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Human Frontal Lobes Are Not Relatively Large Human frontal lobes are not relatively large Robert A. Bartona,1 and Chris Vendittib aEvolutionary Anthropology Research Group, Department of Anthropology, Durham University, Durham DH1 3LE, United Kingdom; and bSchool of Biological Sciences, University of Reading, Reading RG6 6AS, United Kingdom Edited by Katerina Semendeferi, University of California, San Diego, La Jolla, CA, and accepted by the Editorial Board March 12, 2013 (received for review September 10, 2012) One of the most pervasive assumptions about human brain evolu- logged—volumes) (3–5, 7). These measures suggest that human tion is that it involved relative enlargement of the frontal lobes. We frontal cortices are larger as a proportion of total brain size than show that this assumption is without foundation. Analysis of five in other species. However, proportional size differences conflate independent data sets using correctly scaled measures and phylo- selective enlargement with allometric scaling. Volumes of dif- genetic methods reveals that the size of human frontal lobes, and of ferent brain structures change at different rates as brain and body specific frontal regions, is as expected relative to the size of other size evolve (14, 15), and with different implications for variables brain structures. Recent claims for relative enlargement of human more directly related to information processing than volume, such frontal white matter volume, and for relative enlargement shared by as numbers of neurons and synapses (16). For example, the vol- all great apes, seem to be mistaken. Furthermore, using a recently ume of the whole neocortex increases with brain size more rapidly developed method for detecting shifts in evolutionary rates, we find than does the volume of the cerebellum (15), but neuron density that the rate of change in relative frontal cortex volume along the declines more rapidly in the neocortex, so that despite the volu- phylogenetic branch leading to humans was unremarkable and that metric ballooning of the neocortex as overall brain size increases, other branches showed significantly faster rates of change. Al- the proportion of the brain’s neurons in each of the two structures though absolute and proportional frontal region size increased remains approximately constant (16). Volumetric ratios or pro- rapidly in humans, this change was tightly correlated with corre- portions therefore progressively overestimate the contribution of sponding size increases in other areas and whole brain size, and with the neocortex to neuron numbers as brain size increases. decreases in frontal neuron densities. The search for the neural basis The ballooning of cortical volume as brain size increases seems of human cognitive uniqueness should therefore focus less on the to be due largely to allometric constraints on connectivity, because frontal lobes in isolation and more on distributed neural networks. cortical white matter volume increases substantially faster than gray matter volume (12, 15, 17, 18), and explains the positive al- prefrontal cortex | cognition | primates lometry of neocortex size (15). This allometry is especially marked for frontal regions (8, 9, 11, 19). Although allometric scaling lthough it is widely assumed that human brain evolution among brain structures is an interesting issue in its own right and Ainvolved relative expansion of the frontal lobes, no clear probably reflects the way that functional properties such as con- picture has emerged from comparative studies. Early claims (1, nectivity and neural processing speed are conserved across body 2) have been both cited as evidence for relative expansion (3, 4) and brain sizes (17, 18), it would be illogical to conclude from the and questioned owing to small sample sizes and uncertainty observation that human values are closely predicted from a gen- about anatomical boundaries defined using older methods (5, 6). eral scaling relationship for other species that humans are spe- Newer and larger data sets have not yet resolved these uncer- cialized for frontal lobe functions in particular (as opposed to tainties but have been used as support for the claim of dispro- functions mediated by more distributed networks connecting portionate expansion of frontal lobe structures and specific tissue different brain regions). types (4, 6–10), for the lack of thereof (5, 10, 11), or have given In addition to this theoretical point, unscaled measures of ambiguous results depending on factors such as which species are frontal cortex size give problematic empirical results when the EVOLUTION included in the analysis (12). In addition, there is variability comparative net is cast widely. For example, frontal gray matter among these studies as to whether and which other ape species volume is smaller as a proportion of total cortical volume in are reported to exhibit similar relative expansion as humans (5, 6, humans than in several nonhuman prosimian and anthropoid 9). Finally, among those studies reporting larger than expected primates and two mustelid carnivores, and values for several values for humans and/or other apes, there is little consistency in prosimians exceed those for chimpanzees (Pan troglodytes), spi- terms of which measures show differences, with claims based der monkeys (Ateles), and baboons (Papio hamadryas)(calcu- variously on whole frontal cortex volume (5), volume of pre- lated from table 2 in ref. 11). In terms of absolute size, human frontal area 10 (7), prefrontal vs. nonprefrontal white matter frontal cortex exceeds that in other measured species; but sea volume (6), and left (but not right) prefrontal white matter vol- lions (Zalophus californicus)—which have not been noted for ume relative to prefrontal gray matter volume (9). intelligence—exceed several anthropoids, including baboons (P. Resolving this confused picture is of considerable importance hamadryas) and gibbons (Hylobates lar), whereas llamas (Llama to understanding the neural basis of human cognitive evolution. glama) exceed macaque monkeys (Macaca mulatta) (11). Hence, As Rilling (4) states, “In the field of comparative primate neu- unless one is willing to take seriously the hypothesis that lemurs roanatomy, perhaps no question has engendered more interest have more of the qualities bestowed by frontal cortices than do than whether the human frontal lobes are larger than expected humans, or that llamas possess more than monkeys, it must be for a primate of our brain size.” Yet the strongest justifiable concluded that testing the hypothesis that any species is statement that could be made in a recent review was, “It can be tentatively concluded that it is questionable that the size of the prefrontal cortex can account for the human executive Author contributions: R.A.B. and C.V. designed research; R.A.B. and C.V. performed re- functions” (13). search; R.A.B. and C.V. analyzed data; and R.A.B. and C.V. wrote the paper. One reason for ambiguity in the literature is the use of dif- The authors declare no conflict of interest. ferent types of measure that give different results. Claims about This article is a PNAS Direct Submission. K.S. is a guest editor invited by the Editorial Board. frontal lobe evolution in humans are sometimes based on un- 1To whom correspondence should be addressed. E-mail: [email protected]. scaled measures (such as absolute size or percentage of brain This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. volume comprising frontal areas or plots of raw—rather than 1073/pnas.1215723110/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1215723110 PNAS | May 28, 2013 | vol. 110 | no. 22 | 9001–9006 Downloaded by guest on September 27, 2021 specialized for frontal cortex functions, as opposed to functions alternative explanations for the patterns previously reported. We mediated by more extended networks, requires scaling to be also present analyses to determine whether there were statisti- taken into account. Here we test the hypothesis that human cally significant shifts in the rate of size change along the phy- frontal cortex and prefrontal cortex (PFC) size is larger than logenetic branch leading to humans. The issue of which of the expected from scaling against other brain structures, an empirical various anatomical demarcation criteria used in previous studies issue that is still contested (4, 6, 8–10). are most appropriate is important and is addressed in Discussion; There has also been variability in whether and how comparative however, our main concern is to determine which of the claims analyses take account of phylogeny. Some studies have treated based on these data are empirically supportable and whether any species values (or even multiple intraspecific values) as in- consistent pattern across data sets emerges. dependent data points (3, 5–8, 10). It is now well established that species values cannot be assumed to be independent, because Results species share similarities due to common descent as well as to Phylogenetically determined (PGLS) coefficients, r2 values, and independent evolution. Such phylogenetic nonindependence can estimates of the phylogenetic signal in the data (λ values) for the substantially bias estimates of scaling parameters and the mea- relationship between frontal and nonfrontal structures in non- sures of relative size based on them (20, 21). This problem affects human species are presented in Table S1. In Fig. 1 the phylo- both the prediction of human from nonhuman values and claims genetic regression lines for nonhuman species are mapped back of different scaling relationships in different taxa (8, 10, 11). Two onto species values, with humans and 95% confidence intervals notable exceptions are a study of frontal cortex scaling in mam- included. In all four data sets in Fig. 1, the size of frontal cortices mals using the method of phylogenetically independent contrasts in humans is within the 95% confidence limits for the size pre- (11), and recent studies by Smaers and colleagues using a more dicted from the size of other brain regions. This applies to both general phylogenetic method than independent contrasts, phy- the whole human frontal cortex (Fig.
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