Cerebellar Asymmetry and Cortical Connectivity in Monozygotic Twins with Discordant Handedness

Rosch, R. E.; Cowell, P. E.; Gurd, J M

doi:10.1007/s12311-017-0889-y

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Cerebellar Asymmetry and Cortical Connectivity in Monozygotic Twins with Discordant Handedness

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Author(s): R. E. Rosch ¹ ^, ² , P. E. Cowell ³ ^, , J. M. Gurd ³ ^, ⁴

Publication date (Electronic): 23 October 2017

Journal: Cerebellum (London, England)

Publisher: Springer US

Keywords: Cerebellum, Corpus callosum, Twins, monozygotic, Functional laterality, Neuroimaging

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Abstract

Handedness differentiates patterns of neural asymmetry and interhemispheric connectivity in cortical systems that underpin manual and language functions. Contemporary models of cerebellar function incorporate complex motor behaviour and higher-order cognition, expanding upon earlier, traditional associations between the cerebellum and motor control. Structural MRI defined cerebellar volume asymmetries and correlations with corpus callosum (CC) size were compared in 19 pairs of adult female monozygotic twins strongly discordant for handedness (MZHd). Volume and asymmetry of cerebellar lobules were obtained using automated parcellation.CC area and regional widths were obtained from midsagittal planimetric measurements. Within the cerebellum and CC, neurofunctional distinctions were drawn between motor and higher-order cognitive systems. Relationships amongst regional cerebellar asymmetry and cortical connectivity (as indicated by CC widths) were investigated. Interactions between hemisphere and handedness in the anterior cerebellum were due to a larger right-greater-than-left hemispheric asymmetry in right-handed (RH) compared to left-handed (LH) twins. In LH twins only, anterior cerebellar lobule volumes (IV, V) for motor control were associated with CC size, particularly in callosal regions associated with motor cortex connectivity. Superior posterior cerebellar lobule volumes (VI, Crus I, Crus II, VIIb) showed no correlation with CC size in either handedness group. These novel results reflected distinct patterns of cerebellar-cortical relationships delineated by specific CC regions and an anterior-posterior cerebellar topographical mapping. Hence, anterior cerebellar asymmetry may contribute to the greater degree of bilateral cortical organisation of frontal motor function in LH individuals.

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Topography of the human corpus callosum revisited--comprehensive fiber tractography using diffusion tensor magnetic resonance imaging.

Sabine Hofer, Jens Frahm (2006)

Several tracing studies have established a topographical distribution of fiber connections to the cortex in midsagittal cross-sections of the corpus callosum (CC). The most prominent example is Witelson's scheme, which defines five vertical partitions mainly based on primate data. Conventional MRI of the human CC does not reveal morphologically discernable structures, although microscopy techniques identified myelinated axons with a relatively small diameter in the anterior and posterior third of the CC as opposed to thick fibers in the midbody and posterior splenium. Here, we applied diffusion tensor imaging (DTI) in conjunction with a tract-tracing algorithm to gain cortical connectivity information of the CC in individual subjects. With DTI-based tractography, we distinguished five vertical segments of the CC, containing fibers projecting into prefrontal, premotor (and supplementary motor), primary motor, and primary sensory areas as well as into parietal, temporal, and occipital cortical areas. Striking differences to Witelson's classification were recognized in the midbody and anterior third of the CC. In particular, callosal motor fiber bundles were found to cross the CC in a much more posterior location than previously indicated. Differences in water mobility were found to be in qualitative agreement with differences in the microstructure of transcallosal fibers yielding the highest anisotropy in posterior regions of the CC. The lowest anisotropy was observed in compartments assigned to motor and sensory cortical areas. In conclusion, DTI-based fiber tractography of healthy human subjects suggests a modification of the widely accepted Witelson scheme and a new classification of vertical CC partitions.

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Increased corpus callosum size in musicians.

G Schlaug (1995)

Using in-vivo magnetic resonance morphometry it was investigated whether the midsagittal area of the corpus callosum (CC) would differ between 30 professional musicians and 30 age-, sex- and handedness-matched controls. Our analyses revealed that the anterior half of the CC was significantly larger in musicians. This difference was due to the larger anterior CC in the subgroup of musicians who had begun musical training before the age of 7. Since anatomic studies have provided evidence for a positive correlation between midsagittal callosal size and the number of fibers crossing through the CC, these data indicate a difference in interhemispheric communication and possibly in hemispheric (a)symmetry of sensorimotor areas. Our results are also compatible with plastic changes of components of the CC during a maturation period within the first decade of human life, similar to those observed in animal studies.

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The cerebellum predicts the timing of perceptual events.

Jill O'Reilly, M. Marsel Mesulam, Anna Christina Nobre (2008)

Prospective (forward) temporal-spatial models are essential for both action and perception, but the literature on perceptual prediction has primarily been limited to the spatial domain. In this study we asked how the neural systems of perceptual prediction change, when change-over-time must be modeled. We used a naturalistic paradigm in which observers had to extrapolate the trajectory of an occluded moving object to make perceptual judgments based on the spatial (direction) or temporal-spatial (velocity) characteristics of object motion. Using functional magnetic resonance imaging we found that a region in posterior cerebellum (lobule VII crus 1) was engaged specifically when a temporal-spatial model was required (velocity judgment task), suggesting that circuitry involved in motor forward-modeling may also be engaged in perceptual prediction when a model of change-over-time is required. This cerebellar region appears to supply a temporal signal to cortical networks involved in spatial orienting: a frontal-parietal network associated with attentional orienting was engaged in both (spatial and temporal-spatial) tasks, but functional connectivity between these regions and the posterior cerebellum was enhanced in the temporal-spatial prediction task. In addition to the oculomotor spatial orienting network, regions involved in hand movements (aIP and PMv) were recruited in the temporal-spatial task, suggesting that the nature of perceptual prediction may bias the recruitment of sensory-motor networks in orienting. Finally, in temporal-spatial prediction, functional connectivity was enhanced between the cerebellum and the putamen, a structure which has been proposed to supply the brain's metric of time, in the temporal-spatial prediction task.

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Author and article information

Contributors

P. E. Cowell: +44(0)114-222-2426 , p.e.cowell@sheffield.ac.uk

Journal

Journal ID (nlm-ta): Cerebellum

Journal ID (iso-abbrev): Cerebellum

Title: Cerebellum (London, England)

Publisher: Springer US (New York )

ISSN (Print): 1473-4222

ISSN (Electronic): 1473-4230

Publication date (Electronic): 23 October 2017

Publication date PMC-release: 23 October 2017

Publication date (Print): 2018

Volume: 17

Issue: 2

Pages: 191-203

Affiliations

[1 ]ISNI 0000000121901201, GRID grid.83440.3b, Wellcome Trust Centre for Neuroimaging, Institute of Neurology, , University College London, ; London, UK

[2 ]ISNI 0000000121901201, GRID grid.83440.3b, Developmental Neurosciences Programme, UCL Great Ormond Street Institute of Child Health, , University College London, ; London, UK

[3 ]ISNI 0000 0004 1936 9262, GRID grid.11835.3e, Department of Human Communication Sciences, , University of Sheffield, ; 362 Mushroom Lane, Sheffield, S10 2TS UK

[4 ]ISNI 0000 0004 1936 8948, GRID grid.4991.5, Nuffield Department of Clinical Neurosciences, , University of Oxford, ; Oxford, UK

Article

Publisher ID: 889

DOI: 10.1007/s12311-017-0889-y

PMC ID: 5849645

PubMed ID: 29063351

SO-VID: d42ee618-c476-430d-a88a-0dda00c0ab0c

License:

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

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Funding

Funded by: FundRef http://dx.doi.org/10.13039/100004440, Wellcome Trust;

Award ID: 106556/Z/14/Z

Funded by: FundRef http://dx.doi.org/10.13039/501100000265, Medical Research Council;

Funded by: Critchley Charitable Trust

Funded by: FundRef http://dx.doi.org/10.13039/501100000286, British Academy;

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ScienceOpen disciplines: Neurology

Keywords: cerebellum,corpus callosum,twins, monozygotic,functional laterality,neuroimaging

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ScienceOpen disciplines: Neurology

Keywords: cerebellum, corpus callosum, twins, monozygotic, functional laterality, neuroimaging

Cerebellar Asymmetry and Cortical Connectivity in Monozygotic Twins with Discordant Handedness

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Most cited references 61

Topography of the human corpus callosum revisited--comprehensive fiber tractography using diffusion tensor magnetic resonance imaging.

Increased corpus callosum size in musicians.

The cerebellum predicts the timing of perceptual events.

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