Nurture versus nature: long-term impact of forced right-handedness on structure of pericentral cortex and basal ganglia

Stefan Klöppel; Jean-Francois Mangin; Anna Vongerichten; Richard S J Frackowiak; Hartwig R Siebner

doi:10.1523/JNEUROSCI.4394-09.2010

Nurture versus nature: long-term impact of forced right-handedness on structure of pericentral cortex and basal ganglia

Stefan Klöppel, Jean-Francois Mangin, Anna Vongerichten, Richard S J Frackowiak, Hartwig R Siebner

54 Citations (Scopus)

Abstract

Does a conflict between inborn motor preferences and educational standards during childhood impact the structure of the adult human brain? To examine this issue, we acquired high-resolution T1-weighted magnetic resonance scans of the whole brain in adult "converted" left-handers who had been forced as children to become dextral writers. Analysis of sulcal surfaces revealed that consistent right- and left-handers showed an interhemispheric asymmetry in the surface area of the central sulcus with a greater surface contralateral to the dominant hand. This pattern was reversed in the converted group who showed a larger surface of the central sulcus in their left, nondominant hemisphere, indicating plasticity of the primary sensorimotor cortex caused by forced use of the nondominant hand. Voxel-based morphometry showed a reduction of gray matter volume in the middle part of the left putamen in converted left-handers relative to both consistently handed groups. A similar trend was found in the right putamen. Converted subjects with at least one left-handed first-degree relative showed a correlation between the acquired right-hand advantage for writing and the structural changes in putamen and pericentral cortex. Our results show that a specific environmental challenge during childhood can shape the macroscopic structure of the human basal ganglia. The smaller than normal putaminal volume differs markedly from previously reported enlargement of cortical gray matter associated with skill acquisition. This indicates a differential response of the basal ganglia to early environmental challenges, possibly related to processes of pruning during motor development.

Original language	English
Journal	Journal of Neuroscience
Volume	30
Issue number	9
Pages (from-to)	3271-5
Number of pages	5
ISSN	0270-6474
DOIs	https://doi.org/10.1523/JNEUROSCI.4394-09.2010
Publication status	Published - 3 Mar 2010

Keywords

Adaptation, Physiological
Adult
Basal Ganglia
Brain Mapping
Dominance, Cerebral
Female
Functional Laterality
Humans
Hypertrophy
Learning
Magnetic Resonance Imaging
Male
Middle Aged
Motor Cortex
Motor Skills
Movement
Neuronal Plasticity
Neuropsychological Tests
Putamen
Writing
Young Adult

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10.1523/JNEUROSCI.4394-09.2010

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title = "Nurture versus nature: long-term impact of forced right-handedness on structure of pericentral cortex and basal ganglia",

abstract = "Does a conflict between inborn motor preferences and educational standards during childhood impact the structure of the adult human brain? To examine this issue, we acquired high-resolution T1-weighted magnetic resonance scans of the whole brain in adult {"}converted{"} left-handers who had been forced as children to become dextral writers. Analysis of sulcal surfaces revealed that consistent right- and left-handers showed an interhemispheric asymmetry in the surface area of the central sulcus with a greater surface contralateral to the dominant hand. This pattern was reversed in the converted group who showed a larger surface of the central sulcus in their left, nondominant hemisphere, indicating plasticity of the primary sensorimotor cortex caused by forced use of the nondominant hand. Voxel-based morphometry showed a reduction of gray matter volume in the middle part of the left putamen in converted left-handers relative to both consistently handed groups. A similar trend was found in the right putamen. Converted subjects with at least one left-handed first-degree relative showed a correlation between the acquired right-hand advantage for writing and the structural changes in putamen and pericentral cortex. Our results show that a specific environmental challenge during childhood can shape the macroscopic structure of the human basal ganglia. The smaller than normal putaminal volume differs markedly from previously reported enlargement of cortical gray matter associated with skill acquisition. This indicates a differential response of the basal ganglia to early environmental challenges, possibly related to processes of pruning during motor development.",

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T2 - long-term impact of forced right-handedness on structure of pericentral cortex and basal ganglia

AU - Klöppel, Stefan

AU - Mangin, Jean-Francois

AU - Vongerichten, Anna

AU - Frackowiak, Richard S J

AU - Siebner, Hartwig R

PY - 2010/3/3

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N2 - Does a conflict between inborn motor preferences and educational standards during childhood impact the structure of the adult human brain? To examine this issue, we acquired high-resolution T1-weighted magnetic resonance scans of the whole brain in adult "converted" left-handers who had been forced as children to become dextral writers. Analysis of sulcal surfaces revealed that consistent right- and left-handers showed an interhemispheric asymmetry in the surface area of the central sulcus with a greater surface contralateral to the dominant hand. This pattern was reversed in the converted group who showed a larger surface of the central sulcus in their left, nondominant hemisphere, indicating plasticity of the primary sensorimotor cortex caused by forced use of the nondominant hand. Voxel-based morphometry showed a reduction of gray matter volume in the middle part of the left putamen in converted left-handers relative to both consistently handed groups. A similar trend was found in the right putamen. Converted subjects with at least one left-handed first-degree relative showed a correlation between the acquired right-hand advantage for writing and the structural changes in putamen and pericentral cortex. Our results show that a specific environmental challenge during childhood can shape the macroscopic structure of the human basal ganglia. The smaller than normal putaminal volume differs markedly from previously reported enlargement of cortical gray matter associated with skill acquisition. This indicates a differential response of the basal ganglia to early environmental challenges, possibly related to processes of pruning during motor development.

AB - Does a conflict between inborn motor preferences and educational standards during childhood impact the structure of the adult human brain? To examine this issue, we acquired high-resolution T1-weighted magnetic resonance scans of the whole brain in adult "converted" left-handers who had been forced as children to become dextral writers. Analysis of sulcal surfaces revealed that consistent right- and left-handers showed an interhemispheric asymmetry in the surface area of the central sulcus with a greater surface contralateral to the dominant hand. This pattern was reversed in the converted group who showed a larger surface of the central sulcus in their left, nondominant hemisphere, indicating plasticity of the primary sensorimotor cortex caused by forced use of the nondominant hand. Voxel-based morphometry showed a reduction of gray matter volume in the middle part of the left putamen in converted left-handers relative to both consistently handed groups. A similar trend was found in the right putamen. Converted subjects with at least one left-handed first-degree relative showed a correlation between the acquired right-hand advantage for writing and the structural changes in putamen and pericentral cortex. Our results show that a specific environmental challenge during childhood can shape the macroscopic structure of the human basal ganglia. The smaller than normal putaminal volume differs markedly from previously reported enlargement of cortical gray matter associated with skill acquisition. This indicates a differential response of the basal ganglia to early environmental challenges, possibly related to processes of pruning during motor development.

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KW - Adult

KW - Basal Ganglia

KW - Brain Mapping

KW - Dominance, Cerebral

KW - Female

KW - Functional Laterality

KW - Humans

KW - Hypertrophy

KW - Learning

KW - Magnetic Resonance Imaging

KW - Male

KW - Middle Aged

KW - Motor Cortex

KW - Motor Skills

KW - Movement

KW - Neuronal Plasticity

KW - Neuropsychological Tests

KW - Putamen

KW - Writing

KW - Young Adult

U2 - 10.1523/JNEUROSCI.4394-09.2010

DO - 10.1523/JNEUROSCI.4394-09.2010

M3 - Journal article

C2 - 20203186

SN - 0270-6474

VL - 30

SP - 3271

EP - 3275

JO - The Journal of neuroscience : the official journal of the Society for Neuroscience

JF - The Journal of neuroscience : the official journal of the Society for Neuroscience

IS - 9

ER -

Nurture versus nature: long-term impact of forced right-handedness on structure of pericentral cortex and basal ganglia

Abstract

Keywords

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