Cortical Folding of the Primate Brain: An Interdisciplinary Examination of the Genetic Architecture, Modularity, and Evolvability of a Significant Neurological Trait in Pedigreed Baboons (Genus Papio)

By Atkinson, Elizabeth G.; Rogers, Jeffrey et al. | Genetics, June 2015 | Go to article overview

Cortical Folding of the Primate Brain: An Interdisciplinary Examination of the Genetic Architecture, Modularity, and Evolvability of a Significant Neurological Trait in Pedigreed Baboons (Genus Papio)


Atkinson, Elizabeth G., Rogers, Jeffrey, Mahaney, Michael C., Cox, Laura A., Cheverud, James M., Genetics


THE extent of folding of the cerebral cortex, known as "cortical gyrification," has dramatically increased during primate evolution, in parallel with increasing brain volumes. The cortex of Old World monkeys is significantly more folded (gyrified) than that of New World monkeys (Zilles et al. 1989; Martin 1990), and the great apes have the highest degree of gyrification in nonhuman primates (Preuss et al. 2004). Humans are outliers even within the primate clade, with our brain being almost 30% more folded than that of chimps (Rogers et al. 2010). Powerful physical constraints on the upper limit of human neonatal brain volume drive selection toward the most compact brain possible (Rosenberg and Trevathan 2002), while humankind's ecological niche demands high cognitive potential. Since the cell bodies of neurons-the functional units of information processing in the brain-are located in the outermost layer of the laminar brain system, folding the cerebral cortex is an effective method of increasing surface area in which to allocate neurons with minimal overall brain volume expansion.

Selection for a larger brain volume does not automatically create one that is more folded. In fact, in baboons, genetic changes associated with increased brain size have been shown to result in a cortex with fewer folds (Rogers et al. 2010). Human congenital abnormalities also demonstrate the separation of these two phenotypes: conditions of abnormal brain volumes typically present with normal gyrification and vice versa (Stevenson 2006). These findings suggest that gyrification has a separate genetic basis from brain size, so the trend of increased folding in the primate lineage involves selective forces that have been working separately but in tandem with those increasing gross brain volume. While there has been extensive work examining changes in brain size among primates, cortical gyrification has a unique evolutionary history that has not yet been broadly explored.

Previous studies using magnetic resonance (MR) imaging provide preliminary evidence for a heritable genetic component to cortical variation in the baboon population studied here, generally estimating the heritability of cortical morphological features as between 20 and 40% (Mahaney et al. 1993; Rogers et al. 2007; Kochunov et al. 2010). As only ^150 MR scans were previously available, however, precise genetic mapping was impossible. By expanding the sample to glean information from ^1000 skull computed tomography (CT) scans collected in this pedigreed population, we were able to thoroughly assess variation and conduct QTL mapping to isolate defined chromosome regions affecting cortical gyrification phenotypes. QTL techniques are useful in that they provide an unbiased way to discover novel genomic regions associated with traits of interest in addition to implicating known genes in performing unanticipated novel functions. Additionally, conditions of dominance and epistatic interactions can be assessed and the power and strength of a genetic association to the phenotype quantified. The pedigree of the baboon population with which we are working includes six generations, resulting in a genomic linkage map (Rogers et al. 2000; Cox et al. 2006) that is quite well saturated with molecular markers thanks to the many resultant recombination events. This allowed us to isolate relatively narrow regions of interest containing small numbers of candidate genes. The advantage of pedigree-based linkage analyses lies in the fact that variants can be examined directly using identity-bydescent information rather than relying on variant state as a proxy. Furthermore, the effect size attributable to the implicated chromosomal regions can be reasonably estimated and situations of polygeny and/or pleiotropy detected.

Gyrification is extremely interesting from an evolutionary perspective for its neurobiological implications. Not only is increased gyrification useful for fitting more neurons within the skull, but patterns of sulci and gyri have direct implications with regard to the neural network (Ventura-Antunes et al. …

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Cortical Folding of the Primate Brain: An Interdisciplinary Examination of the Genetic Architecture, Modularity, and Evolvability of a Significant Neurological Trait in Pedigreed Baboons (Genus Papio)
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