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NRVS 00022 a0005 4.21 The Evolution of Neuron Types and Cortical Histology in Apes and Humans C C Sherwood, Kent State University, Kent, OH, USA P R Hof, Mount Sinai School of Medicine, New York, NY, USA ª 2007 Elsevier Inc. All rights reserved. 4.21.1 Introduction 2 4.21.1.1 Evolutionary History of the Hominoids 2 4.21.1.2 History of Studies Concerning Hominoid Cortical Histology 3 4.21.2 Comparative Anatomy of the Cerebral Cortex 4 4.21.2.1 Topology of Cortical Maps 4 4.21.2.2 Architecture of the Cortex 4 4.21.2.3 Primary Visual Cortex 5 4.21.2.4 Auditory Cortex 8 4.21.2.5 Primary Motor Cortex 10 4.21.2.6 Inferior Frontal Cortex PROOF 12 4.21.2.7 Prefrontal Cortex 13 4.21.2.8 Anterior Cingulate Cortex 14 4.21.3 Patterns of Cortical Organization in Hominoids 15 4.21.3.1 The Emergence of Cell Types and their Distribution 15 4.21.3.2 The Evolution of Cortical Asymmetries 15 4.21.3.3 How much Variation in Cortical Architecture can be Attributed to Scaling versus Specialization? 17 4.21.3.4 Genomic Data Provide Insights into Cortical Specializations 18 4.21.3.5 On the Horizon 19 FIRST Glossary the structure in question becomes proportionally smaller or less g0005 Allometry Many biological traits scale with numerous with increases in the overall size in a nonlinear fashion. size of the reference variable. Such allometric scaling relation- Chemoarchitecture The microanatomical organization g0010 ships can be expressed by the of the cerebral cortex revealed by power function:ERY¼bXa. The loga- staining for biochemical substances rithmic transformation of the using techniques such as immuno- allometric scaling equation yields: histochemistry and enzyme or log Y¼log bþa log X. The expo- lectin histochemistry. nent of the power function becomes Dysgranular A type of cortex that has a weakly g0015 the slope of the log-transformed Cortex defined layer IV because it is vari- function. The slope of this line can able in thickness. At points, layer then be interpreted in terms of a IV seems to disappear because neu- biological scaling relationship rons from layers IIIc and Va between the independent and intermingle. dependent variable. Positive allo- Encephalization A relative measure of a species’s g0020 metry refers to a scaling brain size that represents the degree relationship with an exponent that to which it is larger or smaller than ELSEVIis greater than 1, which means that expected for a typical animal of its the structure in question grows dis- body size. proportionately larger or more Granular Cortex A type of cortex that has a clearly g0025 numerous with increases in the identifiable layer IV. size of the reference variable. Grey Level Index The proportion of an area of refer- g0030 Negative allometry refers to a scal- (GLI) ence that is occupied by the ing relationship with an exponent projected profiles of all Nissl- that is less than 1, which means that stained elements. This value NRVS 00022 2 The Evolution of Neuron Types and Cortical Histology in Apes and Humans provides an estimate of the fraction 4.21.1 Introduction s0005 of tissue that contains neuronal 4.21.1.1 Evolutionary History of the Hominoids s0010 somata, glial cell nuclei, and endothelial nuclei versus neuropil. Apes and humans are members of the primate super- p0005 GLI values are highly correlated family Hominoidea (Figure 1). Molecular evidence with the volume density occupied indicates that the hominoid lineage split from the b0860 by neurons since glial and endothe- Old World monkeys about 25Ma (Wildman et al., lial cell nuclei contribute only a 2003). The extant representatives of this phylogenetic very small proportion of the total group include two families. The Hylobatidae com- volume. prises gibbons and siamangs, and the Hominidae g0035 Hominoid A phylogenetic clade that includes includes great apes (i.e., orang-utans, gorillas, chim- lesser apes (gibbons and siamangs), b0300 great apes (orang-utans, gorillas, panzees, and bonobos) and humans (Groves, 2001). chimpanzees, and bonobos), and Living hominoids are distinguished by a suite of humans. shared derived traits that point to the key adaptations g0040 Infragranular Cortical layers that are deep to of this clade. These characters include lack of an Layers granular layer IV, i.e., layers V external tail, modifications of the shoulder girdle and and VI. wrist for greater mobility, and stabilization of the b0075 g0045 Minicolumn Morphologically, minicolumns lower back (Begun, 2003). These adaptations allow appear as a single vertical row of hominoids to exploit resources in small branches of neurons with strong vertical inter- trees by developingPROOF suspensory postures to distribute connections among layers, forming their body weight. This form of locomotion may have a fundamental structural and func- tional unit. The core region of the been particularly important in allowing certain species column contains the majority of the to increase body size. In addition, compared to other primates, hominoids have extended periods of growth neurons, their apical dendrites, and b0675 and development (Schultz, 1969), an increased com- both myelinated and unmyelinated b0570 fibers. A cell-poor region, contain- plexity of social interactions (Potts, 2004), and larger ing dendritic arbors, unmyelinated brains than would be expected for a monkey of the b0630 axons, and synapses, surrounds same body size (Rilling and Insel, 1999). The each column. increased encephalization and associated life history g0050 Neuropil The unstained portionFIRST of elongation of these species suggest that cognitive flex- Nissl-stained tissue, which is com- ibility and learning were important aspects of the prised of dendrites, axons, and hominoid adaptive complex, which allowed them to synapses. g0055 Supragranular Cortical layers that are superficial deal with locating ephemeral resources from fruiting trees and to negotiate more complicated relationships Layers to granular layer IV, i.e., layers I, II, b0570 and III. ER in fission–fusion societies (Potts, 2004). Humans 6 Ma 3 Ma Bonobos 7 Ma Chimpanzees 14 Ma Gorillas 18 Ma Orang-utans 25 Ma Gibbons and simiangs 40 Ma ELSEVI Old World monkeys 58 Ma New World monkeys 63 Ma Tarsiers Lemurs and lorises Figure 1 Cladogram showing the phylogenetic relationships of living hominoids and other primates. Estimated divergence dates f0005 b0295 are taken from Goodman et al. (2005). NRVS 00022 The Evolution of Neuron Types and Cortical Histology in Apes and Humans 3 p0010 Although only a small number of hominoid spe- pathological changes subsequent to ablation, some cies persist today, the fossil record reveals a diverse studies also examined cortical projection systems in b0835 b0470 array of successive adaptive radiations of hominoids apes (Walker, 1938; Lassek and Wheatley, 1945; b0460 b0425 in the past. During the Miocene epoch, global cli- Kuypers, 1958; Jackson et al., 1969). After the mates were warm and humid, supporting dense 1950s, however, the amount of research directed forests and lush woodlands extending throughout toward understanding variation in the hominoid the tropics and into northern latitudes. These envir- brain declined. There are three main reasons for onmental conditions were favorable for the this. First, the development of molecular biological diversification of arboreal specialists, such as the techniques caused neuroscientists to focus on a hominoids. In fact, hominoids were the most abun- small number of model species under the implicit dant type of anthropoid primate throughout the assumption that many aspects of cortical structure Miocene in Africa and Eurasia, occupying a range are evolutionarily conserved. These ideas were b0075 of different ecological niches (Begun, 2003). The further bolstered by claims of uniformity in the earliest apes in the fossil record are characterized basic columnar architecture of the cerebral cortex b0650 by hominoidlike dental morphology, but monkey- (Rockel et al., 1980). Second, findings from the first like postcranial anatomy. The best known of these systematic studies of great ape behavior from the early dental apes is the genus Proconsul from field and laboratory were beginning to be appre- b0445 b0660 the Early Miocene (20–18Ma) of East Africa. ciated (e.g., Kortlandt, 1962; Schaller, 1963; e.g., b0870 b0875 Proconsul africanus endocasts show a frontal lobe Yerkes and Learned, 1925; Yerkes and Yerkes, morphology that is similar to modern hominoids in 1929). ThesePROOF studies contributed to a more sophis- being gyrified and lacking the simple V-shaped arc- ticated understanding of cognitive and emotional uate sulcus that is characteristic of most Old World complexity in great apes and suggested that they b0610 monkeys (Radinsky, 1974). Furthermore, Proconsul deserve special protected status with respect to the africanus had a relatively larger brain than extant ethics of invasive neurobiological experimentation. b0830 monkeys of comparable body size (Walker et al., Third, the book Evolution of the Brain and b0430 1983). Thus, increased encephalization and perhaps Intelligence (Jerison, 1973) had an enormous influ- a greater degree of frontal lobe gyrification were ence on the direction of later research in present early in the evolution of the hominoids. comparative neuroanatomy. This book argued for p0015 With the emergence of arid climates in the transi- the predictability of neuroanatomical structure from tion to the Pliocene and the replacement of forestsFIRSTbrain size and encephalization, suggesting that these by mosaic habitats, the arboreal specializations of metrics form the most significant contribution to hominoids were less successful. The relatively slow species diversity in brain organization. Combined reproductive rates of these taxa, moreover, made it with the ready availability of comparative brain difficult for many to endure habitat loss resulting region volumetric data in primates and other mam- from climate change and human encroachment in mals from the publications of Heinz Stephan, Heiko b0420 b0740 recent times (Jablonski et al., 2000).

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