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Evolution of the Size and Functional Areas of the Human Brain ANRV287-AN35-20 ARI 9 September 2006 8:42 Evolution of the Size and Functional Areas of the Human Brain P. Thomas Schoenemann Department of Behavioral Sciences, University of Michigan–Dearborn, Dearborn, Michigan 48128; email: [email protected] Annu. Rev. Anthropol. 2006. 35:379–406 Key Words First published online as a Review in neuroanatomy, encephalization, behavior, adaptation, selection Advance on June 16, 2006 The Annual Review of Anthropology is online Abstract at anthro.annualreviews.org The human brain is one of the most intricate, complicated, and This article’s doi: impressive organs ever to have evolved. Understanding its evolu- by UNIVERSITY OF PENNSYLVANIA LIBRARY on 09/21/06. For personal use only. Annu. Rev. Anthropol. 2006.35:379-406. Downloaded from arjournals.annualreviews.org 10.1146/annurev.anthro.35.081705.123210 tion requires integrating knowledge from a variety of disciplines in Copyright c 2006 by Annual Reviews. the natural and social sciences. Four areas of research are particu- All rights reserved larly important to this endeavor. First, we need to understand basic 0084-6570/06/1021-0379$20.00 principles of brain evolution that appear to operate across broad classes of organisms. Second, we need to understand the ways in which human brains differ from the brains of our closest living rela- tives. Third, clues from the fossil record may allow us to outline the manner in which these differences evolved. Finally, studies of brain structure/function relationships are critical for us to make behav- ioral sense of the evolutionary changes that occurred. This review highlights important questions and work in each of these areas. 379 ANRV287-AN35-20 ARI 9 September 2006 8:42 INTRODUCTION specializations, and possible gene-expression changes.1 The evolution of the human brain has been Encephalization one of the most significant events in the quotient (EQ): evolution of life. Although the outline of calculated as the how and why this happened is being filled PATTERNS OF BRAIN ratio of a species’ in, many fundamental questions remain to actual brain size to EVOLUTION the size expected be answered. The fossil record, in concert given its body weight with a comparative neuroanatomical analy- Brain/Body Scaling sis of closely related species, shows that the How should species be compared with respect hominid brain increased in size more than to brain size? It has long been known that threefold over a period of approximately 2.5 brain size scales with body size across broad million years. However, it has become in- groups of animals (Dubois 1913). For this rea- creasingly clear that the human brain is not son, some measure of relative brain size has simply a large ape brain: Important quali- usually been favored in comparative studies. tative and quantitative changes occurred as Empirically the relationship between brain well. Some of these changes are a result of and body size can be estimated using a func- broad patterns of brain evolution that appear tion of the form [brain] = c[body]a, where c across species, either for developmental rea- and a are empirically derived constants. Be- sons or because of patterns of adaptation that cause the brain/body relationship is nonlin- are inherent in the nature of life. Some are ear, a simple ratio of brain to body is prob- presumably a result of direct selection for lematic (e.g., small animals have larger ratios specific behavioral abilities of various kinds. than larger animals on average). Encephaliza- Unraveling which adaptational explanations tion quotients (EQs) are widely used measures are possible or likely requires understanding of relative brain size that take this empiri- as much as we can about how brain struc- cal relationship between brain and body size ture relates to behavioral variation. Unrav- into account. They are simply the ratio of a eling the story of human evolution requires species’ actual brain size to the brain size ex- research in each of these areas: (a) general pected for an animal of its body size ( Jerison patterns of brain evolution, (b) compara- 1973). The expected brain size for a given tive assessment of brain anatomy across species is usually derived using a regression species, (c) the fossil history of human-brain (or other method, e.g., reduced major axis) of evolution, and (d ) brain structure/function log brain to log body size for the compari- relationships. son group of species, resulting in a formula of This review focuses on trying to under- the type [log brain] = log c + a[log body]. stand evolutionary changes in brain size as Jerison (1973) used mammals as the compar- by UNIVERSITY OF PENNSYLVANIA LIBRARY on 09/21/06. For personal use only. Annu. Rev. Anthropol. 2006.35:379-406. Downloaded from arjournals.annualreviews.org well as the proportions of different brain ison group, but one can estimate EQs, for areas. It highlights conceptual areas and example, on the basis of primates only. One questions that are prone to misunderstand- can also extend the concept to subcomponents ing, need particularly careful assessment, are of the brain and scale them either against of current controversy, or present impor- tant avenues for future research. It neces- sarily leaves out some research areas that 1 are both important and interesting, such as I encourage those interested in extended reviews of human brain evolution to consult Allman 1999, Deacon 1997, Falk deep cortical and brainstem nuclei, the evo- 1992, Geary 2005, Holloway et al. 2004a, and Striedter lution of specific neuron types and their 2005. 380 Schoenemann ANRV287-AN35-20 ARI 9 September 2006 8:42 body size or brain size (see, e.g., Schoenemann tunately, EQs are not so easily interpreted. 1997). If EQ really tells us something about intelli- Because EQs are calculated on the basis gence or general behavioral complexity, what Pongids: of empirical estimates of brain/body-scaling are we to make of the large whales, who have larger-bodied apes, relationships, they are sensitive to the partic- the lowest EQs of all mammals [e.g., hump- part of the taxonomic ular sample used to derive a and c parame- back whales (Megaptera nodosa) have EQs superfamily ters. Jerison (1973) originally estimated the of 0.18 (Schoenemann 1997)]? Humpback Hominoidea, which include common and scaling parameter a (i.e., slope) for mammals whales display a variety of complex behaviors, ∼ bonobo as 0.67, but Martin (1981) estimated it to including structured vocal sequences (songs?) chimpanzees, be 0.76 using a larger sample. Using Jerison’s that last 5–25 min before repeating, and com- gorillas, and (1973) equation, human EQs are ∼7, whereas plex feeding techniques, including the use of orangutans Martin’s (1981) equation gives the values at bubble clouds to encircle prey (Rendell et al. ∼5. Regardless of the slope estimate used, 2001). however, humans consistently have the high- Other species comparisons further high- est values among mammals. light the problem: Guinea pigs (Cavia cut- Figure 1 shows brain/body-size relation- ler) have significantly higher EQs (0.95) than ships for a sample of 52 primate species and do elephants (Loxodonta africana, 0.63). This illustrates different scaling estimates for sep- is true even though guinea pig brains weigh arate primate subtaxa. Primates as a group only ∼3.3 g, whereas elephant brains can tend to have larger brains than the av- weigh over 5700 g (Schoenemann 1997). If erage mammal, with EQs for anthropoids EQ really tells us something important about (all primates excluding prosimians) averag- behavior, this should be evident in a com- ing ∼2 (i.e., anthropoids have brains ap- parison of guinea pig versus elephant be- proximately twice the size of the average havior, yet this does not appear to be the mammal of their body size). Even though case. If anything, given the variety of com- absolute brain size is significantly larger plex social behaviors known in elephants (e.g., in pongids (chimpanzee, bonobo, gorilla, McComb et al. 2001), absolute brain size orangutan) than in all other anthropoids ex- appears more behaviorally relevant in this cept humans, they do not have substantially comparison. larger EQs, indicating their brains are scal- In fact, a number of studies suggest that— ing approximately similar to other anthro- for some behavioral domains—absolute brain poids. Human brain sizes, by contrast, are size is more relevant than EQ. This is true for not explained by brain/body scaling in either measures of the ease of learning abstract rules mammals or primates. as opposed to simple associations (Rumbaugh Although EQs are superficially appeal- et al. 1996), as well as the speed of learning ing as a measure of comparative brain size, object-discrimination tasks (Riddell & Corl by UNIVERSITY OF PENNSYLVANIA LIBRARY on 09/21/06. For personal use only. Annu. Rev. Anthropol. 2006.35:379-406. Downloaded from arjournals.annualreviews.org it is unclear exactly how to interpret EQ 1977). In addition, although relative brain size differences between species. The behavioral is often emphasized in brain/behavior studies, relevance of EQ has long been questioned associations are invariably also significant if (Holloway 1966), yet it is often incorrectly absolute brain volumes are used (e.g., Dunbar assumed that it must be the most behav- 1995, Reader & Laland 2002). Jerison (1973) iorally relevant variable of brain size—as if recognized this when he suggested an alter- it were some coarse estimate of intelligence native to EQ: an estimate of extra neurons, or other behavioral ability (e.g., Kappelman which is the absolute amount of neural tis- 1996). Others have uncritically assumed that sue beyond that predicted empirically by body increases in absolute brain size may not be mass (e.g., two species with identical EQs but meaningful if EQs remain the same (e.g., different body masses also differ in number Wood & Collard 1999, Wynn 2002).
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