PLoS ONE 12(6): e0179624

Developmental trajectory of the corpus callosum from infancy to the juvenile stage: Comparative MRI between chimpanzees and humans

Tomoko Sakai, Akichika Mikami, Juri Suzuki, Takako Miyabe-Nishiwaki, Mie Matsui, Masaki Tomonaga, Yuzuru Hamada, Tetsuro Matsuzawa, Hideyuki Okano, Kenichi Oishi

Abstract

The brain size of humans has increased dramatically during the evolution of Homo sapiens, along with the acquisition of uniquely human features, such as language, memory, self-awareness, creativity, and social communication [1–5]. Elucidating the similarities and differences in the ontogeny of brain structures between humans and our closest living primate relatives, chimpanzees, is important to understand the unique features of the human brain. The corpus callosum (CC) is the major commissural white matter bundle that connects the left and right cerebral hemispheres and provides interhemispheric integration, which is related to sensory, motor, and higher-order cognitive functions [6, 7]. The CC is present in all primates and has evolved with the neocortex [8, 9]. The CC exhibits a topographic pattern of the different cortical areas [7, 10, 11], which is associated with different regions: the rostrum; genu; rostral body; and the anterior midbody connect regions of the prefrontal and frontal cortex; the posterior midbody connects the region of the somatosensory cortex; the isthmus connects regions of the parietal and superior temporal cortex; and the splenium connects the occipital, inferior temporal, and parietal regions [12–17]. This topographic relationship is similar in humans and chimpanzees [18]. The midsagittal area of the CC has been commonly used as a sensitive marker of brain development and maturation [19–23], since the CC area is related to number of axons and morphology, such as axon diameter and myelination [24–28]. In humans, midsagittal CC areas increase rapidly during the first two to three years of life (corresponds to infancy: note that the anthropological definition [29–36], which is different from the medical definition, is adopted in this report. See the Section “Definitions of developmental stages" for details) [37, 38] and continue to increase slowly during the juvenile stage, adolescence [21–23, 38–40], and young adulthood, until the third decade of life [19, 21, 41, 42]. In chimpanzees, a cross-sectional magnetic resonance imaging (MRI) study of the ages from 6 to 54 years (corresponds to the end of the juvenile stage to old age) indicated a gradual increase in the CC areas during this age-range, which was similar to that seen in humans. The only exception was found in the rostrum subdivision of the CC, with no significant increase during this age range [43]. Since the study did not include chimpanzees that were less than six years of age [43], whether there is a rapid increase in CC areas during infancy in chimpanzees, such as that seen in humans, is still unknown. How the rostrum develops during infancy is of particular interest, since the developmental trajectory after the juvenile stage in chimpanzees is different from that seen in humans. To investigate the developmental changes during infancy and the juvenile stage of the chimpanzee CC, we longitudinally quantified areas of the midsagittal total CC and the CC subdivisions of four chimpanzees from 1.8 months to six years of age (infancy to the juvenile stage), using MRI, and compared the results with those of humans.

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Sakai T, Mikami A, Suzuki J, Miyabe-Nishiwaki T, Matsui M, Tomonaga M, Hamada Y, Matsuzawa T, Okano H, Oishi K (2017) Developmental trajectory of the corpus callosum from infancy to the juvenile stage: Comparative MRI between chimpanzees and humans PLoS ONE 12(6): e0179624