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Ann. N.Y. Acad. Sci. ISSN 0077-8923

A N N AL S O F T H E N E W Y O R K A C A DE M Y O F S C I EN C E SIssue: Resources and Technological Advances for Studies of Neurobehavioral Evolution

The human brain: rewired and running hotTodd M. Preuss

Division of Neuropathology and Neurodegenerative Diseases and Center for Translational Social Neuroscience, YerkesNational Primate Research Center, Emory University, Atlanta, Georgia; Department of Pathology, Emory University School ofMedicine, Atlanta, Georgia

Address for correspondence: Todd M. Preuss, Ph.D., Yerkes National Primate Research Center, Emory University, 954Gatewood Road, Atlanta, GA 30329. [email protected]

The past two decades have witnessed tremendous advances in noninvasive and postmortem neuroscientic tech-niques, advances that have made it possible, for the rst time, to compare in detail the organization of the human

brain to that of other primates. Studies comparing humans to chimpanzees and other great apes reveal that human brain evolution was not merely a matter of enlargement, but involved changes at all levels of organization that have been examined.These include thecellular and laminar organization of cortical areas; thehigherorder organization of the cortex, as reected in the expansion of association cortex (in absolute terms, as well as relative to primary areas);the distribution of long-distance cortical connections; and hemispheric asymmetry. Additionally, genetic differences between humansandother primates haveproven to be more extensive than previously thought, raising thepossibilitythat human brain evolution involved signicant modications of neurophysiology and cerebral energy metabolism.

Keywords: hominid; evolution; neuroimaging; genomics; cerebral metabolism

Introduction

Until quite recently, it has been impossible for neu-roscientiststoaddress inmuch detailone of themostfundamental questions in the life scienceshow dohumanbrainsdiffer from those of other animals? Allweve known for sure is that human brains are freak-ishly large for a mammal of our body size. In mostmammals, the portion of the skull devoted to eatingis bigger than the part that houses the equipmentfor thinking, whereas the human brain box dwarfsthemachinery of mastication.Butwhats in thebox?Whats in there that gives us the ability to think andact in specically human-like ways? The allure of neuroscience surely depends on the conviction thattheres something unusual about the human brain, yet neuroscientists have been unable to specify howthe cells and the systems of connections that makeup the brain were modied in human evolution.

The main reason for this failure is that neurosci-entists have lacked the technical means to explore

the human brain in anything like the detail withwhich they are able to study nonhuman species. Fornonhuman species, we have had a range of powerful

investigative techniques available to us, such as in- jecting chemicals into brain tissue to trace neuronalconnections, a procedure considered unethical inhumans. Such invasive techniques, it is importantto note, are also out of bounds for studying rareand endangered species, such as chimpanzees, theanimals most closely related to humans. Withoutthe ability to compare humans to chimpanzees andother great apes, we can say little about whats dis-tinctively human about human brains.

Over the past 20 years, however, and particu-larly over the last decade, the means available forstudying human brains, and for directly compar-ing humans to chimpanzees and other primates,have improved enormously. Of course, the contin-ual renement of noninvasive imaging techniques,and their application to nonhuman primates aswell as to humans, has been very important. Mag-netic resonance imaging (MRI) and positron emis-sion tomography (PET) are the imaging techniquesthat have garnered the most attention, but per-

haps the most important development in this areafor students of human brain evolution is the in-troduction of diffusion-tensor imaging (DTI) and

doi: 10.1111/j.1749-6632.2011.06001.xE182 Ann. N.Y. Acad. Sci. 1225 S1 (2011) E182E191 c 2011 New York Academy of Sciences.


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Preuss The human brain: rewired and running hot

related techniques that can be used to trackwhite-matterpathwaysbetweengray-matter regionsnoninvasively (for a recent review, see Ref. 1).Comparedto conventionaltract-tracing techniques,which involve making injections of chemical trac-ers into the brains of experimental animals, DTIhas certain limitations: its resolution is relatively coarse, because under most circumstances it cannottrack bers into the gray matter, and it cannot dis-tinguish between anterograde and retrograde con-nections. Yet DTI has made it possible to study themajor ber systems in human brains comprehen-sively and also to compare human ber systems tothose of other primates. Far less eye-catching, butnonetheless enormously important, has been the

steadily increasing power of histological techniquesfor exploring the structure of tissue acquired post-mortem, reecting the proliferation of antibodiesand other ligands available for probing the distri-bution of molecules in the brain. Older histologicaland histochemical techniques remain very useful,however. The value of all these techniques, and thevalue of the postmortem tissue to which they canbe applied, has been multiplied by the introductionof antifreeze storage solutions that preserve tissuefor years in a state suitable for immunohistochem-istry and in situ hybridization, avoiding the degrad-ing effects of overxation. 2 A third source of newinformation about human brain evolution comesfrom genomics and comparative molecular biology,including techniques for identifying genes that un-derwent positive selection or expression changes inhuman evolution.

The upshot of these technical innovations is thatthe subject of human brain evolution, long some-thing of a scientic backwater, has become a matter

of keen interest, as reected by a spate of recentbooks (e.g., Refs. 37). Different authors will, of course, have different takes on this subject. Here, Icast my account of current results in the light of hy-potheses and expectations about human brain spe-cializations that were posited before the advent of the new techniques just discussed.

Issues and evidence

Was encephalization accompanied by the expansion of association cortex? There is no question that human brains are much,much larger than would be expected for a primateof our body size, and that most of this difference

reects an enlargement of the neocortex. Classi-cally, it has been supposed that this enlargementresulted from a selective expansion of the higherorder association cortex of the frontal, temporal,and parietal lobes, relative to the primary sensory and motor areas (see, e.g., Refs. 811). With the ap-plication of structural neuroimaging techniques tothe study of human brain evolution, this conclu-sion has been called into question. 12 The essenceof the counterclaim is that association cortexandprefrontal cortex, in particularis no larger in hu-mans than would be expected for an ape with ahuman-sized brain. More specically, the claim isthat if one were to plot the size of prefrontal cor-tex as a function of the size of the rest of the brain

for anthropoid primates, human prefrontal cortexwould fall within the expected size range. One cantake issue with the methods employed by those whohave adopted this view, for they have not measuredprefrontal cortex sizedirectly(something thatis cur-rently not possible to do using imaging techniques),and have instead measured a morphological proxy for prefrontal cortexthe size of the entire frontallobe or the size of the frontal cortex anterior to theprecentral gyrus. Moreover, other authorities haveafrmed the traditional view of association cortexexpansion (e.g., Refs. 13 and 14).

Nevertheless, even if one grants for the sake of argument that humans have the expected amountof prefrontal cortex for a primate brain scaled up tohuman size, there is no getting past the fact that hu-mans have a lot more association cortex in absoluteterms than do chimpanzees or other great apes. 15

Human brains are about three times the volumeof those of chimpanzees, and whereas the primary sensory and motor regions of humans are, in ab-

solute terms, very similar in size to those of apes,humans have a much, much greater amount of as-sociationcortex (Tables1 and2). 15 Thesamepatternholdsforthe sensoryandassociationthalamicnuclei(Table 3). I suggest that the most straightforwardinterpretation of the data is that the primary ar-eas maintained approximately ape-like sizes in hu-man evolution, while association cortex underwentenormous expansion. The mere fact that the mag-nitude of association cortex expansion is (or mightbe) in line with what is expected from brain-sizescaling might be taken to mean that association cor-tex expanded in a predictable manner (perhaps re-ecting some conserved developmental processes),

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The human brain: rewired and running hot Preuss

Table 1. Absolute and relative sizes of primary motor area (area 4), prefrontal cortex, and other cortex in great apesand humans

Area 4 (cm2) Prefrontal (cm 2) Other cortex (cm 2)

Human 7.34 (65%) 181.40 (220%) 499.60 (149%)Great apes Chimp 8.94 (79%) 52.84 (87%) 280.96 (84%)Orang 13.57 (121%) 68.45 (113%) 389.22 (116%)

Data from Blinkov and Glezer, 8 Table 196. Values in parentheses represent species values expressed as a percentage of the mean value of great apes (i.e., mean of chimpanzee and orangutan).

but it doesnt negate the fact that association cor-tex did expand. The result is that humans have abrain dominated by association cortex to an ex-tent unmatched by any other primate, and this dif-ference is likely to have profound implications forthe internal organization of the cortex, 6, 18 for pat-terns of long cortical connections, 19 and for corticalfunction.

Was the expansion of association cortex accompanied by the addition of new,human-specic areas to support human-specic functions? This question has long been a matter of contention,

with notable authorities lining up on both sides of the issue. To some, it has seemed that the enor-mous human brain, with its unique psychologicalfunctions, must contain human-specic areas. 9, 20, 21

Others, however, have failed to be convinced, argu-ing that humans have the same set of cortical areasfound in our close primate relatives. 11 , 22, 23

This important issueremainsunresolved. It needsto be acknowledged, however, that at present, thereis no compelling evidence that humans possessmore cortical areas than do other primates, nor thathuman-specic functions require human-specicbrain structures. The paradigmatic language areasof Broca and Wernicke provide a case in point. Al-though there is little doubt that in humans theseareas are critically involved in language processingand that language is a human specialization, thereis nonetheless evidence that homologues of Brocasand Wernickes areas exist in apes and monkeys,based on similarities in their location withinthecor-tical mantle, in their histology, and in their other,

nonlinguistic functions, such as forelimb and oro-facial movements and activation by species-speciccalls (see reviews in Refs. 24 and 25). Thus, the claim

that Brocas and Wernickes area evolved originally to support functions other than language, and thenwere recruited into a language-processing system(an old claim, in fact; see Ref. 26), is defensible, andwe should not conclude that human-specic func-tions require human-specic brain areas (see alsoRefs. 27 and 28).

Mapping studies of other brain regions also tendto identify a common complement of areas in hu-mans and nonhuman primates. For example, if thecytoarchitectonic maps of Petrides and Pandya 29

are correct, each of the prefrontal areas of humanshas a homologue in macaque monkeys, despite themuch larger prefrontal region of humans. Similarly,

mapping studies of extrastriate visual cortex usingfMRI in humans and macaques identify an identicalcomplement of visual areas, 30 despite the expan-sion of extrastriate cortex relative to striate cortex inhumans.

Recently, areas have been identied in humanparietal cortex that have functional properties notfound in monkeys. The human intraparietal sul-cus (IPS) contains areas that are strongly acti-vated whenviewingthree-dimensional shape-from-motion stimuli; the same stimuli produce minimal

activation in macaque IPS. 31 Ingeneral, IPSareasaremuch moreresponsiveto motion in humans than inmacaques. 32 Similarly,humanspossessanareaintheleft anterior inferior parietal lobule (i.e., the supra-marginal gyrus; area PF or 7b) that is more strongly activated when human subjects view videos depict-ing tools being used to grasp or otherwise manipu-late objects than when hands are viewed perform-ing the same actions. 33 A comparable, tool-selectiveenhancement was not seen in the anterior inferiorparietal lobule of macaques, even in macaques withextensivetraining in tool use. It ispossible,then,thathumans possess new motion-selective and tool-use

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Table 3. Absolute and relative numbers of neurons in thalamic nuclei in humans and great apes

Sensory and motor

Visual Auditory Somato-sensory Motor/PremotorLGB MGBp VB VL

Human 2.07 (102%) 0.87 (107%) 1.69 (147%) 3.31 (165%)Great apes Chimp 2.17 (107%) 0.91 (113%) 1.23 (107%) 2.06 (103%)

Gorilla 1.88 (93%) 0.71 (87%) 1.07 (93%) 1.84 (97%)

Association and limbic

MD PUL LD AP

Human 7.57 (312%) 10.11 (202%) 0.41 (272%) 1.19 (309%)Great apes Chimp 2.50 (103%) 5.45 (109%) 0.15 (99%) 0.39 (100%)

Gorilla 2.35 (97%) 4.56 (91%) 0.15 (101%) 0.38 (100%)

Notes: Data from Armstrong. 17 Values represent the numbers of neurons 106; values in parentheses represent speciesvalues expressed as a percentage of the mean value of great apes (i.e., mean of chimpanzee and gorilla).LGB, lateral geniculate body; MGBp, principal nucleus of the medial geniculate body; VB, ventrobasal nucleus; VL,ventral lateral nucleus; MD, mediodorsal nucleus; PUL, pulvinar-lateral posterior complex; LD, lateral dorsal nucleus;AP, anterior principal nucleus.

territory that occupies the planum temporale and isoften identied with Wernickes area, with humans

having more neuropil space between cell columnson the left than on the right; by contrast, no asym-metry wasfound in chimpanzeesor macaques.Sim-ilar asymmetries, with higher neuropil fractions onthe left than the right, are found in human motorand visual cortex (e.g., Refs. 52 and 53), however.This raises the possibility that the Tpt asymmetry reects a human-specic, cortex-wide asymmetry 54

that is not specically related to language.The advent of DTI has opened up new dimen-

sions of organization for the analysis of asym-metries. One measure derived from DTI is thefractional anisotropy (FA) of brain voxels. FA is ameasure of the propensity of water to diffuse di-rectionally rather than randomly; differences in FAare thought to reect differences in the microstruc-ture of white matterfor example, the amount of myelin and the coherence of bers. One can com-pare the FA of specic bers tracts between hemi-spheres and across species. In a recent report, Liet al .55 found that the corticospinal tracts of chim-

panzees showed higher FA on the left than onthe right, consistent with reports from humans.Work in progress,however, suggests thatother tracts

show marked differences between humans, chim-panzees, and macaques. For example, humans ex-

hibit higher FA on the left than the right in thearcuate fasciculus (the tract that carries bers be-tween Wernickes and Brocas areas), and the mag-nitude of asymmetry is greater in humans than inchimpanzees. 56

Was long-distance cortical connectivity modied in human brain evolution? Cortical areas have extensive systems of long-distance connections; these connections link func-tionally related areas and link the cortex to sen-sory and motor structures in the thalamus andbrainstem. Prior to the development of robustmethods to study ber tracts noninvasively, fewneuroscientists entertained the possibility that long-distance connectivity might differ in important re-spects between humans and other primates; Crickand Jones 20 and Deacon 19 are conspicuous excep-tions. The only widely cited human specializationof connectivity came from evidence that humans,and not other primates, have direct cortical pro-

jections to brainstem nuclei involved in orofacialmotor control, a projection thought to be related tolanguageevolution. 57, 58 Thisevidence,however, was



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obtained using silver staining for degenerating ax-ons, a technique not considered to be very sensitiveor reliable by modern standards.

The recent development of DTI and relatedin vivo ber-tracking techniques makes possiblesystematic comparisons of human and nonhu-man primate connectivity (Fig. 1). The rst suchstudy demonstrated differences in the composi-tion of the arcuate fasciculus in humans, chimps,and macaques. 36 In humans, but not the otherprimates, the arcuate fasciculus carries not only bers that interconnect Brocas area (in the pos-terior inferior frontal gyrus) and Wernickes area(in the posterior superior temporal gyrus), butalso bers traveling between the inferior frontal

lobe and areas in the middle and inferior tem-poral lobe that are known to represent wordmeanings.

Was the microstructure of cortical gray matter modied in human evolution? Until recently, few would have taken seriously thepossibility that cortical microstructure underwentimportant changes in human evolution. Accordingto the doctrine of basic uniformity developed inthe 1970s, the cortex of all mammals was thoughtto be composed of cell columns that were essen-tially unvarying across species in their cell number,cell types, laminar distribution of afferents and ef-ferents, and intrinsic connectivity (see the reviewsin Refs. 59 and 60). In this view, there is littleroom for human specializations at these levels of organization. While basic uniformity has enjoyedtremendous popularity, however, it simply cannotbe squared with evidence from moderncomparativestudies that highlights the diversity of microstruc-

tural organization across mammalian species (re-viewed in Refs. 59 and 60). At present, few studieshave rigorouslycomparedhuman microstructure tothat of other primates. One area that has been stud-ied in some detail, however, is the primary visualarea (area V1; Brodmanns area 17; striate cortex),and this area exhibits a number of human special-izations, particularly in the organization of layer4A.6163 The pattern of differences suggests modi-cations related to motion processing, changes thatmayunderlie thehumanmacaquedifferences in theextrastriate and parietal motion-sensitive areas dis-cussed earlier. Additional specializations of humancortex that have been documented include modi-

cations of neuronal and glial phenotypes, 6467 thehorizontal spacing of neurons, 68 and modicationsof the laminar organization of afferents. 6971

Do human phenotypic specializations result from only a few genetic changes? Since at least the mid-1970s, it has been under-stood that the amino-acid sequences of proteins,and the nucleotide sequences of the genes thatcode for them, are very similar in humans andchimpanzeeson the order of 9899% similar. 72

The magnitude of similarity prompted King andWilson 72 to conclude that evolutionary changesin gene expression, rather than changes in genesequences, are the principal source of human phe-

notypic specializations. Gould73

popularized thisidea, and emphasized the possibility that a smallnumber of expression changes acting early in de-velopment could have profound phenotypic conse-quences. Given this background, and the fact thatthere arefew widely acknowledged specializationsof thehuman brainandcognitionotherthanencephal-ization and language, it is not surprising that whenimproved means to identify human genetic special-izations became available, attention was focused ongenes believed to be related to encephalization andlanguage.7476 The FOXP2 gene has been especially appealing in this regard, as mutations of the generesult in language and cognitive decits, 77 it under-went positive selection in the human lineage, 74 andit codes for a transcription factor that regulates theexpression of numerous brain-expressed genes. 78, 79

I certainly dont disparage the search for genesrelated to language or brain size, yet I fear that infocusing on these weve missed an important les-son of recent genomics research, specically, that

the genetic differences between humans and otherprimates are much more extensive than generally supposed. 60 While the protein-coding sequences of humansandchimpanzeesare thesame atabout98%of nucleotides, the overall DNA sequence similar-ity is more like 9596%.80, 81 There are hundreds of genes, at least, that are differentially expressed in thebrains of human and chimpanzees. 82, 83 There arealso hundreds of genes, at least, that were targets of positive selection in the human lineage subsequentto the humanchimpanzee divergence. 84 Gene du-plications, deletions, and insertions were commonin the human lineage, 8587 in some instances result-ing in the evolution of new genes and gene families



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Figure 1. Summary of results from a DTI study by Rilling et al.36 comparing the organization of the arcuate fasciculus, a white-matter bundle conveying bers between the frontal lobe and posterior cortex, in humans ( Homo sapiens ) and chimpanzees ( Pan

troglodytes ). In both species, the arcuate fasciculus (AF) carries bers between frontal language cortex, including areas 44, 45, and47 (Brocas area), and posterior language cortex, including area 22 (Wernickes area) and the inferior parietal lobule (areas 40 and39). In humans, however, the AF carries bers from middle temporal cortex (area 21) that represent word meanings. Fibers alsopass between the temporal and frontal lobes via a ventral pathway (V), which is relatively prominent in chimpanzees and macaques(not shown).

(e.g., Refs. 88 and 89). There is also evidence of evo-lutionary changes in human protein chemistry notpredicted by differences in genes (e.g., Ref. 90).

Comparisons of humans and nonhuman pri-mates have, in short, yielded an embarrassment of

molecular richesembarrassing, because we cur-rently know a lot more about human genetic spe-cializations than we do about phenotypic special-izations of the human mind and brain. Perhaps weshould start thinking about genetics differently, andinstead of focusing quite so much on identifyinggenes that inuence known phenotypic specializa-tions, use our knowledge of the genes to help usdiscover previouslyunknown human phenotypes. 83

Consider, for example, that we have genomic ev-idence suggesting that humans modied the ex-pression and structure of genes related to synapseformation 91, 92 and aerobic energy metabolism. 9395

This suggests that human brains evolved so as tosupport higher levels of neural activity and plas-ticity than the brains of our closest relatives. Intu-itively, this may seem unsurprising, but one wouldbe hard pressed to identify a clear scientic claim fora human specialization of this kind, backed up by comparative phenotypic data. Such data may not beentirely lacking, however. While there are few mod-

ern data comparing brain metabolic rates betweenhumans and nonhuman primates, those data thathave been published from PET studies suggest that

humanbrainsin theawake statehaveratesof glucoseconsumption per unit of cortical tissue that are ap-proximately equal in absolute terms to those of OldWorld monkeys in the awake state (e.g., Refs. 96 and97). That shouldnt beit is a well-established prin-

ciple of physiology (Kleibers law) that larger organsand organisms tend to use less energy per unit of tissue than do smaller ones. On this basis, we wouldexpect the enormous brain of Homo sapiens , whileusing far more energy overall than that of apes andmonkeys, to use less energy per gram of tissue. Butthe current evidence suggests this is not the case,and that human brains are running hot. 91 If true,this would likely have profound consequences forhuman psychology, neurophysiology, disease, andlife history.

Conclusions

Neuroscientists are now in possession of powerful,noninvasive techniques for understanding the phys-ical basis of the human mind. More than that, wecan now determine what the human brain shareswith that of other species, as well as what is dis-tinctively humanthat is, what we have evolvedsince our lineage parted ways with the lineage lead-

ing to our great-ape relatives. What is novel aboutthis research, however, is not only the noninva-sive methods employed, but also the strategy of



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comparative investigation. As valuable as studies of model species unquestionably are, if we want tounderstand how humans resemble and differ fromother species, there is no substitute for studies thatdirectly compare humans to other primates, and es-pecially to our closest relatives, the chimpanzees.

Acknowledgments

The author would like to thank the organizers fortheir invitation to participate in the symposium,Chet Sherwood and Emmanuel Gilessen for sharingtheir views on some of the issues discussed here, andKatherine Bryant, Nicole Taylor, Mary Ann Cree,and Carolyn Suwyn for reviewing earlier drafts of the manuscript. The authors research is supported

by the Yerkes base grant (NIH RR-00165).Conicts of interest

The author declares no conicts of interest.

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