Evolutionary and developmental implications of asymmetric brain folding in a large primate pedigree

Atkinson, Elizabeth G.; Rogers, Jeffrey; Cheverud, James M.

doi:10.1111/evo.12867

Cited by 10 publications

(9 citation statements)

References 73 publications

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“…Voxel-based structural asymmetries that are typically reported in the neuroimaging literature can be considered directional asymmetries. That is, a consistent left or right asymmetry is observed across a sample (Palmer and Strobeck, 1986;Atkinson et al, 2016). Body morphology also exhibits fluctuating asymmetries.…”

Section: Introductionmentioning

confidence: 70%

A deformation-based approach for characterizing brain asymmetries at different spatial scales of resolution

Eckert

Vaden

2019

Journal of Neuroscience Methods

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Background.-Structural cerebral asymmetries are hypothesized to provide an architectural foundation for functional asymmetries and behavioral lateralities. Studies of structural asymmetries typically focus on gray matter measures that are influenced by gross deformation fields used for normalization, and thus characterize a combination of different morphologic influences on structural asymmetries. New Method.-A deformation-based morphometry approach was developed to characterize structural asymmetries at different spatial scales of resolution, which can provide relatively more specific inference about the morphologic reason(s) for structural asymmetries, using a dataset of 347 typically developing children (7.00-12.92 years). Results.-Significant structural asymmetries were observed for a larger lobar spatial scale (e.g., frontal petalia) and for a smaller gyral/sulcal spatial scale of resolution (e.g., marginal sulcus). Total intracranial volume was significantly associated with asymmetries at the larger spatial scale of normalization, while age was significantly associated with asymmetries at the smaller scale of normalization. There were no significant anti-or fluctuating asymmetry effects based on Hartigan Dip Tests and Bonnett Tests, respectively. Comparison with Existing Method(s).-While spatially similar asymmetries were observed in both gray matter and deformation field data (e.g., medial planum temporale / Heschl's gyrus), the deformation approach characterizes asymmetries based on three iterations of successively smaller scales of normalization. Conclusions.-Structural asymmetries can be identified in normalization deformations with a procedure that is tailored for sensitivity to structures at different spatial scales of resolution where there may be different mechanisms for the expression of asymmetry.

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Section: Introductionmentioning

confidence: 70%

A deformation-based approach for characterizing brain asymmetries at different spatial scales of resolution

Eckert

Vaden

2019

Journal of Neuroscience Methods

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“…There have been a number of comparative studies in apes and monkeys that have quantified the length of the Sylvian fissure as a proxy to estimating PT asymmetries by direct measures on the cortical surface [79] or from three-dimensional reconstructions of sulci from MRI scans or endocasts [56,58,[80][81][82]. In general, the evidence suggests that both chimpanzees and various monkey species show a leftward bias in Sylvian fissure length, but to what extent that reflects asymmetries in PT surface area or volume remains unclear.…”

Section: (C) Comparisons To Other Primatesmentioning

confidence: 99%

Reproducibility of leftward planum temporale asymmetries in two genetically isolated populations of chimpanzees ( Pan troglodytes )

et al. 2020

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Once considered a hallmark of human uniqueness, brain asymmetry has emerged as a feature shared with several other species, including chimpanzees, one of our closest living relatives. Most notable has been the discovery of asymmetries in homologues of cortical language areas in apes, particularly in the planum temporale (PT), considered a central node of the human language network. Several lines of evidence indicate a role for genetic mechanisms in the emergence of PT asymmetry; however, the genetic determinants of cerebral asymmetries have remained elusive. Studies in humans suggest that there is heritability of brain asymmetries of the PT, but this has not been explored to any extent in chimpanzees. Furthermore, the potential influence of non-genetic factors has raised questions about the reproducibility of earlier observations of PT asymmetry reported in chimpanzees. As such, the present study was aimed at examining both the heritability of phenotypic asymmetries in PT morphology, as well as their reproducibility. Using magnetic resonance imaging, we evaluated morphological asymmetries of PT surface area (mm 2 ) and mean depth (mm) in captive chimpanzees ( n = 291) derived from two genetically isolated populations. Our results confirm that chimpanzees exhibit a significant population-level leftward asymmetry for PT surface area, as well as significant heritability in the surface area and mean depth of the PT. These results conclusively demonstrate the existence of a leftward bias in PT asymmetry in chimpanzees and suggest that genetic mechanisms play a key role in the emergence of anatomical asymmetry in this region.

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“…This difference points to a greater environmental influence on left -right differences in humans. Some authors have suggested that 'in the absence of differential developmental effects, the correlation between the two sides of the same organ should be 1' ( [55], p. 708). This expectation is true for perfectly symmetric organs and for those showing genetically determined DA.…”

Section: (A) Directional Asymmetry and Functional Lateralizationmentioning

confidence: 99%

The heritability of chimpanzee and human brain asymmetry

et al. 2016

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Human brains are markedly asymmetric in structure and lateralized in function, which suggests a relationship between these two properties. The brains of other closely related primates, such as chimpanzees, show similar patterns of asymmetry, but to a lesser degree, indicating an increase in anatomical and functional asymmetry during hominin evolution. We analysed the heritability of cerebral asymmetry in chimpanzees and humans using classic morphometrics, geometric morphometrics, and quantitative genetic techniques. In our analyses, we separated directional asymmetry and fluctuating asymmetry (FA), which is indicative of environmental influences during development. We show that directional patterns of asymmetry, those that are consistently present in most individuals in a population, do not have significant heritability when measured through simple linear metrics, but they have marginally significant heritability in humans when assessed through three-dimensional configurations of landmarks that reflect variation in the size, position, and orientation of different cortical regions with respect to each other. Furthermore, genetic correlations between left and right hemispheres are substantially lower in humans than in chimpanzees, which points to a relatively stronger environmental influence on left-right differences in humans. We also show that the level of FA has significant heritability in both species in some regions of the cerebral cortex. This suggests that brain responsiveness to environmental influences, which may reflect neural plasticity, has genetic bases in both species. These results have implications for the evolvability of brain asymmetry and plasticity among humans and our close relatives.

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Evolutionary and developmental implications of asymmetric brain folding in a large primate pedigree

Cited by 10 publications

References 73 publications

A deformation-based approach for characterizing brain asymmetries at different spatial scales of resolution

A deformation-based approach for characterizing brain asymmetries at different spatial scales of resolution

Reproducibility of leftward planum temporale asymmetries in two genetically isolated populations of chimpanzees ( Pan troglodytes )

The heritability of chimpanzee and human brain asymmetry

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