Human Brain Evolution
There have been significant changes in brain development, anatomy, and molecular biology over the course of human evolution.
Modern humans are characterized by remarkable specializations of cognition, including a language that is rich in syntactic complexity and symbolic meaning, a nuanced understanding of the mental states of others, a strong motivation to share in pursuing joint goals, an ability to manufacture sophisticated tools, and an extraordinary capacity for cultural learning. What are the evolutionary changes in brain structure and molecular biology that underlie these cognitive faculties? A comprehensive understanding of human brain evolution requires data from multiple perspectives, incorporating information from fossils, archaeology, comparative neuroanatomy, and genetics.
Evolution of the brain in the human lineage
Compared to other primates and our earliest hominin ancestors, modern humans have very large brains. Weighing approximately 1,400 g on average, our brains are roughly three times bigger than those of other great apes and also significantly larger than expected for a primate of our body size (Jerison 1973; Martin 1990). Because great apes (chimpanzees, bonobos, gorillas, and orangutans) are the closest living relatives of humans, they provide the most relevant phylogenetic basis for comparison. More broadly, there are several mammalian species, including elephants, dolphins, and whales, that have bigger brains than humans in absolute size. Pilot whale brains have even been shown to contain more neocortical neurons than those of humans (Mortensen et al. 2014). But humans are the most extreme outlier from the typical mammalian brain-body size scaling relationship. Although the average adult human brain is only approximately 2% of body size, it consumes about 20% of the whole body’s energy budget (nearly 400 kcal per day) due to the high level of activity of neuronal firing and signal transmission across synaptic connections (Kuzawa et al. 2014).
The hominin fossil record indicates that there has been a general trend over time for steadily increasing cranial capacity, accompanied by reorganization of cerebral morphology (de Sousa and Cunha 2012; Falk 2012; Holloway 2015). The cranial capacity of hominin ancestors shows very gradual increase in brain size early in the evolution of the lineage, with a period of more accelerated growth within the last two million years since the origin of the genus Homo (Du et al. 2018). There are some notable exceptions to this apparent trend, however, such as Homo naledi, a southern African hominin which had a small cranial capacity of 460 ml at about 300,000 years ago (Holloway et al. 2018), and Homo floresiensis from the island of Flores in Indonesia, which had a cranial capacity of approximately 400 ml at 190,000–50,000 years ago (Falk et al. 2005). Additionally, it is apparent that evolution of endocranial morphology in fossil hominins has not always been tightly synchronized with brain size changes (de Sousa and Cunha 2012; Falk 2012; Holloway 2015). For example, there are differences in endocranial shape between recent modern humans and similarly large-brained close relatives, the Neandertals, and the earliest Homo sapiens. The endocranial shape of modern humans is more globular, or rounded, due to bulging of the parietal and lateral cerebellar regions (Bruner et al. 2003; Neubauer et al. 2018).
Several interrelated features of life history biology are associated with the large brains of modern humans, including elevated nutritional and metabolic requirements, slower development, a longer lifespan, and more involvement in raising offspring by fathers and grandparents to assist mothers (Sherwood and Gómez-Robles 2017; Hawkes and Finlay 2018). Also, likely due to obstetrical or energetic constraints on the timing of parturition (Rosenberg 1992; Dunsworth et al. 2012), a larger fraction of brain growth in humans occurs after birth compared to other primates (Halley 2017). This means that significant neurodevelopmental events that lay the groundwork for brain function, such the refinement of synaptic connections and myelination of axons, take place over a prolonged period of time in a rich social and ecological context (Petanjek et al. 2011; Miller et al. 2012; Bianchi et al. 2013). The plastic brains of our helpless human infants incorporate these experience as neuronal circuits are being constructed, paving the way for more elaborate cultural learning (Bufill et al. 2011; Sherwood and Gómez-Robles 2017).
Detailed comparisons of human brain anatomy to that of other primates, particularly chimpanzees, have shown that the association regions of the prefrontal, posterior parietal, precuneus, and temporal cortex involved in higher-order cognitive functions have become especially expanded (Buckner and Krienen 2013; Rilling 2014; Bruner et al. 2017; Mars et al. 2017; Smaers et al. 2017). These cortical regions also mature particularly late in development (Sakai et al. 2011; Fjell et al. 2015). Some have argued that change in the absolute and proportional size of the prefrontal association cortex is tightly correlated with corresponding changes in other brain areas (Barton and Venditti 2013; Gabi et al. 2016), whereas other analyses show that human prefrontal cortex is enlarged beyond what would be predicted from primate brain scaling trends (Smaers et al. 2017).
To some extent, evolutionary changes to human association cortex have involved differential expansion of regions that have clear and well-established homologs in other primates (Donahue et al. 2018). Notably, many regions of the prefrontal cortex, including Broca’s language area, have been shown to be homologous among humans, great apes, and various other anthropoid species (Gil-da-Costa et al. 2006; Schenker et al. 2008; Wilson et al. 2015). Furthermore, cerebral hemispheric asymmetry is not entirely unique in human brain evolution, and seems to be an extension of trends that can be observed in other primates, especially great apes (Balzeau et al. 2011; Hopkins et al. 2015). Some other changes in human association cortex, however, appear to comprise proliferation of novel and functionally distinct areas. For example, data suggest that, compared to rhesus macaques, human intraparietal sulcus includes four additional motion-sensitive areas dedicated to processing of three-dimensional form in relation to motion (Orban et al. 2006). As a result, human parietal cortex might include more regions dedicated to processing of shape. Addition of these and other posterior parietal areas likely enhanced processing of visual and somatosensory information involved in manipulative abilities associated with tool production and handling (Stout and Chaminade 2007). More detailed comparative mapping of parietal cortex in great apes, however, is needed to resolve whether the observed intraparietal sulcus organization in humans is truly unique or shared with our closest primate relatives.
In addition to changes in the size of neuroanatomical structures, it is also apparent that there has been significant rewiring of fiber tract connections in human brain evolution. Several of the long-range pathways that interconnect the association regions of the frontal, parietal, and temporal cortex with each other and to the cerebellum are differentially expanded in human brains compared to other primates (Rilling et al. 2008; Balsters et al. 2010; Hecht et al. 2015). These circuits, which include the arcuate and superior longitudinal fasciculi, are involved in language, tool making, and imitation. Furthermore, reward systems utilizing the neurotransmitter dopamine in the striatum have been reshaped, likely to increase attention to social signals and facilitate vocal learning. Notably, comparative molecular and anatomical examinations of the basal ganglia show human-specific increase in dopaminergic innervation of the medial caudate nucleus (Raghanti et al. 2016; Sousa et al. 2017), a highly interconnected region of the striatum that is involved in language production, among other functions.
The evolutionary changes in the genome underlying distinctive molecular and cellular process of human brain development have also been investigated extensively. These studies have shown how single nucleotide substitutions, gene duplications, and modifications that regulate gene expression have impacted fundamental aspects of human neurobiology. Uniquely human genetic changes increase cell proliferation as the brain is being formed or stimulate neurons to grow more complex dendritic branches with a higher number of synaptic connections (Enard 2011; Florio et al. 2017; Suzuki et al. 2018). One particularly striking case is the gene SRGAP2, which has a human-specific duplicate (SRGAP2C) that functions to increase the density of synaptic spines on dendrites (Charrier et al. 2012). Relatedly, analyses of RNA transcript level in brain tissues of humans and other species have revealed increased gene expression in the human brain compared to nonhuman primates, which is not evident in non-brain tissue, such as the heart and the liver (Enard et al. 2002). These human-specific upregulated genes are enriched for functions including synaptic transmission and energy metabolism (Cáceres et al. 2003; Uddin et al. 2004; Somel et al. 2013; Muntané et al. 2015), supporting the idea that human brain evolution is characterized by molecular modifications to increase levels of neuronal activity (Preuss 2011).
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