Coerced training of the nondominant hand resulting in cortical reorganization: a high-field functional magnetic resonance imaging study

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Object. The authors investigated brain strategies associated with hand use in an attempt to clarify genetic and nongenetic factors influencing handedness by using high-field functional magnetic resonance imaging.

Methods. Three groups of patients were studied. The first two groups comprised individuals in whom handedness developed spontaneously (right-handed and left-handed groups). The third group comprised individuals who were coercively trained to use the right hand and developed mixed handedness, referred to here as trained ambidexterity. All trained ambidextrous volunteers were certain that they were innately left-handed, but due to social pressure had modified their preferred hand use for certain tasks common to the right hand.

Although right-handed and left-handed volunteers displayed virtually identical cortical activation, involving homologous cortex primarily located contralateral to the hand motion, trained ambidextrous volunteers exhibited a clearly unique activation pattern. During right-handed motion, motor areas in both hemispheres were activated in these volunteers. During left-handed motion, the right supplemental motor area and the right intermediate zone of the anterior cerebellar lobe were activated significantly more frequently than observed in naturally right-handed or left-handed volunteers.

Conclusions. The results provide strong evidence that cortical organization of spontaneously developed right- and left-handedness involves homologous cortex primarily located contralateral to the hand motion, and this organization is likely to be prenatally determined. By contrast, coerced training of the nondominant hand during the early stages of an individual's development results in mixed handedness (trained ambidexterity), indicating cortical reorganization.

Article Information

Address reprint requests to: Tsutomu Nakada, M.D., Ph.D., Center for Integrated Human Brain Science, Brain Research Institute, University of Niigata, 1 Asahimachi, Niigata 951–8585, Japan. email: tnakada@bri.niigata-u.ac.jp.

© AANS, except where prohibited by US copyright law.

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Figures

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    Representative functional maps for right-handed, left-handed, and trained ambidextrous volunteers obtained during motions of the right and left hands. The left (L) and right (R) hemispheres are indicated. Although the pattern of activation for right- and left-handed individuals is virtually identical and located primarily contralateral to the site of the hand motion, activation maps in trained ambidextrous volunteers are clearly different, demonstrating greater areas of activation extending into parietal cortices.

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    Schematic summary of analyses performed in each group (15 volunteers/group). The size of the interior circle provides a relative indication of the number of volunteers with activation of the specified anatomical site. Asterisks indicate a significant increase in the frequency of activation compared with the other two groups. The activation pattern of trained ambidextrous volunteers was unequivocally distinct from that of left- and right-handed volunteers. The activation pattern in the ambidextrous group shared an intriguing similarity with that of right-handed stroke patients in whom fMR images demonstrated cortical reorganization and who clinically had a slow recovery from their hemiparesis. Cbll = anterior lobe of the cerebellum; M1 = primary motor cortex; SMA = supplementary motor area.

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    Schematic summary of patients with hemiparesis who exhibited a slow, but significant motor recovery during the first 6 months after the onset of stroke. All patients had a subcortical lesion and had been right-handed before stroke onset. The size of the internal circles provides a relative indication of the number of volunteers in whom activation of the specified anatomical site was activated relative to healthy volunteers (see Fig. 2). Asterisks indicate a significant increase in the frequency of activation in the patient group compared with healthy volunteers, whereas the dagger indicates a significant decrease. Arrows indicate the lesion. Note that the cortical activation pattern of the paretic hand of patients with hemiparesis who had recovery of function is almost identical to that associated with the right hand motion of trained ambidextrous volunteers (see Fig. 2).

References

  • 1.

    Annett M: Genetic and nongenetic influences on handedness. Behav Genet 8:2272491978Annett M: Genetic and nongenetic influences on handedness. Behav Genet 8:227–249 1978

    • Search Google Scholar
    • Export Citation
  • 2.

    Carter-Saltzman L: Biological and sociocultural effects of handedness: comparison between biological and adoptive families. Science 209:126312651980Carter-Saltzman L: Biological and sociocultural effects of handedness: comparison between biological and adoptive families. Science 209:1263–1265 1980

    • Search Google Scholar
    • Export Citation
  • 3.

    Fujii YNakada T: Cortical reorganization in patients with subcortical hemiparesis: neural mechanisms of functional recovery and prognostic implication. J Neurosurg 98:64732003Fujii Y Nakada T: Cortical reorganization in patients with subcortical hemiparesis: neural mechanisms of functional recovery and prognostic implication. J Neurosurg 98:64–73 2003

    • Search Google Scholar
    • Export Citation
  • 4.

    Klar AJ: A single locus, RGHT, specifies preference for hand utilization in humans. Cold Spring Harb Symp Quant Biol 61:59651996Klar AJ: A single locus RGHT specifies preference for hand utilization in humans. Cold Spring Harb Symp Quant Biol 61:59–65 1996

    • Search Google Scholar
    • Export Citation
  • 5.

    McManus ICBryden MP: The genetics of handedness, cerebral dominance and lateralization in Rapin ISegalowitz SJ (eds): Handbook of Neuropsychology. Amsterdam: Elsevier1992 Vol 6 pp 251281McManus IC Bryden MP: The genetics of handedness cerebral dominance and lateralization in Rapin I Segalowitz SJ (eds): Handbook of Neuropsychology. Amsterdam: Elsevier 1992 Vol 6 pp 251–281

    • Search Google Scholar
    • Export Citation
  • 6.

    Nakada TFujii YKwee IL: Brain strategies for reading in the second language are determined by the first language. Neurosci Res 40:3513582001Nakada T Fujii Y Kwee IL: Brain strategies for reading in the second language are determined by the first language. Neurosci Res 40:351–358 2001

    • Search Google Scholar
    • Export Citation
  • 7.

    Nakada TFujii YYoneoka Yet al: Planum temporale where spoken and written language meet. Eur Neurol 46:1211252001Nakada T Fujii Y Yoneoka Y et al: Planum temporale where spoken and written language meet. Eur Neurol 46:121–125 2001

    • Search Google Scholar
    • Export Citation
  • 8.

    Nakada TSuzuki KFujii Yet al: Independent component-cross correlation-sequential epoch (ICS) analysis of high field fMRI time series: direct visualization of dual representation of the primary motor cortex in human. Neurosci Res 37:2372442000Nakada T Suzuki K Fujii Y et al: Independent component-cross correlation-sequential epoch (ICS) analysis of high field fMRI time series: direct visualization of dual representation of the primary motor cortex in human. Neurosci Res 37:237–244 2000

    • Search Google Scholar
    • Export Citation
  • 9.

    Oldfield RC: The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:971131971Oldfield RC: The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113 1971

    • Search Google Scholar
    • Export Citation
  • 10.

    Shimizu AEndo M: Handedness and familial sinistrality in a Japanese student population. Cortex 19:2652721983Shimizu A Endo M: Handedness and familial sinistrality in a Japanese student population. Cortex 19:265–272 1983

    • Search Google Scholar
    • Export Citation
  • 11.

    Webster WGPoulos M: Handedness distributions among adults who stutter. Cortex 23:7057081987Webster WG Poulos M: Handedness distributions among adults who stutter. Cortex 23:705–708 1987

    • Search Google Scholar
    • Export Citation

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