazziotta JC, Fazio F (1994) Mapping motor representations with positron emission tomography. Nature 371(6498):600–602

    Article  PubMed  CAS  Google Scholar 

  • Ehrsson HH, Spence C, Passingham RE (2004) That’s my hand! Activity in premotor cortex reflects feeling of ownership of a limb. Science 305(5685):875–877

    Article  PubMed  CAS  Google Scholar 

  • Fiorio M, Tinazzi M, Aglioti SM (2006) Selective impairment of hand mental rotation in patients with focal hand dystonia. Brain 129(Pt 1):47–54

    PubMed  Google Scholar 

  • Frith CD, Blakemore SJ, Wolpert DM (2000) Abnormalities in the awareness and control of action. Philos Trans R Soc Lond B Biol Sci 355(1404):1771–1788

    Article  PubMed  CAS  Google Scholar 

  • Gentilucci M, Daprati E, Gangitano M (1998a) Implicit visual analysis in handedness recognition. Conscious Cogn 7(3):478–493

    Article  PubMed  CAS  Google Scholar 

  • Gentilucci M, Daprati E, Gangitano M (1998b) Right-handers and left-handers have different representations of their own hand. Brain Res Cogn Brain Res 6(3):185–192

    Article  PubMed  CAS  Google Scholar 

  • Girardi A, Macpherson SE, Abrahams S (2011) Deficits in emotional and social cognition in amyotrophic lateral sclerosis. Neuropsychology 25(1):53–65

    Article  PubMed  Google Scholar 

  • Gogos A, Gavrilescu M, Davison S, Searle K, Adams J, Rossell SL, Bell R, Davis SR, Egan GF (2010) Greater superior than inferior parietal lobule activation with increasing rotation angle during mental rotation: an fMRI study. Neuropsychologia 48(2):529–535

    Article  PubMed  Google Scholar 

  • Gonzalez B, Rodriguez M, Ramirez C, Sabate M (2005) Disturbance of motor imagery after cerebellar stroke. Behav Neurosci 119(2):622–626

    Article  PubMed  Google Scholar 

  • Harris IM, Egan GF, Sonkkila C, Tochon-Danguy HJ, Paxinos G, Watson JD (2000) Selective right parietal lobe activation during mental rotation: a parametric PET study. Brain 123(Pt 1):65–73

    Article  PubMed  Google Scholar 

  • Head H, Holms G (1911) Sensory disturbances from cerebral lesions. Brain 34(1):102–254

    Article  Google Scholar 

  • Hochberg J, Gellman L (1977) The effect of landmark features on mental rotation times. Mem Cognit 5(1):23–26

    Article  PubMed  CAS  Google Scholar 

  • Ionta S, Fourkas AD, Fiorio M, Aglioti SM (2007) The influence of hands posture on mental rotation of hands and feet. Exp Brain Res 183(1):1–7

    Article  PubMed  Google Scholar 

  • Jeannerod M (1995) Mental imagery in the motor context. Neuropsychologia 33(11):1419–1432

    Article  PubMed  CAS  Google Scholar 

  • Jeannerod M (1999) Visuomotor channels: their integration in goal-directed prehension. Hum Mov Sci 18:201–218

    Article  Google Scholar 

  • Jeannerod M (2001) Neural simulation of action: a unifying mechanism for motor cognition. Neuroimage 14(1 Pt 2):S103–S109

    Article  PubMed  CAS  Google Scholar 

  • Jeannerod M, Decety J (1995) Mental motor imagery: a window into the representational stages of action. Curr Opin Neurobiol 5(6):727–732

    Article  PubMed  CAS  Google Scholar 

  • Jordan K, Heinze HJ, Lutz K, Kanowski M, Jancke L (2001) Cortical activations during the mental rotation of different visual objects. Neuroimage 13(1):143–152

    Article  PubMed  CAS  Google Scholar 

  • Kew JJ, Leigh PN, Playford ED, Passingham RE, Goldstein LH, Frackowiak RS, Brooks DJ (1993) Cortical function in amyotrophic lateral sclerosis. A positron emission tomography study. Brain 116(Pt 3):655–680

    Article  PubMed  Google Scholar 

  • Kew JJ, Brooks DJ, Passingham RE, Rothwell JC, Frackowiak RS, Leigh PN (1994) Cortical function in progressive lower motor neuron disorders and amyotrophic lateral sclerosis: a comparative PET study. Neurology 44(6):1101–1110

    Article  PubMed  CAS  Google Scholar 

  • Konrad C, Henningsen H, Bremer J, Mock B, Deppe M, Buchinger C, Turski P, Knecht S, Brooks B (2002) Pattern of cortical reorganization in amyotrophic lateral sclerosis: a functional magnetic resonance imaging study. Exp Brain Res 143(1):51–56

    Article  PubMed  Google Scholar 

  • Konrad C, Jansen A, Henningsen H, Sommer J, Turski PA, Brooks BR, Knecht S (2006) Subcortical reorganization in amyotrophic lateral sclerosis. Exp Brain Res 172(3):361–369

    Article  PubMed  CAS  Google Scholar 

  • Kosslyn SM, Behrmann M, Jeannerod M (1995) The cognitive neuroscience of mental imagery. Neuropsychologia 33(11):1335–1344

    Article  PubMed  CAS  Google Scholar 

  • Lomen-Hoerth C, Murphy J, Langmore S, Kramer JH, Olney RK, Miller B (2003) Are amyotrophic lateral sclerosis patients cognitively normal? Neurology 60(7):1094–1097

    Article  PubMed  CAS  Google Scholar 

  • Lule D, Diekmann V, Kassubek J, Kurt A, Birbaumer N, Ludolph AC, Kraft E (2007) Cortical plasticity in amyotrophic lateral sclerosis: motor imagery and function. Neurorehabil Neural Repair 21(6):518–526

    Article  PubMed  Google Scholar 

  • Milivojevic B, Hamm JP, Corballis MC (2009) Functional neuroanatomy of mental rotation. J Cogn Neurosci 21(5):945–959

    Article  PubMed  Google Scholar 

  • Mulder DW (1982) Clinical limits of amyotrophic lateral sclerosis. Adv Neurol 36:15–22

    PubMed  CAS  Google Scholar 

  • Ni Choisdealbha A, Brady N, Maguinness C (2011) Differing roles for the dominant and non-dominant hands in the hand laterality task. Exp Brain Res 211(1):73–85

    Article  PubMed  Google Scholar 

  • Nico D, Daprati E, Rigal F, Parsons L, Sirigu A (2004) Left and right hand recognition in upper limb amputees. Brain 127(Pt 1):120–132

    Article  PubMed  Google Scholar 

  • Parsons LM (1987) Imagined spatial transformations of one’s hands and feet. Cogn Psychol 19(2):178–241

    Article  PubMed  CAS  Google Scholar 

  • Parsons LM (1994) Temporal and kinematic properties of motor behavior reflected in mentally simulated action. J Exp Psychol Hum Percept Perform 20(4):709–730

    Article  PubMed  CAS  Google Scholar 

  • Parsons LM, Fox PT, Downs JH, Glass T, Hirsch TB, Martin CC, Jerabek PA, Lancaster JL (1995) Use of implicit motor imagery for visual shape discrimination as revealed by PET. Nature 375(6526):54–58

    Article  PubMed  CAS  Google Scholar 

  • Parsons LM, Gabrieli JD, Phelps EA, Gazzaniga MS (1998) Cerebrally lateralized mental representations of hand shape and movement. J Neurosci 18(16):6539–6548

    PubMed  CAS  Google Scholar 

  • Pelgrims B, Michaux N, Olivier E, Andres M (2010) Contribution of the primary motor cortex to motor imagery: a subthreshold TMS study. Hum Brain Mapp 32(9):1471–1482

    Article  PubMed  Google Scholar 

  • Podzebenko K, Egan GF, Watson JD (2002) Widespread dorsal stream activation during a parametric mental rotation task, revealed with functional magnetic resonance imaging. Neuroimage 15(3):547–558

    Article  PubMed  Google Scholar 

  • Raaphorst J, de Visser M, Linssen WH, de Haan RJ, Schmand B (2010) The cognitive profile of amyotrophic lateral sclerosis: a meta-analysis. Amyotroph Lateral Scler 11(1–2):27–37

    Article  PubMed  Google Scholar 

  • Raven JC, Court JH, Raven J (1996) Manual for Raven’s progressive matrices and vocabulary scales. Section 3, Standard progressive matrices. 1996 ed edn. Oxford Psychologists Press, Oxford

    Google Scholar 

  • Reed CL, Farah MJ (1995) The psychological reality of the body schema: a test with normal participants. J Exp Psychol Hum Percept Perform 21(2):334–343

    Article  PubMed  CAS  Google Scholar 

  • Schoenfeld MA, Tempelmann C, Gaul C, Kuhnel GR, Duzel E, Hopf JM, Feistner H, Zierz S, Heinze HJ, Vielhaber S (2005) Functional motor compensation in amyotrophic lateral sclerosis. J Neurol 252(8):944–952

    Article  PubMed  Google Scholar 

  • Schwoebel J, Friedman R, Duda N, Coslett HB (2001) Pain and the body schema: evidence for peripheral effects on mental representations of movement. Brain 124(Pt 10):2098–2104

    Article  PubMed  CAS  Google Scholar 

  • Sekiyama K (1982) Kinesthetic aspects of mental representations in the identification of left and right hands. Percept Psychophys 32(2):89–95

    Article  PubMed  CAS  Google Scholar 

  • Shenton JT, Schwoebel J, Coslett HB (2004) Mental motor imagery and the body schema: evidence for proprioceptive dominance. Neurosci Lett 370(1):19–24

    Article  PubMed  CAS  Google Scholar 

  • Shepard RN, Metzler J (1971) Mental rotation of three-dimensional objects. Science 171(972):701–703

    Article  PubMed  CAS  Google Scholar 

  • 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):1564–1568

    Article  PubMed  CAS  Google Scholar 

  • Stanton BR, Williams VC, Leigh PN, Williams SC, Blain CR, Giampietro VP, Simmons A (2007) Cortical activation during motor imagery is reduced in Amyotrophic Lateral Sclerosis. Brain Res 1172:145–151

    Article  PubMed  CAS  Google Scholar 

  • ter Horst AC, van Lier R, Steenbergen B (2010) Mental rotation task of hands: differential influence number of rotational axes. Exp Brain Res 203(2):347–354

    Article  PubMed  Google Scholar 

  • Tomasino B, Rumiati RI, Umilta CA (2003) Selective deficit of motor imagery as tapped by a left-right decision of visually presented hands. Brain Cogn 53(2):376–380

    Article  PubMed  Google Scholar 

  • Tsermentseli S, Leigh PN, Goldstein LH (2011) The anatomy of cognitive impairment in amyotrophic lateral sclerosis: more than frontal lobe dysfunction. Cortex 48(2):166–182

    Article  PubMed  Google Scholar 

  • Uccelli R, Binazzi A, Altavista P, Belli S, Comba P, Mastrantonio M, Vanacore N (2007) Geographic distribution of amyotrophic lateral sclerosis through motor neuron disease mortality data. Eur J Epidemiol 22(11):781–790

    Article  PubMed  Google Scholar 

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Acknowledgments

A.S. was partially supported by QUALIA—Associazione per la ricerca teorica e applicata in scienze cognitive.

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  The authors declare that they have no conflict of interest.

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Correspondence to G. Bottini.

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F. Fiori and A. Sedda equally contributed to this work.

An erratum to this article is available at http://dx.doi.org/10.1007/s00221-016-4605-9.

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Fiori, F., Sedda, A., Ferrè, E.R. et al. Exploring motor and visual imagery in Amyotrophic Lateral Sclerosis. Exp Brain Res 226, 537–547 (2013). https://doi.org/10.1007/s00221-013-3465-9

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