Skip to main content
SpringerLink
Log in

Excessive motor overflow reveals abnormal inter-hemispheric connectivity in Friedreich ataxia

  • Original Communication
  • Published:
Journal of Neurology Aims and scope Submit manuscript

Abstract

This study sought to characterise force variability and motor overflow in 12 individuals with Friedreich ataxia (FRDA) and 12 age- and gender-matched controls. Participants performed a finger-pressing task by exerting 30 and 70 % of their maximum finger force using the index finger of the right and left hand. Control of force production was measured as force variability, while any involuntary movements occurring on the finger of the other, passive hand, was measured as motor overflow. Significantly greater force variability in individuals with FRDA compared with controls is indicative of cortico-cerebellar disruption affecting motor control. Meanwhile, significantly greater motor overflow in this group provides the first evidence of possible abnormal inter-hemispheric activity that may be attributable to asymmetrical neuronal loss in the dentate nucleus. Overall, this study demonstrated a differential engagement in the underlying default processes of the motor system in FRDA.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Pandolfo M (2009) Friedreich ataxia: the clinical picture. J Neurol 256:3–8

    Article  PubMed  Google Scholar 

  2. Delatycki MB, Williamson R, Forrest SM (2000) Friedreich ataxia: an overview. J Med Genet 37:1–8

    Article  PubMed  CAS  Google Scholar 

  3. Murayama S, Bouldin TW, Suzuki K (1992) Pathological stuffy of corticospinal-tract degeneration in Friedreich’s ataxia. Neuropathol Appl Neurobiol 18:81–86

    Article  PubMed  CAS  Google Scholar 

  4. Hou JG, Jancovic J (2003) Movement disorders in Friedreich’s ataxia. J Neurol Sci 206:59–64

    Article  PubMed  Google Scholar 

  5. Delatycki MB, Paris D, Gardner RJ, Nicholson GA, Nassif N, Storey E et al (1999) Clinical and genetic study of Friedreich ataxia in an Australian population. Am J Med Genet 87:168–174

    Article  PubMed  CAS  Google Scholar 

  6. Corben LA, Tai G, Wilson C, Collins V, Churchyard A, Delatycki M (2010) A comparison of three measures of upper limb function in Friedreich’s ataxia. J Neurol 257(4):523–528

    Article  Google Scholar 

  7. Epstein E, Farmer J, Tsou A, Perlman S, Subramony SH, Gomez CM et al (2008) Health related quality of life in Friedreich’s ataxia. J Neurol Sci 272:123–128

    Article  PubMed  Google Scholar 

  8. Brownell B, Oppenheimer DR, Hughes JT (1970) The central nervous system in motor neuron disease. J Neurol Neurosurg Psychiatry 41:287–410

    Google Scholar 

  9. Akhlaghi H, Corben L, Georgiou-Karistianis N, Bradshaw J, Delatycki M, Egan G A functional MRI study of motor dysfunction in Friedreich’s ataxia. Brain Res (in press)

  10. Corben LA, Delatycki MB, Bradshaw JL, Horne MK, Fahey MC, Churchyard AJ, Georgiou-Karistianis N (2010) Impairment in motor reprogramming in Friedreich ataxia reflecting possible cerebellar dysfunction. J Neurol 257(5):782–791

    Article  PubMed  Google Scholar 

  11. Corben LA, Akhlaghi H, Georgiou-Karistianis N, Bradshaw JL, Egan GF, Storey E, Delatycki M (2011) Impaired inhibition of prepotent motor tendencies in Friedreich ataxia demonstrated by the Simon interference task. Brain Cogn 76:140–145

    Article  PubMed  CAS  Google Scholar 

  12. Corben LA, Delatycki MB, Bradshaw JL, Churchyard AJ, Georgiou-Karistianis N (2011) Utilisation of advance motor information is impaired in Friedreich ataxia. Cerebellum 10(4):793–803

    Article  PubMed  Google Scholar 

  13. Brighina F, Scalia S, Gennuso M, Lupo I, Matta F, Piccoli T et al (2005) Hypoexcitability of cortical areas in patients affected by Friedreich ataxia: a TMS study. J Neurol Sci 235:19–22

    Article  PubMed  CAS  Google Scholar 

  14. Courchesne E, Allen G (1997) Predicting and preparation, fundamental functions of the cerebellum. Learn Mem 4:1–35

    Article  PubMed  CAS  Google Scholar 

  15. Della Nave R, Ginestroni A, Tessa C, Salvatore E, Bartolomei I, Salvi F et al (2008) Brain white matter tracts degeneration in Friedreich ataxia: an in vivo MRI study using tract-based spatial statistics and voxel-based morphometry. Neuroimage 40(1):19–35

    Article  PubMed  Google Scholar 

  16. Middleton FA, Strick PL (2000) Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res Rev 31:236–250

    Article  PubMed  CAS  Google Scholar 

  17. Georgiou-Karistianis N, Akhlaghi H, Corben LA, Delatycki M, Storey E, Bradshaw JL, Egan G (2012) Decreased functional brain activation in Friedreich ataxia using the Simon interference task. Brain Cogn 79:200–208

    Article  PubMed  CAS  Google Scholar 

  18. Ginestroni A, Diciotti S, Cecchi P, Pesaresi I, Tessa C, Giannelli M et al (2012) Neurodegeneration in Friedreich’s ataxia is associated with a mixed activation pattern of the brain. A fMRI study. Hum Brain Mapp 33:1780–1791

    Article  PubMed  Google Scholar 

  19. Armatas CA, Summers JJ, Bradshaw JL (1994) Mirror movements in normal adult subjects. J Clin Exp Neuropsychol 16(3):405–413

    Article  PubMed  CAS  Google Scholar 

  20. Armatas CA, Summers JJ, Bradshaw JL (1996) Strength as a factor influencing mirror movements. Hum Mov Sci 15:689–705

    Article  Google Scholar 

  21. Armatas CA, Summers JJ, Bradshaw JL (1996) Handedness and performance variability as factors influencing mirror movement occurrence. J Clin Exp Neuropsychol 18(6):823–835

    Article  PubMed  CAS  Google Scholar 

  22. Abercrombie M, Lindon R, Tyson M (1964) Associated movements in normal and physically handicapped children. Dev Med Child Neurol 6:573–580

    Article  PubMed  CAS  Google Scholar 

  23. Addamo PK, Farrow M, Hoy KE, Bradshaw JL, Georgiou-Karistianis N (2009) The influence of task characteristics on younger and older adult motor overflow. Quart J Exp Psychol 62(2):239–247

    Article  Google Scholar 

  24. Cohen HJ, Taft TT, Mahadeviah MS, Birch HG (1967) Developmental changes in overflow in normal and aberrantly functioning children. J Pediatrics 71:39–47

    Article  CAS  Google Scholar 

  25. Conolly K, Stratton P (1968) Developmental changes in associated movements. Dev Med Child Neurol 10:49–56

    Article  Google Scholar 

  26. Nass R (1985) Mirror movement asymmetries in congenital hemiparesis: the inhibition hypothesis revisited. Neurology 35:1059–1062

    Article  PubMed  CAS  Google Scholar 

  27. Addamo PK, Farrow M, Hoy KE, Bradshaw JL, Georgiou-Karistianis N (2007) The effects of age and attention on motor overflow production—a review. Brain Res Rev 54:189–204

    Article  PubMed  Google Scholar 

  28. Espay AJ, Li J-Y, Johnston L, Chen R, Lang AE (2005) Mirror movements in Parkinsonism: evaluation of a new clinical sign. J Neurol Neurosurg Psychiatry 76:1355–1359

    Article  PubMed  CAS  Google Scholar 

  29. Georgiou-Karistianis N, Hoy KE, Bradshaw JL, Farrow M, Chiu E, Churchyard A et al (2004) Motor overflow in Huntington’s disease. J Neurol Neurosurg Psychiatry 75:904–906

    Article  PubMed  CAS  Google Scholar 

  30. Hoy KE, Fitzgerald PB, Bradshaw JL, Armatas CA, Georgiou-Karistianis N (2004) Investigating the cortical origins of motor overflow. Brain Res Rev 46:315–327

    Article  PubMed  Google Scholar 

  31. Dennis M (1976) Impaired sensory and motor differentiation with corpus callosum agenesis: a lack of callosal inhibition during ontogeny? Neuropsychologia 14:455–469

    Article  PubMed  CAS  Google Scholar 

  32. Muller F, Kunesch E, Binkofski F, Freund HJ (1991) Residual sensorimotor functions in a patient after right sided hemispherectomy. Neuropsychologia 29:125–145

    Article  PubMed  CAS  Google Scholar 

  33. Addamo PK, Farrow M, Hoy KE, Bradshaw JL, Georgiou-Karistianis N (2009) A developmental study of the influence of task characteristics on motor overflow. Brain Cogn 69:413–419

    Article  PubMed  Google Scholar 

  34. Baliz Y, Armatas C, Farrow M, Hoy KE, Fitzgerald PB, Bradshaw JL, Georgiou-Karistianis N (2005) The influence of attention and age on the occurrence of mirror movements. J Int Neuropsychol Soc 11:855–862

    Article  PubMed  Google Scholar 

  35. Hoy KE, Fitzgerald PB, Bradshaw JL, Farrow M, Brown TL, Armatas CA, Georgiou-Karistianis N (2004) Motor overflow in schizophrenia. Psychiatry Res 125:129–137

    Article  PubMed  Google Scholar 

  36. Subramony SH, May W, Lynch D, Gomez C, Fischbeck K, Hallett M et al (2005) Measuring Friedreich ataxia: interrater reliability of a neurologic rating scale. Neurology 64:1261–1262

    Article  PubMed  CAS  Google Scholar 

  37. Morris S (2002) Ashworth and Tardieu scales: their clinical relevance for measuring spasticity in adult and paediatric neurological populations. Phys Ther Rev 7:53–62

    Article  Google Scholar 

  38. Grice KO, Vogel KA, Le V, Mitchell A, Muniz S, Vollmer MA (2003) Adult norms for a commercially available nine hole peg test for finger dexterity. Am J Occup Ther 57:570–573

    Article  Google Scholar 

  39. Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J (1961) An inventory for measuring depression. Arch Gen Psychiatry 4:561–571

    Article  PubMed  CAS  Google Scholar 

  40. Oldfield RC (1970) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  Google Scholar 

  41. Corben LA, Georgiou-Karistianis N, Fahey MC, Storey E, Churchyard A, Horne M et al (2006) Towards an understanding of cognitive function in Friedreich ataxia. Brain Res Bull 70:197–202

    Article  PubMed  Google Scholar 

  42. Ito M (2008) Control of mental activities by internal models in the cerebellum. Nat Rev Neurosci 9(4):304–313

    Article  PubMed  CAS  Google Scholar 

  43. Rizzo G, Tonon C, Valentino ML, Manners D, Fortuna F, Gellera C et al (2011) Brain diffusion-weighted imaging in Friedreich’s ataxia. Mov Disord 26(4):705–712

    Article  PubMed  Google Scholar 

  44. Sehm B, Perez MA, Xu B, Hidler J, Cohen LG (2010) Functional neuroanatomy of mirroring during a unimanual force generation task. Cereb Cortex 20:34–45

    Article  PubMed  CAS  Google Scholar 

  45. Habas C, Cabanis EA (2006) Cortical areas functionally linked with the cerebellar second homunculus during out-of-phase bimanual movements. Neuroradiology 48(4):273–279

    Article  PubMed  Google Scholar 

  46. Doya K (2002) Complementary roles of basal ganglia and cerebellum in learning and motor control. Curr Opin Neurobiol 10:732–739

    Article  Google Scholar 

  47. Minzenberg MJ, Yoon JH, Soosman SK, Carter CS (2012) Excessive contralateral motor overflow in schizophrenia measured by fMRI. Psychiatry Res 202:38–45

    Article  PubMed  Google Scholar 

  48. Addamo PK, Farrow M, Bradshaw JL, Moss S, Georgiou-Karistianis N (2010) The effect of attending to motor overflow on its voluntary inhibition in young and older adults. Brain Cogn 74:358–364

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank all participants for taking part in our research. MBD is a NHMRC Practitioner Fellow. This research was funded by the School of Psychology and Psychiatry, Monash University.

Conflicts of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Experimental Neuropsychology Research Unit, School of Psychology and Psychiatry, Monash University, Clayton, VIC, 3800, Australia

    Sze-Cheen Low, Louise A. Corben, Anne-Marie Ternes & Nellie Georgiou-Karistianis

  2. Bruce Lefroy Centre for Genetic Health Research, Murdoch Childrens Research Institute, Parkville, VIC, Australia

    Louise A. Corben & Martin B. Delatycki

  3. Departments of Clinical Genetics and Medicine, University of Melbourne, Austin Health, Heidelberg, VIC, 3084, Australia

    Martin B. Delatycki

  4. Institute of Sports, Exercise and Active Living, Victoria University, Footscray Park Campus, Footscray, VIC, Australia

    Patricia K. Addamo

Authors
  1. Sze-Cheen Low
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Louise A. Corben
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Martin B. Delatycki
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anne-Marie Ternes
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Patricia K. Addamo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nellie Georgiou-Karistianis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nellie Georgiou-Karistianis.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Low, SC., Corben, L.A., Delatycki, M.B. et al. Excessive motor overflow reveals abnormal inter-hemispheric connectivity in Friedreich ataxia. J Neurol 260, 1757–1764 (2013). https://doi.org/10.1007/s00415-013-6869-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00415-013-6869-3

Keywords

Search

Navigation