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What is special about the human arcuate fasciculus? Lateralization, projections, and expansion.

ABSTRACT: Evolutionary adaptations of the human brain are the basis for our unique abilities such as language. An expansion of the arcuate fasciculus (AF), the dorsal language tract, in the human lineage involving left lateralization is considered canonical, but this hypothesis has not been tested in relation to other architectural adaptations in the human brain. Using diffusion-weighted MRI, we examined AF in the human and macaque and quantified species differences in white matter architecture and surface representations. To compare surface results in the two species, we transformed macaque representations to human space using a landmark-based monkey-to-human cortical expansion model. We found that the human dorsal AF, but not the ventral inferior fronto-occipital fasciculus (IFO), is left-lateralized. In the monkey AF is not lateralized. Moreover, compared to the macaque, human AF is relatively increased with respect to IFO. A comparison of human and transformed macaque surface representations suggests that cortical expansion alone cannot account for the species differences in the surface representation of AF. Our results show that the human AF has undergone critical anatomical modifications in comparison with the macaque AF. More generally, this work demonstrates that studies on the human brain specializations underlying the language connectome can benefit from current methodological advances in comparative neuroanatomy.

SUBMITTER: Eichert N

PROVIDER: S-EPMC6699597 | biostudies-literature | 2019 Sep

REPOSITORIES: biostudies-literature

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What is special about the human arcuate fasciculus? Lateralization, projections, and expansion.

Eichert Nicole N Verhagen Lennart L Folloni Davide D Jbabdi Saad S Khrapitchev Alexandre A AA Sibson Nicola R NR Mantini Dante D Sallet Jerome J Mars Rogier B RB

Cortex; a journal devoted to the study of the nervous system and behavior 20180512

Evolutionary adaptations of the human brain are the basis for our unique abilities such as language. An expansion of the arcuate fasciculus (AF), the dorsal language tract, in the human lineage involving left lateralization is considered canonical, but this hypothesis has not been tested in relation to other architectural adaptations in the human brain. Using diffusion-weighted MRI, we examined AF in the human and macaque and quantified species differences in white matter architecture and surfac ...[more]

PMID: 29937266

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Project description:Current evidence strongly suggests that the arcuate fasciculus (AF) is critical for language, from spontaneous speech and word retrieval to repetition and comprehension abilities. However, to further pinpoint its unique and differential role in language, its anatomy needs to be explored in greater detail and its contribution to language processing beyond that of known cortical language areas must be established. We address this in a comprehensive evaluation of the specific functional role of the AF in a well-characterized cohort of individuals with chronic aphasia (n = 33) following left hemisphere stroke. To evaluate macro- and microstructural integrity of the AF, tractography based on the constrained spherical deconvolution model was performed. The AF in the left and right hemispheres were then manually reconstructed using a modified 3-segment model (Catani et al., 2005), and a modified 2-segment model (Glasser and Rilling, 2008). The normalized volume and a measure of microstructural integrity of the long and the posterior segments of the AF were significantly correlated with language indices while controlling for gender and lesion volume. Specific contributions of AF segments to language while accounting for the role of specific cortical language areas - inferior frontal, inferior parietal, and posterior temporal - were tested using multiple regression analyses. Involvement of the following tract segments in the left hemisphere in language processing beyond the contribution of cortical areas was demonstrated: the long segment of the AF contributed to naming abilities; anterior segment - to fluency and naming; the posterior segment - to comprehension. The results highlight the important contributions of the AF fiber pathways to language impairments beyond that of known cortical language areas. At the same time, no clear role of the right hemisphere AF tracts in language processing could be ascertained. In sum, our findings lend support to the broader role of the left AF in language processing, with particular emphasis on comprehension and naming, and point to the posterior segment of this tract as being most crucial for supporting residual language abilities.

Dataset Information

What is special about the human arcuate fasciculus? Lateralization, projections, and expansion.

Publications

What is special about the human arcuate fasciculus? Lateralization, projections, and expansion.

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