Prolonged myelination in human neocortical evolution

Abstract

Nerve myelination facilitates saltatory action potential conduction and exhibits spatiotemporal variation during development associated with the acquisition of behavioral and cognitive maturity. Although human cognitive development is unique, it is not known whether the ontogenetic progression of myelination in the human neocortex is evolutionarily exceptional. In this study, we quantified myelinated axon fiber length density and the expression of myelinrelated proteins throughout postnatal life in the somatosensory (areas 3b/3a/1/2), motor (area 4), frontopolar (prefrontal area 10), and visual (areas 17/18) neocortex of chimpanzees (N = 20) and humans (N = 33). Our examination revealed that neocortical myelination is developmentally protracted in humans compared with chimpanzees. In chimpanzees, the density of myelinated axons increased steadily until adult-like levels were achieved at approximately the time of sexual maturity. In contrast, humans displayed slower myelination during childhood, characterized by a delayed period of maturation that extended beyond late adolescence. This comparative research contributes evidence crucial to understanding the evolution of human cognition and behavior, which arises from the unfolding of nervous system development within the context of an enriched cultural environment. Perturbations of normal developmental processes and the decreased expression of myelin-related molecules have been related to psychiatric disorders such as schizophrenia. Thus, these species differences suggest that the human-specific shift in the timing of cortical maturation during adolescence may have implications for vulnerability to certain psychiatric disorders.C omparative studies suggest that human neurobiological development is unique. For example, humans differ from other primates in extending a rapid, fetal-like brain mass growth rate into the first postnatal year, thereby achieving relatively large adult brain size (1). Gene expression patterns related to postnatal development of the prefrontal cortex are delayed in humans compared with chimpanzees and macaque monkeys (2). In addition, synapse maturation (3, 4) and axon myelination (5, 6) occur during later life history stages in humans compared with macaques. Furthermore, recent volumetric data obtained by using in vivo MRI demonstrates that human neural development and aging differ from those of our close nonhuman primate relatives (7-9). Together, these observations indicate that a marked delay in the developmental schedule of human neocortex may play an important role in the growth of connections that contribute to our species-specific cognitive abilities by providing greater opportunities for social learning to influence the establishment of circuits.

Differences in brain morphology and working memory capacity across childhood

“…White matter changes are thought to be a key process in postnatal brain development, which continues throughout childhood and adolescence into early adulthood (Barnea‐Goraly, 2005; Muftuler et al., 2012; Qiu, Tan, Zhou, & Khong, 2008; Tau & Peterson, 2010). In particular, the myelination of axons is thought to be a critical mechanism of brain development in this age range (Miller et al., 2012). Differences in microstructural properties, namely FA, as measured by diffusion MRI are directly related to myelination and have been linked to cognitive development (Clayden et al., 2012; Mabbott, Noseworthy, Bouffet, Laughlin, & Rockel, 2006).…”

Synaptogenesis and development of pyramidal neuron dendritic morphology in the chimpanzee neocortex resembles humans

“…These results suggest that several key features of human brain ontogeny for enhanced developmental plasticity emerged before the divergence of the chimpanzee and human lineages. In addition to these shared similarities of early postnatal development, later phases of human neocortical maturation appear to be more evolutionarily modified and distinct from chimpanzees, involving prolonged myelination that continues into early adulthood (30). When combined with changes to human social organization, the prolonged developmental plasticity and shift toward delayed development of the prefrontal cortex present in hominin ancestors may have increased learning potential for higher-order sociocognitive functions.…”

“…Indeed, many genetic differences between humans and other primates affect processes involved in cerebral development (33)(34)(35). Until recently, however, little was known about the nature of microstructural changes during neural ontogeny in the cerebral cortex of nonhuman primates other than macaques, making it difficult to assess how the developmental trajectory of the human brain might be unique (30). Our current analyses demonstrate that similar to humans, synaptic proliferation in chimpanzees is prolonged through the midjuvenile period, and development of pyramidal neurons in the prefrontal cortex is delayed relative to other cortical areas.…”

“…Relative to chimpanzees, however, human brain development is marked by more rapid addition of white matter volume during the first year of life (28,29). That white matter growth differs between humans and chimpanzees has been further demonstrated by recent histological analyses demonstrating that myelination within the cerebral cortex continues past adolescence in humans, whereas it is completed by sexual maturity in chimpanzees (30).…”

Diffusion-weighted imaging uncovers likely sources of processing-speed deficits in schizophrenia

“…Two decades of research have implicated impaired brain connectivity as a source of functional disability in schizophrenia (1, 2). Delayed information processing is one of the most robust cognitive deficits (3, 4) and may contribute to other cognitive impairments in working memory and executive function (4-6).Myelinated axons in the brain's white matter (WM) support its functionality by propagating electric signal transmissions through saltatory conductance (7,8). Reports of WM abnormalities in patients with schizophrenia are common and include reduced fractional anisotropy (FA) of water diffusion measured by diffusion tensor imaging (DTI) MRI (9-11) as well as reduced axonal myelin levels and glial cell density in postmortem brain studies (12)(13)(14).…”