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Normalisation of brain connectivity through compensatory behaviour, despite congenital hand absence.

Hahamy A, Sotiropoulos SN, Henderson Slater D, Malach R, Johansen-Berg H, Makin TR - Elife (2015)

Bottom Line: Compared with two-handed controls, one-handers showed reduced symmetry of hand region inter-hemispheric resting-state functional connectivity and corticospinal white matter microstructure.We therefore suggest that compensatory arm usage maintains symmetrical sensorimotor functional connectivity in one-handers.Since variability in spontaneous functional connectivity in our study reflects ecological behaviour, we propose that inter-hemispheric symmetry, typically observed in resting sensorimotor networks, depends on coordinated motor behaviour in daily life.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurobiology, Weizmann Institute of Science, Rehovot, Israel.

ABSTRACT
Previously we showed, using task-evoked fMRI, that compensatory intact hand usage after amputation facilitates remapping of limb representations in the cortical territory of the missing hand (Makin et al., 2013a). Here we show that compensatory arm usage in individuals born without a hand (one-handers) reflects functional connectivity of spontaneous brain activity in the cortical hand region. Compared with two-handed controls, one-handers showed reduced symmetry of hand region inter-hemispheric resting-state functional connectivity and corticospinal white matter microstructure. Nevertheless, those one-handers who more frequently use their residual (handless) arm for typically bimanual daily tasks also showed more symmetrical functional connectivity of the hand region, demonstrating that adaptive behaviour drives long-range brain organisation. We therefore suggest that compensatory arm usage maintains symmetrical sensorimotor functional connectivity in one-handers. Since variability in spontaneous functional connectivity in our study reflects ecological behaviour, we propose that inter-hemispheric symmetry, typically observed in resting sensorimotor networks, depends on coordinated motor behaviour in daily life.

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Increased structural asymmetry in one-handers.(A) White matter values (mean fractional anisotropy ± s.e.m.) were extracted from the bilateral corticospinal tracts of each participant, and laterality indices were computed to determine the level of white matter asymmetry across hemispheres ([(intact − residual)/(intact + residual)] for one-handers, and [(dominant − nondominant)/(dominant + nondominant)] for controls). Laterality indices were significantly higher in one-handers compared to controls. (B) To spatially identify regions of increased white-matter laterality, laterality indices were computed for each slice along the superior–inferior axis of the corticospinal tracts, and a group comparison was conducted using permutation-based cluster statistics. Regions showing significant group differences along the corticospinal tracts were centred around the posterior limb of the internal capsule, reflecting higher laterality in one-handers compared to controls. Results are presented on the left corticospinal tract from a posterior view. (C) Right: Regions that show significantly higher laterality values in one-handers are presented on the left corticospinal tract (highlighted in green) along with their spatial locations along the z axis, as marked by arrows. Left: The lateralisation profile of white matter microstructure along the corticospinal tract is represented by p-values, derived from the comparison between one-handers and controls. Higher values indicate stronger statistical differences. The red line marks the significance threshold, corrected for multiple comparisons. 1H, one-handers; CTR, controls; asterisks denote significance at the level of **p < 0.01.DOI:http://dx.doi.org/10.7554/eLife.04605.002
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fig1: Increased structural asymmetry in one-handers.(A) White matter values (mean fractional anisotropy ± s.e.m.) were extracted from the bilateral corticospinal tracts of each participant, and laterality indices were computed to determine the level of white matter asymmetry across hemispheres ([(intact − residual)/(intact + residual)] for one-handers, and [(dominant − nondominant)/(dominant + nondominant)] for controls). Laterality indices were significantly higher in one-handers compared to controls. (B) To spatially identify regions of increased white-matter laterality, laterality indices were computed for each slice along the superior–inferior axis of the corticospinal tracts, and a group comparison was conducted using permutation-based cluster statistics. Regions showing significant group differences along the corticospinal tracts were centred around the posterior limb of the internal capsule, reflecting higher laterality in one-handers compared to controls. Results are presented on the left corticospinal tract from a posterior view. (C) Right: Regions that show significantly higher laterality values in one-handers are presented on the left corticospinal tract (highlighted in green) along with their spatial locations along the z axis, as marked by arrows. Left: The lateralisation profile of white matter microstructure along the corticospinal tract is represented by p-values, derived from the comparison between one-handers and controls. Higher values indicate stronger statistical differences. The red line marks the significance threshold, corrected for multiple comparisons. 1H, one-handers; CTR, controls; asterisks denote significance at the level of **p < 0.01.DOI:http://dx.doi.org/10.7554/eLife.04605.002

Mentions: The corticospinal tracts mediate a range of descending pathways from cortical motor areas to the spinal cord, as well as ascending tracts to somatosensory cortex. To study structural alterations in motor-related pathways of one-handers, asymmetry in white matter microstructure of the bilateral corticospinal tracts was investigated. Fractional anisotropy (FA), an index commonly derived from diffusion MRI, was used as a probe of tissue microstructure. This measurement is thought to reflect myelination and fibre density, but is also influenced by other micro-features (e.g., membrane permeability, tissue geometry, see ‘Discussion’) (Zatorre et al., 2012; Jones et al., 2013; Sampaio-Baptista et al., 2013). One-handers showed increased asymmetry in white matter microstructure (reflected by decreased white matter FA in the corticospinal tract contralateral to the missing hand relative to the ipsilateral tract) compared to controls (p = 0.003, randomisation test, Figure 1A). The effect peaked at the posterior limb of the internal capsule (peak z coordinate = 88, p = 0.02 corrected, Figure 1B), an area that contains sensory thalamic fibres, but was also distributed across extensive regions of the tract (Figure 1C). No significant group differences were found for control tracts that are not directly associated with the sensorimotor system (Inferior fronto-occipital fasciculus: p = 0.28, Inferior longitudinal fasciculus: p = 0.27, randomisation tests).10.7554/eLife.04605.002Figure 1.Increased structural asymmetry in one-handers.


Normalisation of brain connectivity through compensatory behaviour, despite congenital hand absence.

Hahamy A, Sotiropoulos SN, Henderson Slater D, Malach R, Johansen-Berg H, Makin TR - Elife (2015)

Increased structural asymmetry in one-handers.(A) White matter values (mean fractional anisotropy ± s.e.m.) were extracted from the bilateral corticospinal tracts of each participant, and laterality indices were computed to determine the level of white matter asymmetry across hemispheres ([(intact − residual)/(intact + residual)] for one-handers, and [(dominant − nondominant)/(dominant + nondominant)] for controls). Laterality indices were significantly higher in one-handers compared to controls. (B) To spatially identify regions of increased white-matter laterality, laterality indices were computed for each slice along the superior–inferior axis of the corticospinal tracts, and a group comparison was conducted using permutation-based cluster statistics. Regions showing significant group differences along the corticospinal tracts were centred around the posterior limb of the internal capsule, reflecting higher laterality in one-handers compared to controls. Results are presented on the left corticospinal tract from a posterior view. (C) Right: Regions that show significantly higher laterality values in one-handers are presented on the left corticospinal tract (highlighted in green) along with their spatial locations along the z axis, as marked by arrows. Left: The lateralisation profile of white matter microstructure along the corticospinal tract is represented by p-values, derived from the comparison between one-handers and controls. Higher values indicate stronger statistical differences. The red line marks the significance threshold, corrected for multiple comparisons. 1H, one-handers; CTR, controls; asterisks denote significance at the level of **p < 0.01.DOI:http://dx.doi.org/10.7554/eLife.04605.002
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4281879&req=5

fig1: Increased structural asymmetry in one-handers.(A) White matter values (mean fractional anisotropy ± s.e.m.) were extracted from the bilateral corticospinal tracts of each participant, and laterality indices were computed to determine the level of white matter asymmetry across hemispheres ([(intact − residual)/(intact + residual)] for one-handers, and [(dominant − nondominant)/(dominant + nondominant)] for controls). Laterality indices were significantly higher in one-handers compared to controls. (B) To spatially identify regions of increased white-matter laterality, laterality indices were computed for each slice along the superior–inferior axis of the corticospinal tracts, and a group comparison was conducted using permutation-based cluster statistics. Regions showing significant group differences along the corticospinal tracts were centred around the posterior limb of the internal capsule, reflecting higher laterality in one-handers compared to controls. Results are presented on the left corticospinal tract from a posterior view. (C) Right: Regions that show significantly higher laterality values in one-handers are presented on the left corticospinal tract (highlighted in green) along with their spatial locations along the z axis, as marked by arrows. Left: The lateralisation profile of white matter microstructure along the corticospinal tract is represented by p-values, derived from the comparison between one-handers and controls. Higher values indicate stronger statistical differences. The red line marks the significance threshold, corrected for multiple comparisons. 1H, one-handers; CTR, controls; asterisks denote significance at the level of **p < 0.01.DOI:http://dx.doi.org/10.7554/eLife.04605.002
Mentions: The corticospinal tracts mediate a range of descending pathways from cortical motor areas to the spinal cord, as well as ascending tracts to somatosensory cortex. To study structural alterations in motor-related pathways of one-handers, asymmetry in white matter microstructure of the bilateral corticospinal tracts was investigated. Fractional anisotropy (FA), an index commonly derived from diffusion MRI, was used as a probe of tissue microstructure. This measurement is thought to reflect myelination and fibre density, but is also influenced by other micro-features (e.g., membrane permeability, tissue geometry, see ‘Discussion’) (Zatorre et al., 2012; Jones et al., 2013; Sampaio-Baptista et al., 2013). One-handers showed increased asymmetry in white matter microstructure (reflected by decreased white matter FA in the corticospinal tract contralateral to the missing hand relative to the ipsilateral tract) compared to controls (p = 0.003, randomisation test, Figure 1A). The effect peaked at the posterior limb of the internal capsule (peak z coordinate = 88, p = 0.02 corrected, Figure 1B), an area that contains sensory thalamic fibres, but was also distributed across extensive regions of the tract (Figure 1C). No significant group differences were found for control tracts that are not directly associated with the sensorimotor system (Inferior fronto-occipital fasciculus: p = 0.28, Inferior longitudinal fasciculus: p = 0.27, randomisation tests).10.7554/eLife.04605.002Figure 1.Increased structural asymmetry in one-handers.

Bottom Line: Compared with two-handed controls, one-handers showed reduced symmetry of hand region inter-hemispheric resting-state functional connectivity and corticospinal white matter microstructure.We therefore suggest that compensatory arm usage maintains symmetrical sensorimotor functional connectivity in one-handers.Since variability in spontaneous functional connectivity in our study reflects ecological behaviour, we propose that inter-hemispheric symmetry, typically observed in resting sensorimotor networks, depends on coordinated motor behaviour in daily life.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurobiology, Weizmann Institute of Science, Rehovot, Israel.

ABSTRACT
Previously we showed, using task-evoked fMRI, that compensatory intact hand usage after amputation facilitates remapping of limb representations in the cortical territory of the missing hand (Makin et al., 2013a). Here we show that compensatory arm usage in individuals born without a hand (one-handers) reflects functional connectivity of spontaneous brain activity in the cortical hand region. Compared with two-handed controls, one-handers showed reduced symmetry of hand region inter-hemispheric resting-state functional connectivity and corticospinal white matter microstructure. Nevertheless, those one-handers who more frequently use their residual (handless) arm for typically bimanual daily tasks also showed more symmetrical functional connectivity of the hand region, demonstrating that adaptive behaviour drives long-range brain organisation. We therefore suggest that compensatory arm usage maintains symmetrical sensorimotor functional connectivity in one-handers. Since variability in spontaneous functional connectivity in our study reflects ecological behaviour, we propose that inter-hemispheric symmetry, typically observed in resting sensorimotor networks, depends on coordinated motor behaviour in daily life.

Show MeSH