Hostname: page-component-848d4c4894-hfldf Total loading time: 0 Render date: 2024-06-02T06:47:34.866Z Has data issue: false hasContentIssue false
  • English
  • Français

The Role of Motor System in Mental Rotation: New Insights from Myotonic Dystrophy Type 1

Published online by Cambridge University Press:  11 December 2019

Giorgia Cona Open the ORCID record for Giorgia Cona [Opens in a new window] ,
Arianna Casagrande ,
Sabrina Lenzoni ,
Elena Pegoraro ,
Virginia Bozzoni ,
Luca Bello ,
Gianni Sorarù ,
Annalisa Botta  and
Carlo Semenza
Giorgia Cona*
Affiliation:
Department of General Psychology, University of Padova, Padova, Italy Padova Neuroscience Center, Padova, Italy
Arianna Casagrande
Affiliation:
Department of Neuroscience, University of Padova, Padova, Italy
Sabrina Lenzoni
Affiliation:
Department of Neuroscience, University of Padova, Padova, Italy
Elena Pegoraro
Affiliation:
Department of Neuroscience, University of Padova, Padova, Italy
Virginia Bozzoni
Affiliation:
Department of Neuroscience, University of Padova, Padova, Italy
Luca Bello
Affiliation:
Department of Neuroscience, University of Padova, Padova, Italy
Gianni Sorarù
Affiliation:
Department of Neuroscience, University of Padova, Padova, Italy
Annalisa Botta
Affiliation:
Department of Biomedicine and Prevention, Medical Genetics Section, University of Rome Tor Vergata, Rome, Italy
Carlo Semenza
Affiliation:
Padova Neuroscience Center, Padova, Italy Department of Neuroscience, University of Padova, Padova, Italy IRCCS San Camillo Hospital, Venice, Italy
*
*Correspondence and reprint requests to: Giorgia Cona, Department of General Psychology, Via Venezia, 8, 35131, University of Padova, Padova, Italy. E-mail: giorgia.cona@unipd.it
Get access Rights & Permissions [Opens in a new window]

Abstract

Objective:

This study explored mental rotation (MR) performance in patients with myotonic dystrophy 1 (DM1), an inherited neuromuscular disorder dominated by muscular symptoms, including muscle weakness and myotonia. The aim of the study was twofold: to gain new insights into the neurocognitive mechanisms of MR and to better clarify the cognitive profile of DM1 patients. To address these aims, we used MR tasks involving kinds of stimuli that varied for the extent to which they emphasized motor simulation and activation of body representations (body parts) versus visuospatial imagery (abstract objects). We hypothesized that, if peripheral sensorimotor feedback system plays a pivotal role in modulating MR performance, then DM1 patients would exhibit more difficulties in mentally rotating hand stimuli than abstract objects.

Method:

Twenty-four DM1 patients and twenty-four age- and education-matched control subjects were enrolled in the study and were required to perform two computerized MR tasks involving pictures of hands and abstract objects.

Results:

The analysis of accuracy showed that patients had impaired MR performance when the angular disparities between the stimuli were higher. Notably, as compared to controls, patients showed slower responses when the stimuli were hands, whereas no significant differences when stimuli were objects.

Conclusion:

The findings are coherent with the embodied cognition view, indicating a tight relation between body- and motor-related processes and MR. They suggest that peripheral, muscular, abnormalities in DM1 lead to alterations in manipulation of motor representations, which in turn affect MR, especially when body parts are to mentally rotate.

Keywords

Movement disordersMental rotationMyotonic dystrophy 1Motor systemEmbodied cognitionMotor imageryVisuospatial
Type
Regular Research
Information
Journal of the International Neuropsychological Society , Volume 26 , Issue 5 , May 2020 , pp. 492 - 502
Copyright
Copyright © INS. Published by Cambridge University Press, 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Amick, M.M., Schendan, H.E., Ganis, G., & Cronin-Golomb, A. (2006). Frontostriatal circuits are necessary for visuomotor transformation: Mental rotation in Parkinson’s disease. Neuropsychologia, 44(3), 339–349. doi: 10.1016/j.neuropsychologia.2005.06.002CrossRefGoogle ScholarPubMed
Amorim, M.A., Isableu, B., & Jarraya, M. (2006). Embodied spatial transformations: “Body analogy” for the mental rotation of objects. Journal of Experimental Psychology: General, 135(3). doi: 10.1037/0096-3445.135.3.327Google Scholar
Antonini, G., Mainero, C., Romano, A., Giubilei, F., Ceschin, V., Gragnani, F., Morino, S., Fiorelli, M., Soscia, F., Di Pasquale, A., & Caramia, F. (2004). Cerebral atrophy in myotonic dystrophy: A voxel based morphometric study. Journal of Neurology, Neurosurgery & Psychiatry, 75(11), 1611–1613. doi: 10.1136/jnnp.2003.032417CrossRefGoogle ScholarPubMed
Ashizawa, T., Dubel, J.R., Dunne, P.W., Dunne, C.J., Pizzuti, A., Caskey, C.T., Perryman, M.B., Epstein, H.F., & Hejtmancik, J.F. (1992). Anticipation in myotonic dystrophy: II. Complex relationships between clinical findings and structure of the GCT repeat. Neurology, 42(10), 1877–1877. doi: 10.1212/WNL.42.10.1877Google ScholarPubMed
Barsalou, L.W. (1999). Perceptual symbol systems. Behavioral and Brain Sciences, 22, 577–660. doi: 10.1017/S0140525X99002149CrossRefGoogle ScholarPubMed
Barsalou, L.W. (2008). Grounded cognition. Annual Review of Psychology, 59, 617–645. doi: 10.1146/annurev.psych.59.103006.093639CrossRefGoogle ScholarPubMed
Bode, S., Koeneke, S., & Jäncke, L. (2007). Different strategies do not moderate primary motor cortex involvement in mental rotation: A TMS study. Behavioral and Brain Functions, 3(1), 38. doi: 10.1186/1744-9081-3-38CrossRefGoogle Scholar
Cohen, M.S., Kosslyn, S.M., Breiter, H.C., DiGirolamo, G.J., Thompson, W.L., Anderson, A.K., Bookheimer, S.Y., Rosen, B.R., & Belliveau, J.W. (1996). Changes in cortical activity during mental rotation A mapping study using functional MRI. Brain, 119(1), 89–100. doi: 10.1093/brain/119.1.89CrossRefGoogle ScholarPubMed
Cole, J. & Paillard, J. (1995). Living without touch and peripheral information about body position and movement: Studies with deafferented subjects, In Bermudez, J.L., Marcel, A., & Eilan, N. (Eds.), The body and the self, (pp. 245–266). Cambridge, MA: MIT PressGoogle Scholar
Cona, G., Marino, G., & Semenza, C. (2017). TMS of supplementary motor area (SMA) facilitates mental rotation performance: Evidence for sequence processing in SMA. Neuroimage, 146, 770–777. doi: 10.1016/j.neuroimage.2016.10.032CrossRefGoogle ScholarPubMed
Cona, G., Panozzo, G., & Semenza, C. (2017). The role of dorsal premotor cortex in mental rotation: A transcranial magnetic stimulation study. Brain and Cognition, 116, 71–78. doi: 10.1016/j.bandc.2017.06.002CrossRefGoogle ScholarPubMed
Cona, G. & Scarpazza, C. (2019). Where is the “where” in the brain? A meta-analysis of neuroimaging studies on spatial cognition. Human Brain Mapping, 40(6), 1867–1886. doi: 10.1002/hbm.24496CrossRefGoogle Scholar
Cona, G. & Semenza, C. (2017). Supplementary motor area as key structure for domain-general sequence processing: A unified account. Neuroscience & Biobehavioral Reviews, 72, 28–42. doi: 10.1016/j.neubiorev.2016.10.033CrossRefGoogle ScholarPubMed
Corballis, M.C. & Sergent, J. (1989). Hemispheric specialization for mental rotation. Cortex, 25(1), 15–25. doi: 10.1016/S0010-9452(89)80002-4CrossRefGoogle ScholarPubMed
Day, J.W. & Ranum, L.P. (2005). RNA pathogenesis of the myotonic dystrophies. Neuromuscular Disorders, 15(1), 5–16. doi: 10.1016/j.nmd.2004.09.012CrossRefGoogle ScholarPubMed
Decety, J & Grèzes, J. (2006) The power of simulation: Imagining one’s own and other’s behavior. Brain Research, 1079, 4–14. doi: 10.1016/j.brainres.2005.12.115CrossRefGoogle ScholarPubMed
de Lange, F.P., Roelofs, K., & Toni, I. (2007). Increased self-monitoring during imagined movements in conversion paralysis. Neuropsychologia, 45(9), 2051–2058. doi: 10.1016/j.neuropsychologia.2007.02.002CrossRefGoogle ScholarPubMed
de Lange, F.P., Toni, I., & Roelofs, K. (2010). Altered connectivity between prefrontal and sensorimotor cortex in conversion paralysis. Neuropsychologia, 48(6), 1782–1788. doi: 10.1016/j.neuropsychologia.2010.02.029CrossRefGoogle ScholarPubMed
De Vries, S. & Mulder, T. (2007). Motor imagery and stroke rehabilitation: A critical discussion. Journal of Rehabilitation Medicine, 39(1), 5–13. doi: 10.2340/16501977-0020CrossRefGoogle ScholarPubMed
Dienes, Z. (2014). Using Bayes to get the most out of non-significant results. Frontiers in Psychology, 781(1), 17. doi: 10.3389/fpsyg.2014.00781Google Scholar
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), 727–741. doi: 10.1016/0028-3932(95)00008-QCrossRefGoogle ScholarPubMed
Fiorio, M., Tinazzi, M., & Aglioti, S.M. (2006). Selective impairment of hand mental rotation in patients with focal hand dystonia. Brain, 129(1), 47–54. doi: 10.1093/brain/awh630CrossRefGoogle ScholarPubMed
Ganis, G., Keenan, J.P., Kosslyn, S.M., & Pascual-Leone, A. (2000). Transcranial magnetic stimulation of primary motor cortex affects mental rotation. Cerebral Cortex, 10(2), 175–180. doi: 10.1093/cercor/10.2.175CrossRefGoogle ScholarPubMed
Ganis, G. & Kievit, R. (2015). A new set of three-dimensional shapes for investigating mental rotation processes: Validation data and stimulus set. Journal of Open Psychology Data Files in this Item Files Size Format View 13-116-2-PB. pdf 567.5 Kb PDF View/Open, 3(1), e3. doi: 10.5334/jopd.aiGoogle Scholar
Gardony, A.L., Taylor, H.A., & Brunyé, T.T. (2014). What does physical rotation reveal about mental rotation? Psychological Science, 25(2), 605–612. doi: 10.1177/0956797613503174CrossRefGoogle ScholarPubMed
Gibbs, R.W. Jr. (2006) Embodiment and cognitive science. New York: Cambridge University Press.Google Scholar
Goldinger, S.D., Papesh, M.H., Barnhart, A.S., Hansen, W.A., & Hout, M.C. (2016). The poverty of embodied cognition. Psychonomic Bulletin & Review, 23(4), 959–978. doi: 10.3758/s13423-015-0860-1CrossRefGoogle ScholarPubMed
Grush, R. (2004). The emulation theory of representation: Motor control, imagery, and perception. Behavioral and Brain Sciences, 27(3), 377–396. doi: 10.1017/S0140525X0 4000093CrossRefGoogle ScholarPubMed
Hallett, M. (1998). The neurophysiology of dystonia. Archives of Neurology, 55(5), 601–603. doi: 10.1001/archneur.55.5.601CrossRefGoogle ScholarPubMed
Harper, P.S., van Engelen, B.G.M., Eymard, B., Rogers, M., & Wilcox, D. (2002). 99th ENMC international workshop: Myotonic dystrophy: present management, future therapy: 9–11 November 2001, Naarden, The Netherlands. Neuromuscular Disorders, 12(6), 596–599. doi: 10.1016/S0960-8966(02)00020-2CrossRefGoogle ScholarPubMed
Hochberg, J. & Gellman, L. (1977). The effect of landmark features on mental rotation times. Memory & Cognition, 5(1), 23–26. doi: 10.3758/BF03209187CrossRefGoogle ScholarPubMed
Iachini, T., Ruggiero, G., Bartolo, A., Rapuano, M., & Ruotolo, F. (2019). The effect of body-related stimuli on mental rotation in children, young and elderly adults. Scientific Reports, 9(1), 1169. doi: 10.1038/s41598-018-37729-7CrossRefGoogle Scholar
Jackson, P.L., Lafleur, M.F., Malouin, F., Richards, C., & Doyon, J. (2001). Potential role of mental practice using motor imagery in neurologic rehabilitation. Archives of Physical Medicine and Rehabilitation. 82, 1133–1141. doi: 10.1053/apmr.2001.24286CrossRefGoogle ScholarPubMed
Jansen, P. & Heil, M. (2010). The relation between motor development and mental rotation ability in 5-to 6-year-old children. International Journal of Developmental Science, 4(1), 67–75. doi: 10.3233/DEV-2010-4105CrossRefGoogle Scholar
Jansen, P. & Kaltner, S. (2014). Object-based and egocentric mental rotation performance in older adults: The importance of gender differences and motor ability. Aging, Neuropsychology, and Cognition, 21(3), 296–316. doi: 10.1080/13825585.2013.805725CrossRefGoogle ScholarPubMed
Jeannerod, M. & Decety, J. (1995). Mental motor imagery: A window into the representational stages of action. Current Opinion in Neurobiology, 5(6), 727–732. doi: 10.1016/0959-4388(95)80099-9CrossRefGoogle ScholarPubMed
Jeffreys, H. (1946). An invariant form for the prior probability in estimation problems. Proceedings of the Royal Society of London. Series A. Mathematical and Physical Sciences, 186(1007), 453–461. doi: 10.1098/rspa.1946.0056Google ScholarPubMed
Johnson, E.R., Abresch, R.T., Carter, G.T., Kilmer, D.D., Fowler, W.M. Jr, Sigford, B.J., & Wanlass, R.L. (1995). Profiles of neuromuscular diseases: Myotonic dystrophy1. American Journal of Physical Medicine & Rehabilitation, 74(5), S117.CrossRefGoogle Scholar
Johnson-Frey, S.H. (2004). Stimulation through simulation? Motor imagery and functional reorganization in hemiplegic stroke patients. Brain and Cognition, 55, 328–331. doi: 10.1016/j.bandc.2004.02.032CrossRefGoogle ScholarPubMed
Katschnig, P., Edwards, M.J., Schwingenschuh, P., Aguirregomozcorta, M., Kägi, G., Rothwell, J.C., & Bhatia, K.P. (2010). Mental rotation of body parts and sensory temporal discrimination in fixed dystonia. Movement Disorders, 25(8), 1061–1067. doi: 10.1002/mds.23047CrossRefGoogle ScholarPubMed
Kornblum, C., Reul, J., Kress, W., Grothe, C., Amanatidis, N., Klockgether, T., & Schröder, R. (2004). Cranial magnetic resonance imaging in genetically proven myotonic dystrophy type 1 and 2. Journal of Neurology, 251(6), 710–714. doi: 10.1007/s00415-004-0408-1CrossRefGoogle ScholarPubMed
Kosslyn, S.M., Ganis, G., & Thompson, W.L. (2001). Neural foundations of imagery. Nature Reviews Neuroscience, 2(9), 635. doi: 10.1038/35090055CrossRefGoogle ScholarPubMed
Mathieu, J., Boivin, H., Meunier, D., Gaudreault, M., & Begin, P. (2001). Assessment of a disease-specific muscular impairment rating scale in myotonic dystrophy. Neurology, 56(3), 336–340. doi: 10.1212/WNL.56.3.336CrossRefGoogle ScholarPubMed
Milivojevic, B., Hamm, J.P., & Corballis, M.C. (2009). Functional neuroanatomy of mental rotation. Journal of Cognitive Neuroscience, 21(5), 945–959. doi: 10.1162/jocn.2009.21085CrossRefGoogle ScholarPubMed
Modoni, A., Silvestri, G., Pomponi, M.G., Mangiola, F., Tonali, P.A., & Marra, C. (2004). Characterization of the pattern of cognitive impairment in myotonic dystrophy type 1. Archives of Neurology, 61(12), 1943–1947. doi: 10.1001/archneur.61.12.1943CrossRefGoogle ScholarPubMed
Morey, R.D. & Rouder, J.N. (2015). BayesFactor (Version 0.9.11-3)[Computer software].Google Scholar
Moseley, G.L. (2004). Graded motor imagery is effective for long-standing complex regional pain syndrome: A randomised controlled trial. Pain, 108(1–2), 192–198. doi: 10.1016/j.pain.2004.01.006CrossRefGoogle ScholarPubMed
Munzert, J., Lorey, B., & Zentgraf, K. (2009). Cognitive motor processes: The role of motor imagery in the study of motor representations. Brain Research Reviews, 60(2), 306–326. doi: 10.1016/j.brainresrev.2008.12.024CrossRefGoogle Scholar
Paivio, A. (1986). Mental representations: A dual coding approach. New York: Oxford University PressGoogle Scholar
Parsons, L.M. (1994). Temporal and kinematic properties of motor behavior reflected in mentally simulated action. Journal of Experimental Psychology: Human Perception and Performance, 20(4), 709. doi: 10.1037/0096-1523.20.4.709Google ScholarPubMed
Pelgrims, B., Michaux, N., Olivier, E., & Andres, M. (2011). Contribution of the primary motor cortex to motor imagery: A subthreshold TMS study. Human Brain Mapping, 32(9), 1471–1482. doi: 10.1002/hbm.21121CrossRefGoogle ScholarPubMed
Richter, W., Somorjai, R., Summers, R., Jarmasz, M., Menon, R.S., Gati, J.S., Georgopoulos, A.P., Tegeler, C., Ugurbil, K., & Kim, S.G. (2000). Motor area activity during mental rotation studied by time-resolved single-trial fMRI. Journal of Cognitive Neuroscience, 12(2), 310–320. doi: 10.1162/089892900562129CrossRefGoogle ScholarPubMed
Ricker, K., Koch, M.C., Lehmann-Horn, F., Pongratz, D., Otto, M., Heine, R., & Moxley, R.T. (1994). Proximal myotonic myopathy: A new dominant disorder with myotonia, muscle weakness, and cataracts. Neurology, 44(8), 1448–1448. doi: 10.1212/WNL.44.8.1448CrossRefGoogle ScholarPubMed
Romeo, V., Pegoraro, E., Ferrati, C., Squarzanti, F., Sorarù, G., Palmieri, A., Zucchetta, P., Antunovic, L., Bonifazi, E., Novelli, G., & Angelini, C. (2010). Brain involvement in myotonic dystrophies: Neuroimaging and neuropsychological comparative study in DM1 and DM2. Journal of Neurology, 257(8), 1246–1255. doi: 10.1007/s00415-010-5498-3CrossRefGoogle ScholarPubMed
Rouder, J.N., Morey, R.D., Speckman, P.L., & Province, J.M. (2012). Default Bayes factors for ANOVA designs. Journal of Mathematical Psychology, 56(5), 356–374. doi: 10.1016/j.jmp.2012.08.001CrossRefGoogle Scholar
Sauner, D., Bestmann, S., Siebner, H.R., & Rothwell, J.C. (2006). No evidence for a substantial involvement of primary motor hand area in handedness judgements: A transcranial magnetic stimulation study. European Journal of Neuroscience, 23(8), 2215–2224.CrossRefGoogle ScholarPubMed
Schubotz, R.I. (2007). Prediction of external events with our motor system: Towards a new framework. Trends in Cognitive Sciences, 11(5), 211–218. doi: 10.1016/j.tics.2007.02.006CrossRefGoogle ScholarPubMed
Schwoebel, J., Friedman, R., Duda, N., & Coslett, H.B. (2001). Pain and the body schema: evidence for peripheral effects on mental representations of movement. Brain, 124(10), 2098–2104. doi: 10.1093/brain/124.10.2098CrossRefGoogle Scholar
Serra, L., Cercignani, M., Bruschini, M., Cipolotti, L., Mancini, M., Silvestri, G., Petrucci, A., Bucci, E., Antonini, G., Licchelli, L., & Spanò, B. (2016). “I know that you know that I know”: Neural substrates associated with social cognition deficits in DM1 patients. PLoS One, 11(6), e0156901. doi: 10.1371/journal.pone.0156901CrossRefGoogle ScholarPubMed
Shepard, R.N. (1987). Toward a universal law of generalization for psychological science. Science, 237(4820), 1317–1323. doi: 10.1126/science.3629243CrossRefGoogle Scholar
Shepard, R.N. & Metzler, J. (1971). Mental rotation of three-dimensional objects. Science, 171(3972), 701–703. doi: 10.1126/science.171.3972.701CrossRefGoogle ScholarPubMed
Sirigu, A. & Duhamel, J.R. (2001). Motor and visual imagery as two complementary but neurally dissociable mental processes. Journal of Cognitive Neuroscience, 13(7), 910–919. doi: 10.1162/089892901753165827CrossRefGoogle ScholarPubMed
Sirigu, A., Duhamel, J.R., Cohen, L., Pillon, B., Dubois, B., & Agid, Y. (1996). The mental representation of hand movements after parietal cortex damage. Science, 273(5281), 1564–1568. doi: 10.1126/science.273.5281.1564CrossRefGoogle ScholarPubMed
Sistiaga, A., Urreta, I., Jodar, M., Cobo, A.M., Emparanza, J., Otaegui, D., Poza, J.J., Merino, J.J., Imaz, H., Marti-Masso, J.F., & López De Munain, A. (2010). Cognitive/personality pattern and triplet expansion size in adult myotonic dystrophy type 1 (DM1): CTG repeats, cognition and personality in DM1. Psychological Medicine, 40(3), 487–495. doi: 10.1017/S0033291709990602CrossRefGoogle ScholarPubMed
Stevens, J.A. (2005). Interference effects demonstrate distinct roles for visual and motor imagery during the mental representation of human action. Cognition, 95(3), 329–350. doi: 10.1016/j.cognition.2004.02.008CrossRefGoogle ScholarPubMed
Thayer, Z.C., Johnson, B.W., Corballis, M.C., & Hamm, J.P. (2001). Perceptual and motor mechanisms for mental rotation of human hands. Neuroreport, 12(16), 3433–3437.CrossRefGoogle ScholarPubMed
Tomasino, B., Borroni, P., Isaja, A., & Ida Rumiati, R. (2005). The role of the primary motor cortex in mental rotation: A TMS study. Cognitive Neuropsychology, 22(3–4), 348–363. doi: 10.1080/02643290442000185CrossRefGoogle ScholarPubMed
Weber, Y.G., Roebling, R., Kassubek, J., Hoffmann, S., Rosenbohm, A., Wolf, M., Steinbach, P., Jurkat-Rott, K., Walter, H., Reske, S.N., & Lehmann-Horn, F. (2010). Comparative analysis of brain structure, metabolism, and cognition in myotonic dystrophy 1 and 2. Neurology, 74(14), 1108–1117. doi: 10.1212/WNL.0b013e3181d8c35fCrossRefGoogle ScholarPubMed
Wiedenbauer, G. & Jansen-Osmann, P. (2008). Manual training of mental rotation in children. Learning and Instruction, 18(1), 30–41. doi: 10.1016/j.learninstruc.2006.09.009CrossRefGoogle Scholar
Wiedenbauer, G., Schmid, J., & Jansen-Osmann, P. (2007). Manual training of mental rotation. European Journal of Cognitive Psychology, 19(1), 17–36. doi: 10.1080/09541440600709906CrossRefGoogle Scholar
Wilson, M. (2002). Six views of embodied cognition. Psychonomic Bulletin & Review, 9(4), 625–636. doi: 10.3758/BF03196322CrossRefGoogle ScholarPubMed
Winblad, S., Lindberg, C., & Hansen, S. (2006). Cognitive deficits and CTG repeat expansion size in classical myotonic dystrophy type 1 (DM1). Behavioral and Brain Functions, 2(1), 16. doi: 10.1186/1744-9081-2-16CrossRefGoogle Scholar
Wohlschläger, A. & Wohlschläger, A. (1998). Mental and manual rotation. Journal of Experimental Psychology: Human Perception and Performance, 24(2), 397. doi: 10.1037/0096-1523.24.2.397Google ScholarPubMed
Zacks, J.M. (2008). Neuroimaging studies of mental rotation: A meta-analysis and review. Journal of Cognitive Neuroscience, 20(1), 1–19. doi: 10.1162/jocn.2008.20013CrossRefGoogle ScholarPubMed
Zalonis, I., Bonakis, A., Christidi, F., Vagiakis, E., Papageorgiou, S.G., Kalfakis, N., Manta, P., & Vassilopoulos, D. (2010). Toward understanding cognitive impairment in patients with myotonic dystrophy type 1. Archives of Clinical Neuropsychology, 25(4), 303–313. doi: 10.1093/arclin/acq016CrossRefGoogle ScholarPubMed