Comparative morphology of the corpus callosum across the adult lifespan in chimpanzees (Pan troglodytes) and humans

Abstract

The human corpus callosum exhibits substantial atrophy in old age, which is stronger than what would be predicted from parallel changes in overall brain anatomy. To date, however, it has not been conclusively established whether this accentuated decline represents a common feature of brain aging across species, or whether it is a specific characteristic of the aging human brain. In the present cross-sectional study, we address this question by comparing age-related difference in corpus callosum morphology of chimpanzees and humans. For this purpose, we measured total midsagittal area and regional thickness of the corpus callosum from T1-weighted MRI data from 213 chimpanzees, aged between 9 and 54 years. The results were compared with data drawn from a large-scale human sample which was age-range matched using two strategies: (a) matching by chronological age (human sample size: n = 562), or (b) matching by accounting for differences in longevity and various maturational events between the species (i.e., adjusted human age range: 13.6 to 80.9 years; n = 664). Using generalized additive modeling to fit and compare aging trajectories, we found significant differences between the two species. The chimpanzee aging trajectory compared with the human trajectory was characterized by a slower increase from adolescence to middle adulthood, and by a lack of substantial decline from middle to old adulthood, which, however, was present in humans. Thus, the accentuated decline of the corpus callosum found in aging humans is not a universal characteristic of the aging brain, and appears to be human-specific. K E Y W O R D S aging, atrophy, comparative anatomy, corpus callosum, Pan troglodytes 1 | BACKGROUND The corpus callosum is the major white-matter commissure (Schmahmann & Pandya, 2006) and has an important role in human perception and cognition (Gazzaniga, 2000). It supports the integration of complementary sensory information distributed across the two hemispheres (e.g.,

Corpus callosum morphology across the lifespan in baboons (Papio anubis): a cross-sectional study of relative mid-sagittal surface area and thickness

“…In this, the present study supplements the findings of a series of previous studies suggesting that the aging trajectories of the corpus callosum differ substantially between primate species. The here reported linear trajectory of baboons, best resembles the rather flat lifespan trajectory found in capuchin monkeys (Phillips & Sherwood, 2012), but appears dissimilar to the more accentuated trajectories found in chimpanzees (Hopkins et al, 2016; Hopkins & Phillips, 2010; Westerhausen et al, 2020) and humans (Danielsen et al, 2020; Rauch & Jinkins, 1994; Salat et al, 1997). Figure 3 was created to follow-up on this comparative perspective.…”

“…Figure 3 was created to follow-up on this comparative perspective. It provides a visual comparison of GAM-fitted lifespan trajectory of the total baboon corpus callosum with the trajectories found in humans and chimpanzees reported in a previous study (Westerhausen et al, 2020). Adjusting for differences in longevity between the three species (Figure 3, left graph) it gets obvious that the trajectories deviate from each other both during development and in old age.…”

“…The present study did not find any significant sex differences in the baboon corpus callosum: neither did we detect a main effect of sex on midsagittal area or thickness measures, nor did we find any indication for differences in the lifespan trajectories between the sexes. In general, sex difference in the corpus callosum have been frequently examined in various primate species and yield inconsistent results (e.g., rhesus monkeys: Franklin et al, 2000; Payne, Cirilli, & Bachevalier, 2017; marmosets: Sakai et al, 2017; capuchin monkeys: Phillips, Sherwood, & Lilak, 2007; chimpanzees: Hopkins et al, 2016; Phillips & Hopkins, 2012; Westerhausen et al, 2020). Best studied regarding sex differences is obviously the human corpus callosum.…”

“…In both capuchin monkey ( Cebus paella ; Phillips & Sherwood, 2012) and rhesus monkeys ( Macaca mulatta ; Bowley, Cabral, Rosene, & Peters, 2010; Lacreuse et al, 2005) no significant old-age reduction of midsagittal area was found. Likewise, in chimpanzees ( Pan troglodytes ) a plateau or continuous increase of relative corpus callosum area and thickness has been reported in old age (Hopkins et al, 2016; Hopkins & Phillips, 2010; Westerhausen et al, 2020). A recent direct comparison of human and chimpanzee lifespan trajectories, additionally confirms that the old-age reduction in total midsagittal callosal area is significantly stronger in humans (Westerhausen et al, 2020).…”

“…Likewise, in chimpanzees ( Pan troglodytes ) a plateau or continuous increase of relative corpus callosum area and thickness has been reported in old age (Hopkins et al, 2016; Hopkins & Phillips, 2010; Westerhausen et al, 2020). A recent direct comparison of human and chimpanzee lifespan trajectories, additionally confirms that the old-age reduction in total midsagittal callosal area is significantly stronger in humans (Westerhausen et al, 2020). Thus, taken together, old-age atrophy of the corpus callosum has not been reported in any other primate species but humans, so that it appears tempting to conclude that it represents human□ specific phenomenon of brain aging.…”