Human Brain Evolution Writ Large and Small
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M. A. Hofman and D. Falk (Eds.) Progress in Brain Research, Vol. 195 ISSN: 0079-6123 Copyright Ó 2012 Elsevier B.V. All rights reserved. CHAPTER 11 Human brain evolution writ large and small { { { { Chet C. Sherwood*, , Amy L. Bauernfeind , Serena Bianchi , Mary Ann Raghanti } } and Patrick R. Hof , { Department of Anthropology, The George Washington University, Washington, DC, USA { Department of Anthropology and School of Biomedical Sciences, Kent State University, Kent, OH, USA } Fishberg Department of Neuroscience and Friedman Brain Institute, Mount Sinai School of Medicine, New York, NY, USA } New York Consortium in Evolutionary Primatology, New York, NY, USA Abstract: Human evolution was marked by an extraordinary increase in total brain size relative to body size. While it is certain that increased encephalization is an important factor contributing to the origin of our species-specific cognitive abilities, it is difficult to disentangle which aspects of human neural structure and function are correlated by-products of brain size expansion from those that are specifically related to particular psychological specializations, such as language and enhanced “mentalizing” abilities. In this chapter, we review evidence from allometric scaling studies demonstrating that much of human neocortical organization can be understood as a product of brain enlargement. Defining extra-allometric specializations in humans is often hampered by a severe lack of comparative data from the same neuroanatomical variables across a broad range of primates. When possible, we highlight evidence for features of human neocortical architecture and function that cannot be easily explained as correlates of brain size and, hence, might be more directly associated with the evolution of uniquely human cognitive capacities. Keywords: pyramidal neuron; cortical area; chimpanzee; great ape. Human brain evolution writ large exceptionally large size. Although elephants and whales have larger brains than humans, allometric The most obvious and distinctive evolutionary scaling analyses have demonstrated that humans specialization of the modern human brain is its are the most encephalized of all mammals (Jerison, 1973; Martin and Harvey, 1985), with a brain that is more than three times larger than *Corresponding author. Tel.: þ1-202-994-6346; Fax: þ1-202-994-6097 would be expected for a primate at the same body E-mail: [email protected] mass (Holloway, 1979). This disproportionate DOI: 10.1016/B978-0-444-53860-4.00011-8 237 238 growth of the brain in the human lineage is a rel- “a theory that explains everything really explains atively recent phenomenon, having increased dra- nothing” seems apt. matically in the past 2.5 million years (Falk et al., To some extent, explaining human 2000; Holloway et al., 2004). Although it is appar- cognitive uniqueness as merely a by-product of ent that large brain size is a hallmark of human encephalization, absolute brain size, or total num- cognitive and cultural evolution, consensus is bers of neurons reflects the infancy of studies in lacking on the selection pressures driving evolutionary neuroscience. If the goal is to under- encephalization. Among the hypotheses put for- stand the distinctive neural bases of the specific ward, it has been proposed that the complexity behavioral abilities that are unique to humans, of social interaction, with a greater focus on coop- then how can any unitary variable explain such eration and learning from others (Boyd et al., a multifaceted suite of characteristics? Although 2011), as well as deception (Byrne and Whiten, still a source of debate, there appears to be a 1988), might have played a role. growing consensus that human cognition is most While difficult to test, these hypothesized unique in (1) the representational understanding causes of encephalization are appealing because of one’s own and other’s mental states, such as they attempt to explain the evolutionary benefits beliefs, desires, and goals—that is, “theory of associated with such a prominent feature of mind” or “mentalizing”—and (2) syntactically human neuroanatomy. Given the high energetic ordered symbolic communication in the form of costs of growing and maintaining neural tissue language (Hauser et al., 2002; Herrmann et al., (Aiello and Wheeler, 1995; Chugani and Phelps, 2007; Suddendorf et al., 2009). Even if brain 1986), it is reasonable to conclude that there must size can be understood as a major contributor be decisive fitness benefits associated with to human cognitive uniqueness in these respects, increased investment in brain mass beyond what it would still be necessary to learn more about is minimally necessary for a given body size. how this single large variable translates to Indeed, it has been demonstrated across taxa that smaller-scale differences that can be interpreted there is a trade-off between relative brain mass in terms of the development of connectivity, and other metabolically expensive tissues, as the integration and signaling of neurons, and the well as the extent and timing of life history flow of information within the central nervous stages (Barrickman et al., 2008; Barton and system. Further, advances from modern behav- Capellini, 2011; Deaner et al., 2002). Some have ioral neuroscience and clinical neuropsychology proposed that encephalization (Jerison, 1973)or show that dramatic differences in behavior, greater total numbers of neurons (Herculano- including social cognition and language, can be Houzel, 2011) can be taken as a satisfactory, mediated by subtle microstructural and molecular or singular, explanation for our cognitive cap- changes in brain organization (Arnold and acities. Among primates, correlations have been Breedlove, 1985; Craig and Halton, 2009; found between relative brain size and an Donaldson and Young, 2008; Robinson and enormously diverse range of variables, including Becker, 1986; Rosenzweig and Bennett, 1996), exercise capacity (Raichlen and Gordon, 2011), most often in the absence of any major difference the total amount of visual input as measured by in brain size. the size of the optic canal (Kirk, 2006), the extent At present, however, we have only a rudimen- of stereoscopy as indicated by the degree of tary understanding of the anatomical, functional, orbital convergence (Barton, 2004), behavioral and energetic consequences of increased brain innovation (Reader and Laland, 2002), sociality size or encephalization in human evolution. In (Shultz and Dunbar, 2010a), and executive large part, this is because only a few studies have function (Shultz and Dunbar, 2010b). The adage, yet probed the differences between human brains 239 and those of our close relatives, the great apes, in 1999b; Rilling and Seligman, 2002; Semendeferi any detail. Consequently, many questions remain and Damasio, 2000; Semendeferi et al., 1998, unanswered. For example, the extent to which 2001, 2002; Sharma et al., 2010; Sherwood et al., particular modifications of neuronal morphology 2004, 2005a,b, 2006, 2007, 2010). In many ways, and cell type distributions regularly scale up with after taking overall brain size into account, com- increases in brain size is poorly known; it is parative evidence indicates that human neuro- unclear whether all regions of the cerebral cortex anatomy is not unexpected. For example, it has tend to increase in size at the same rate, or if been shown that the total number of neurons in there are particular areas that grow dispropor- the neocortex of humans closely matches tionately in correlation with brain size evolution; expectations for a primate of the same brain size and it has not been determined how the connec- (Azevedo et al., 2009), that total neocortical white tivity of the cerebral cortex varies with brain size. matter and corpus callosum size are predicted While theoretical models exist to predict some of by scaling (Bush and Allman, 2003; Rilling and these scaling regularities across mammals (Kaas, Insel, 1999a), and that the frontal cortex of 2000; Striedter, 2005), the absence of sufficient humans is not any larger than expected for brain comparative data from hominoid primates pre- size (Bush and Allman, 2004; Semendeferi et al., cludes clear assessment of whether human neural 2002). Human neocortical architecture at the organization is largely determined by increased histological level may also be examined from brain size, or alternatively, whether certain the perspective of allometric scaling. For example, features have emerged as departures from allo- the ratio of glial cells to neurons and the metric expectations. proportion of different subtypes of inhibitory Within this framework, we will discuss changes GABAergic interneurons in the dorsolateral in neocortical architecture in the evolution of the prefrontal cortex (Brodmann’s area 9) of humans human brain. Specifically, we will review evi- have been shown to be explained by scaling dence for microstructural modifications of neo- predictions (Sherwood et al., 2006, 2010). Thus, cortical structure as reflected in cellular at present, scaling exponents have been calculated distributions and neuronal morphology, and we for a number of macro- and microscopic neocorti- will consider their implications for energetics. cal variables, including neuron number and Other excellent recent reviews discuss the allome- density, cortical thickness and surface area, white tric scaling of larger anatomical components of matter volume, number of brain areas, number the brains among humans and other