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Provided for non-commercial research and educational use only. Not for reproduction, distribution or commercial use. This chapter was originally published in the book Fundamental Neuroscience.The copy attached is provided by Elsevier for the author’s benefit and for the benefit of the author’s institution, for non-commercial research, and educational use. This includes without limitation use in instruction at your institution, distribution to specific colleagues, and providing a copy to your institution’s administrator. All other uses, reproduction and distribution, including without limitation commercial reprints, selling or licensing copies or access, or posting on open internet sites, your personal or institution’s website or repository, are prohibited. For exceptions, permission may be sought for such use through Elsevier's permissions site at: http://www.elsevier.com/locate/permissionusematerial From Jon H. Kaas, Human Brain Evolution. In: Larry R. Squire, editor,Fundamental Neuroscience. San Diego:Academic Press, 2008, p. p1017-1038 ISBN:978-0-12-374019-9 Copyright @ 2008, Elsevier Inc. Academic Pres S E C T I O N V I I BEHAVIORAL AND COGNITIVE NEUROSCIENCE C H A P T E R 44 Human Brain Evolution Much of the allure of the neurosciences stems from the common conviction that there is something unusual about the human brain and its behavioral capacities. Nevertheless, modern neuroscientists have paid rather little attention to the study of brain evolution, and so our understanding of how the human brain differs from that of other animals is very rudimentary. In part, this neglect is due to a widely held belief that mammalian brains are all essentially similar in their internal structure and that species differ mainly in the size of the brain. This chapter reviews the modern evidence concerning brain evolution and shows that brain structure, far from being uniform across species, exhibits some remarkable variations. Because the subject is vast, the discussion is necessarily selective. Thus, after a brief review of evolutionary principles, this chapter describes the evolutionary history of three groups of vertebrates that are of special interest to people: mammals, primates, and humans themselves. The major steps are outlined in the evolution of our large, complex, and extremely useful brains from the smaller, simpler brains of the first mammals, focusing on the neocortex, as this part of the brain has been studied most extensively. The neocortex is disproportionately large in humans and is critically involved in mental activities and processes that are considered to be distinctly human. EVOLUTIONARY AND COMPARATIVE PRINCIPLES How Do We Learn about Brain Evolution? There are three main ways to learn about how different brains have evolved. First, the fossil record can Fundamental Neuroscience, Third Edition be studied. Much of what we have learned about the evolution of vertebrates in general has come from studying fossils. However, because bones readily fossilize, whereas soft tissues seldom do, we know a lot about the bones of our ancestors, but much less about everything else. Of course, one can infer much about some soft tissues, such as muscles, from their effects on bones, and this is true for brains as well. The brains of mammals fill the skull tightly, and thus the skull cavity of fossils rather closely reflects the size and shape of the brain, and even the locations of major fissures. Much has been learned and written about the changes in brain size from the fossil record (Jerison, 2007), and we could learn more by considering changes in the proportions of brain parts and even the proportions of parts of neocortex. For example, early primates already differed from most early mammals by having more neocortex in proportion to the rest of the brain, and more neocortex devoted to the temporal lobe where visual processing occurs. This implies a greater emphasis on functions mediated by neocortex and a greater emphasis especially on the processing of visual information. We can even learn something about the functional organization of the neocortex from fossils. For instance, subdivisions of the body representation in the primary somatosensory cortex often are marked by fissures in the brain, and fissure patterns revealed by endocasts (internal casts of the brain case) from fossil skulls have been used to suggest specializations of the somatosensory cortex in extinct mammals. Recently, David Van Essen (1997, 2007) has proposed that an important factor in the development of brain fissures is the pattern of connections within the developing brain. According to this theory, densely interconnected regions tend to resist separation during brain growth and form bulges 1019 © 2008, 2003, 1999 Elsevier Inc. 1020 44. HUMAN BRAIN EVOLUTION (gyri) that limit the separation distance, whereas poorly interconnected regions are free to fold and form fissures (sulci) that would increase the separation distance. Thus, it is because the hand and face regions of the somatosensory cortex are poorly interconnected that a fissure may develop between the two. If this explanation of fissures is correct, then the locations of brain fissures seen in fossil endocasts can potentially tell us something about anatomical connections in the brains of extinct mammals. Unfortunately, little of the brain’s great internal complexity is revealed by its size, shape, and fissures. Thus, to learn more about brain evolution, it is necessary to study the brains of extant (present-day) species and use comparative methods to deduce the organization of ancestral brains. There has been great progress since the early 1980s in understanding how to use comparative approaches to study evolution. In the final analysis, even studies of the fossil record involve a comparative approach. It is seldom known, for example, whether any given fossil was an actual ancestor of another fossil, but only that the comparative evidence, together with suitable times of existence, suggests that they could be. As Darwin (1859) recognized, each living species represents the living tip of a largely dead branch of an extremely bushy tree of life. By examining other living tips of the tree, we can infer much about the organizations of the brains (and other body parts) of ancestors that occupied the branching points of this tree. Theories of brain evolution, including those of the evolution of the human brain, depend on reconstructing the probable features of the brains of ever more distant relatives. The comparative method depends on (1) examining the brains of suitable ranges of extant species and (2) determining what features they share and whether these features are shared because they were inherited from a common ancestor or because they evolved separately. The 50-year-old field of cladistics provides guidelines for making such judgments. The choice of species for comparison depends on the question being asked. For example, to deduce what the brains of early mammals were like, one should examine brains from each of the major branches of the mammalian evolutionary tree (Fig. 44.1), and thus consider members of the monotreme, marsupial, and placental mammal branches. To know about early primates, members of the major branches of primate evolution should be considered, along with mammals thought to be closely related to primates, such as tree shrews. In principle, the more branches considered, the better, because a broad comparative approach is required to accurately reconstruct ancestral brain organization. As brain studies can be difficult, time-consuming, and labor intensive, it is not always possible to study a large number of species, and one must concentrate on the most informative species. The brains of all living mammals contain mixtures of ancestral and derived features, and comparative studies are needed to distinguish the two, however one might first consider the brains of those mammals that are likely to have changed the least since the time of their divergence. Because we know from the fossil record that early mammals had small brains with little neocortex, mammals with large brains and much neocortex obviously have changed quite a bit, and it is likely to be more useful to concentrate on present-day mammals with brain proportions similar to those of early mammals. Whereas the very large brains of humans and whales undoubtedly share features inherited from a small-brained common ancestor, it may be difficult to detect the common features among the multitude of changes. As early primates more closely resembled many of the living prosimian primates in brain size and proportions than monkeys, apes, and humans, studies of the brains of prosimians are likely to be especially relevant for theories of early primate brain organization. Also, it is useful to consider the probable impact of obvious specializations on the brain organizations of living mammals. Although monotremes represent a very early major branch of the mammalian tree, the living monotremes, consisting of the duckbilled platypus with a “bill” and a capacity for electroreception and the spiny echidna with spines and a long sticky tongue for eating ants, are quite specialized, as are their somatosensory systems. Although the brains of some mammals may have retained more primitive characteristics than others, it is dangerous to assume that the brain of any living mammal fully represents an ancestral condition. Brain features need to be evaluated trait by trait in a comparative context, as any particular feature could be primitive (i.e., ancestral) or derived. To reconstruct the course of brain evolution, we need to distinguish ancestral and derived characters rather than ancestral and derived species. The existence of a mixture of ancestral and derived features in a single species is referred to as mosaic evolution. A third source of information about brain evolution is based on understandings of the mechanisms and modes of brain development and the constraints they impose on evolution. For example, Finlay and Darlington (1995) have presented evidence that brains change in orderly ways as they get bigger. In general, larger brains have proportionately more neocortex and less brain stem. Finlay and Darlington suggest this is the case because the late-maturing neocortex of large VII. BEHAVIORAL AND COGNITIVE NEUROSCIENCE 1021 EVOLUTIONARY AND COMPARATIVE PRINCIPLES La mo go rph s nt i a de s Ro d an ate im Sc Si re ni Hy a ra co Tu id e bu a lid en Ma tar cro ia sce lide Xe a nar thra my o y o m 120 10 0 m tia en Placental mammals yo Early mammals 200+ myo 180 myo 135 21 Tree shrews 20 Flying lemurs 19 Mega bats 18 Old world microbats 17 New world microbats 16 Pangolins Pholi dot a 15 Cats, dogs Carnivo ra 14 Rhinos,tapirs Perisso dacty horses la C e tace 13 Dolphins,whales a e a d i m 12 Hippos Hippopota ntia i na m u 11 Cows,deer R ae elid m a 10 Camels C ae a uid yphl Insectivora S t 9 Pigs o Moles ida lip Eu ric 8 Shrews o s ea Hedgehogs ro id c Af os Tenrecs 7 ob Golden moles Pr 6 Elephants Pr 24 Rabbits 23 Rats,mice 22 Primates es trem Mono A Platypus Echidna 4 Hyraxes 3 Aardvarks 2 Elephant shrews 1 Armadillos sloths anteaters Mar supia ls 5 Manatees B Opossums kangaroos FIGURE 44.1 The probable course of the major branches of mammalian evolution (e.g., mammalian orders). Proposed clades of placental mammals are numbered, whereas monotremes (A) and marsupials (B) are lettered. Each branch of the tree also has branched many times given the great numbers of present-day species. Note how this branching pattern differs from long-standing notions of a scale of nature from simple to complex. Based on Springer and deJong (2001). brains grows proportionately longer and larger. Another difference between large and small brains is that large brains have more neurons and longer connections. The increase in neurons makes it difficult for each neuron in a large brain to maintain the same proportion of connections with other neurons, as do neurons in a small brain, and to maintain the same transmission times over longer axons. Thus, as larger brains evolve, changes in organization are needed to reduce the commitment to connections, especially connections requiring long, thick axons. A deeper understanding of the genetic, developmental, and structural constraints on brain design could allow us to better postulate how brains are likely to change in organization with changes in brain size. Cladistics and Phylogenetic Trees To understand brain evolution, we need to understand the evolutionary relationships among mammals, which are summarized in biological classifications (taxonomies). The science of classification (known as “systematics”) has a long history, but an early classification that divided the world into “things that belong to the Emperor and things that don’t” is clearly outmoded. Our modern understanding of plant and animal relationships emerged from the efforts of the Swedish naturalist Linnaeus (1707–1778), who grouped species into ever-larger categories (species, genus, family, order, class, phylum) according to degrees of resemblance and dissimilarity. We now understand VII. BEHAVIORAL AND COGNITIVE NEUROSCIENCE 1022 44. HUMAN BRAIN EVOLUTION why life forms exhibit the particular pattern of similarities and differences they do, and we have a logic for extending and refining the Linnaean system. In brief, complex life on Earth appears to have evolved only once. It is based on a molecular template that is passed on from generation to generation and yet is modifiable. Because this molecular material usually is not exchanged between individuals from different species, a phylogenetic classification can be derived that reflects times of divergence from common ancestors. Similarities retained over time reflect the preservation of parts of the code, whereas differences reflect alterations in the code. The many different modifications of the genome in the many diverging lines of descent over billions of years have led to the great diversity of life that we see today. Our current classification scheme is based on our understanding of phylogenetic (ancestor-descendant) relationships. Because this understanding continues to grow, parts of the classification scheme continue to be modified. Phylogenetic relationships are deduced from comparative evidence. The entomologist Willi Hennig (1966) helped reinvigorate this field of study when he formulated a rigorous comparative method of reconstructing phylogenetic relationships, sometimes known as “cladistics.” The term reflects Hennig’s emphasis on the correct identification of “clades,” groups of organisms that share a common ancestor. A clade is simply a branch of the evolutionary tree, which is connected through a set of ancestors (which are the branching points of the tree) to all the other branches in the tree. In Hennig’s method, evolutionary relationships are reconstructed by a process of “character analysis.” A character is any observable feature or attribute of an organism. A character could be a feature of the brain, such as the corpus callosum between the two cerebral hemispheres, or a feature of any other part of the body, or (as is often the case today) a molecule or a DNA sequence. By considering the states of as many characters as possible—for example, whether a corpus callosum is present (as it is in placental mammals) or absent (as in other vertebrates)—and by adopting the assumption that closely related species will share more character states than distantly related species, one can arrive at a hypothesis about the relationships of the groups being examined. Because a given character state can evolve independently in different lineages (e.g., forelimbs that function as wings evolved independently in birds and bats), not every character will yield an accurate picture of evolutionary relationships. It is therefore important to base reconstructions of evolutionary relationships on as many characters as possible. Typically, a very large number of possible trees can be generated from a given character analysis; the tree that requires the smallest number of changes to account for the observed pattern of character states (the maximum-parsimony solution) usually is considered to be the best estimate of the correct tree. The growth of molecular biology has provided a new source of comparative information to supplement character analyses based on anatomical characteristics, helping to improve the resolution of modern mammalian trees (Fig. 44.1). These trees guide our interpretation of the evolutionary history of brain organization. To communicate precisely, comparative biologists have developed a specialized nomenclature. The concepts of homology and analogy are central to comparative biology (Box 44.1). A group of species that all share a common evolutionary history is a natural taxon or a monophyletic group, which is the same thing as a clade. “Unnatural” taxa are groups that either exclude one or more of an ancestor’s descendants (paraphyletic groups) or that combine descendants of multiple ancestors (polyphyletic groups). The traditional classification of the great apes (orangutans, gorillas, chimpanzees) in the family Pongidae now is known to be paraphyletic because it excludes humans, which share a recent common ancestor with chimpanzees and gorillas. If a character state is found throughout a monophyletic group, it likely was present in the common ancestor of the group or even earlier. Thus, comparisons are necessary with members of a sister group, which is the monophyletic taxon thought to be related most closely to the group under study. To determine whether a character is derived (new) or ancestral, one examines members of one or more outgroup, the more distant relatives of the group under examination. The direction of change is called its polarity. For example, mammals include forms that lay eggs, the monotremes, whereas the sister group of monotremes, the marsupial–placental group, gives birth to live offspring. We can determine the polarity of these character states (egg laying, live birth) by examining out groups; that is, by examining other vertebrates like reptiles and amphibians. Because most nonmammalian vertebrates lay eggs, we conclude that egg laying is ancestral for mammals, and live birth derived. Misconceptions about Brain Evolution Probably the most serious misconception about brain evolution is that theories of evolutionary change are necessarily highly speculative (Striedter, 1998). As in other historical sciences, direct observation of the process of brain evolution is usually not possible, but objective criteria for evaluating theories and reconstructions of ancestral brains do exist (e.g., character VII. BEHAVIORAL AND COGNITIVE NEUROSCIENCE EVOLUTIONARY AND COMPARATIVE PRINCIPLES 1023 BOX 44.1 HOMOLOGY AND ANALOGY Homology and analogy are two of the most important concepts in evolutionary biology. Both terms refer to similarity, but to similarity arising from different sources. The terms can be applied to any biological characteristic or feature, including brain structures and even behavior. In our efforts to understand brain evolution, features of brains are compared across species, and it is important to deduce if these features have been inherited from a common ancestor or emerged independently. The two terms reflect conclusions based on the available evidence, and uncertainty is common. Homology When different species possess similar characteristics because they inherited them from a common ancestor, the characteristics are said to be homologous. This does not mean they are identical in structure or function. For example, all mammals appear to have a primary somatosensory area, S1, as a subdivision of neocortex. This structure appears to be involved in electroreception in the duck-billed platypus, a monotreme, but not in other mammals. Humans and monotremes have inherited an S1 from a distant ancestor (at least 150 million years ago), but subsequently, ancestors have specialized S1 in quite different ways. Analogy and Homoplasy Characteristics that have evolved independently are referred to as analogous or homoplaseous. Some authors prefer to refer to similarities in function as analogous and similarities in appearance as homoplaseous, whereas others use the terms interchangeably or prefer analogous as the more common term. As an example, most primates and some carnivores such as cats divide the primary visual cortex, V1, into alternating bands of tissue activated mostly by one eye or the other, the so-called ocular dominance columns or bands. Because carnivores and primates almost certainly diverged from a common ancestor that did not have ocular dominance columns, we conclude that this way of subdividing visual cortex evolved independently at least two times. When analogous similarities evolve, the process is called convergent or parallel evolution (parallel if the sequences of changes were similar). Both homology and analogy can be applied to structures or to specific features of structures. The forelimbs of bats and birds are homologous as forelimbs because both bats and birds inherited forelimbs from their common ancestors. The common ancestor of bats and birds did not fly, however, and the modifications that have transformed the forelimbs of bats and birds into wings evolved independently; these wing-like characteristics are therefore analogous. Correctly identifying homologies is a very important step in deducing the course of evolution of the human brain. Features such as S1, which are homologous in most or nearly all mammals, must have evolved early with the first mammals or before, whereas features common to only primates, such as the middle temporal visual area (MT), would have emerged much later in only the line leading to the first primates. Some brain features related to language production may have arisen quite recently with the emergence of archaic or modern humans. Identifying homologies and their distributions across groups of related mammals (clades) allows us to reconstruct the details of brain evolution in the different lines of descent, including the one leading to modern humans. The problem of distinguishing homologies from analogies is that both are identified by similarities. However, analogous structures have similarities based on common adaptations for functional roles, and thus they should also vary greatly in details unrelated to function. In contrast, homologous structures likely have retained many details from a common ancestor that may not be functionally necessary. Thus, aspects of structures that appear to be unessential may count more in judging homologies. Much can also be deduced from studying brain development and the development of similarities. Of course, knowledge about the phyletic (cladistic) distribution of similarities is critical, as is accounting for differences in structures by finding species with intermediate types. Ultimately, one hopes to have evidence for so many similarities that the independent evolution of them all seems extremely improbable, or sufficient evidence from differences to indicate that the similarities in structures were acquired independently. Often the evidence is far from compelling, and opinions may change with new evidence. VII. BEHAVIORAL AND COGNITIVE NEUROSCIENCE Jon H. Kaas and Todd M. Preuss 1024 44. HUMAN BRAIN EVOLUTION analysis). It is not the case that one opinion is as good as the next, although such a view has allowed poorly founded theories to persist. Another serious misconception is that evolution has a single goal or direction. This stems from the persistent belief in a “phylogenetic scale” that starts with lowly forms such as sponges; proceeds with insects, fish, amphibians, reptiles, and various mammals at successively higher levels; and reaches its pinnacle with humans. This view that the history of life is like a scale or ladder reflects the popular idea that evolution is primarily a process of progressive improvement, a philosophical and religious viewpoint that reassuringly identifies us as the most perfect species. However, evolutionary biologists have long recognized the great diversity of life and have adopted from Darwin the branching tree as a metaphor for the process whereby parent species divide to form daughter species, with each branch becoming adapted to its particular environment through natural selection. This perspective still leaves a place for progress in evolution, if progress means to become better adapted, but there are so many different ways organisms can become better adapted—most of which do not involve becoming bigger brained or smarter—that there can be no single dimension of progress, as the phylogenetic scale implies. Progress, for example, might mean reducing the size of the visual system to reduce metabolic costs in mammals living underground. Thus, there is also no universal trend toward increased complexity, as evolving brains sometimes simplify by reducing or losing parts. Overall, the brains of many mammalian groups evolved to get bigger, but this change partly reflects the fact that they started off small, and it was more often adaptive to get bigger than smaller. However, mammals with very small brains, near the theoretical limit of smallness in mammalian brain size, persist today and there are reasons to think that small brain size is not the primitive condition in all these groups, but sometimes resulted from relatively recent reductions in brain size. Interestingly, domestic mammals, with our efforts to improve a wild stock, generally have reduced brain size. Evolutionary biologists make a distinction between traits that are ancestral (also termed primitive or plesiomorphic) from those that are recently acquired (also known as derived or apomorphic), but this distinction does not imply that primitive is simple and that derived is complex. A third misconception is that ontogeny recapitulates phylogeny. At one time, evolution was thought to proceed by sequentially adding new parts (terminal addition), and that in the development of complex forms, the newest parts were those added last. Thus, the evolutionary history of any organism would be revealed in its sequence of development. Though this is not the case in general, the study of brain development remains relevant to the study of brain evolution because evolution occurs through alterations in the course of development. It is also the case that many changes in the course of development that have led to new adaptations have occurred in the later stages of development, primarily because alterations in early stages often are lethal or produce profoundly different and maladaptive adult forms. Nevertheless, it is important to recognize that the course of development can be altered in many ways and at many stages. Studies of brain development are useful because they can indicate how homologous structures that appear dissimilar in adults arose from forms that were more similar early in development. The concepts of progress and terminal addition have led some investigators to consider certain features of the brains of such mammals as humans, monkeys, and cats as either relatively old or new on the basis of their histological appearance. Poorly differentiated areas of neocortex—areas with indistinct lamination—were considered to be ancient, and welldifferentiated areas were thought to be new. For example, because the primary visual cortex (V1) has very highly differentiated layers in many primates, including humans, V1 has been considered by some to be a recently acquired area of the cortex. However, a comparative analysis indicates that the primary visual cortex (V1) is as old as the first mammals, perhaps much older. The cellular layers of V1 were poorly differentiated in early mammals, and they remain poorly differentiated in many living species. Yet, humans do not have the most highly laminated V1: this distinction belongs to the tarsier, a tiny, nocturnal primate with enormous eyes. As another example, the superior colliculus or optic tectum, an ancient visual structure, has well-differentiated layers in many birds and reptiles, but they are poorly or moderately differentiated in many mammals (including humans), yet well differentiated in other mammals, such as squirrels and tree shrews. Origin of the Neocortex The hallmark of the evolution of mammalian brains was the emergence of the neocortex. The cerebral cortex (or pallium) covers the deeper parts of the forebrain (telencephalon). In mammals, the cortex generally is divided into three parts: the lateral paleocortex or olfactory piriform cortex, the medial archicortex or hippocampus and subiculum, and the neocortex or isocortex lying in between (Fig. 44.2). The archicortex VII. BEHAVIORAL AND COGNITIVE NEUROSCIENCE EVOLUTIONARY AND COMPARATIVE PRINCIPLES A. Dorsal cortex neocortex B. DVR Temporal neocortex Rat Neocortex Superior Neocortex Temporal Neocortex Hippocampus Diencephalon Striatum Dorsal Pallidum Internal Capsule Claustrum Endopiriform Basal Amygdala Thalamus Olfactory Cortex Optic Tract Turtle ampus Hippoc Olf ac Co tor y r tex Dorsal Cortex Pallial thickening DVR Striatum Dorsal Pallidum Diencephalon Optic Tract FIGURE 44.2 Theories of the origin of neocortex. One view is that (A) only the dorsal cortex of stem amniotes gave rise to the neocortex. A less supported view is that (B) the dorsal cortex gave rise only to the superior part of the neocortex, whereas the dorsal ventricular ridge (DVR) gave rise to the temporal neocortex of extant mammals such as rats (top). See below for the location of dorsal cortex and the DVR in extant reptiles such as turtles. The neocortex and dorsal cortex are much different in size, as well as in cellular organization (see text). and paleocortex can be recognized in reptiles, and their names reflect the early conclusion that they are phylogenetically old parts of the forebrain. All extant mammals have an obvious neocortex, and the presence of a neocortex is clearly indicated in the endocasts of the skulls of early mammals, but nothing quite like the neocortex exists in sauropsids, reptiles, and birds, which represent the nonmammalian branches of amniote evolution. Hence, the term neocortex was applied to this seemingly new part of the brain. Nevertheless, the neocortex as a structure is not really new, as current evidence indicates that it is homologous to a structure in reptiles called the dorsal cortex. In contrast to the neocortex of mammals, however, which has multiple layers with different cell types and 1025 packing densities, the dorsal cortex of reptiles is a rather small and thin sheet of tissue. Whereas dorsal cortex has little more than a single row of neurons, an imaginary line drawn through the thickness of the neocortex would likely encounter over 100 neurons. Thus, the neocortex is much different in structure than the dorsal cortex. Unfortunately, no species exist today to show us what intermediate states were like in the evolution of the mammalian neocortex. Because the neocortex as a structure did not really originate with mammals and because it is not “new,” some investigators refer to the neocortex as the isocortex, using a term that refers to the relatively uniform appearance of the neocortex throughout all regions. However, the changes in the dorsal cortex that produced the neocortex are impressive, and no other vertebrates have a structure that clearly resembles the neocortex. Thus, mammals are characterized as much by their neocortex as a modified structure as they are by their mammary glands. Although the neocortex has a nearly uniform histological appearance, its considerable variability in size and organization is what allows mammals to differ so much in behavior and abilities. To understand how variations in the neocortex make this possible, it is necessary to identify ancestral features of the neocortex, that is, features that were present in the last common ancestor of living mammals, and then determine how this organization was modified in different lineages of living mammals, such as primates. The laminar organization of the neocortex appears to be similar in most mammals, suggesting that the ancestral design was so useful that many features have been retained in modern groups. For example, in most mammals and over most of the neocortex, six layers can be recognized (Brodmann, 1909). Of the six layers of neurons, layer 4 receives activating inputs from the thalamus or from other parts of the cortex. Layer 3 communicates with other regions of the cortex, layer 5 projects to subcortical structures, and layer 6 sends feedback to the thalamic nuclei or cortical area providing activating inputs. This ancestral framework for cortical neural circuits has been modified and elaborated in various lines of descent to give us the great variability in brain function we see today. The neocortex has changed by diversifying its neuron types, differentiating (and in some cases simplifying) its laminar structure in various ways, altering connections, changing its overall size and the sizes of individual cortical areas, adding cortical areas, and dividing areas into specialized modular processing units or cortical “columns.” What was achieved through these changes ranges from echolocation to language. Of course, changes in the neocortex have been accompanied by VII. BEHAVIORAL AND COGNITIVE NEUROSCIENCE 1026 44. HUMAN BRAIN EVOLUTION modifications occurring in other parts of the brain because cortical and subcortical structures often have integrated functions. For example, the superior colliculus of the midbrain has been variously modified in function, largely by changing and expanding the direct inputs from neocortex, but also through other alterations. To begin to understand how cortical organization has changed to produce the remarkable human brain, we first focus on the neocortex of early mammals. Brains of Early Mammals Early mammals had small brains with little neocortex. By comparing the histological appearance of the neocortex in extant mammals of differing lines of descent, we can conclude that the neocortex of early mammals was not as highly differentiated in terms of distinct layers and neuron types as is the cortex of many modern mammals. However, the cortex likely was not homogeneous in appearance either. In present-day mammals, the primary sensory areas typically have a noticeably different layer 4 (the receiving layer) with somewhat smaller and more densely packed neurons than in other areas. From such slight regional differences in appearance, early investigators such as Brodmann (1909) surmised that all mammals have functionally significant subdivisions of the cortex, called areas, that some areas are shared by many species (homologous areas), and that mammals differ in numbers of areas. What was difficult for Brodmann and other early investigators was to reliably identify areas by their histological appearance, especially in the poorly differentiated cortex of many small-brained mammals, but sometimes even in the large expanses of the rather homogeneous cortex in large-brained mammals. As a result, areas were often incorrectly delimited, and the sometimes radical changes in the appearance of certain areas that took place across species resulted in mistaken interpretations of homology. To Brodmann’s credit, he correctly identified the primary visual cortex in species as different from each other as humans, where the task is easy because of the area’s histological distinctiveness, and hedgehogs, which are insectivores with poor cortical differentiation. Although Brodmann’s subdivisions of human and other brains are commonly portrayed in textbooks today, many of his proposed areas and proposed homologies have little validity. Fortunately, modern methods allow us to compare many features of cortical biology in great detail, including connection patterns, neuron-response properties, and cortical histochemistry, which allows us to identify cortical areas and evaluate homologies with a high degree of assurance. From these methods, we can conclude that the neocortex of early mammals was subdivided into a small number of functionally distinct areas, on the order of 10–20, and these areas have been retained in most lines of descent. The neocortex of North American opossums (Fig. 44.3), which are small-brained marsupials, reflects many of the features of other small-brained mammals. Much of the limited expanse of the neocortex is dominated by sensory inputs relayed from the thalamus. Caudally, the neocortex includes a large primary visual area, V1, bordered laterally by a strip-like second visual area, V2. More laterally, an additional strip of cortex responds to visual stimuli, but the organization of this cortex is not known. Nearly all existing mammals have a V1, V2, and a more lateral zone of visual cortex. This pattern likely emerged with (or before) the first mammals. More rostrally, opossums have a primary somatosensory area, S1, bordered laterally by two additional representations of tactile receptors, the second somatosensory areas, S2, and the parietal ventral area, PV. Connection patterns indicate that narrow bands of the cortex rostral and caudal to S1 are also involved in processing somatosensory inputs. This collection of five somatosensory fields is seen repeatedly in small-brained mammals, although S2 and PV are not always distinct from each other. A region of cortex caudal to S2 and PV responds to auditory stimuli, and much of this region is occupied by the primary auditory area, A1, which is present in all or nearly all living mammals. However, the auditory cortex contains a number of additional areas in most mammals, including many of the studied smallbrained mammals, although homologies are often uncertain. Thus, early mammals probably had several auditory fields. More rostrally, the frontal cortex of opossums is very small and does not contain any obvious motor areas. Instead, motor-related information from the cerebellum is relayed to S1. However, opossums are marsupials (Fig. 44.1), and most or all placental mammals have a primary motor area, M1, just rostral to S1 (and the narrow somatosensory band bordering S1), and possibly a second motor area, M2, also known as the supplementary motor area, SMA. The frontal cortex also includes an orbitofrontal region, which mediates autonomic responses to exteroceptive stimuli. On the medial wall of the cerebral hemisphere, opossums and other mammals share several divisions of the limbic cortex with inputs from the anterior and lateral dorsal nuclei of the thalamus. In addition, narrow strips of the entorhinal cortex are present that connect the neocortex with the hippocampus. VII. BEHAVIORAL AND COGNITIVE NEUROSCIENCE EVOLUTION OF PRIMATE BRAINS Opossum Cortical Areas lf V1 SC uf S1 V2 Vis SR frontal S2 CT AUD olfactory bulb PV Piriform 2 mm FIGURE 44.3 Some of the proposed neocortical areas in North American opossums. Somatosensory areas include the primary area (S1), a secondary area (S2), a parietal ventral area (PV), and caudal (SC) and rostral (SR) somatosensory belts. The auditory cortex (AUD) is limited and likely contains a primary field (A1) and possibly another area or two. The visual cortex includes primary (V1) and secondary (V2) areas and a visual (Vis) belt. The caudotemporal (ct) field is probably visual. In V1, the upper visual field (uf) is represented caudal to the lower visual field (lf). Modified from Beck et al. (1996). From this ancestral pattern, a great variety of brain organizations have evolved through alterations in size and the number of parts and the connections within and between parts (Kaas, 2007a). Consider, for example, the variations of the primary somatosensory cortex. The duck-billed platypus devotes most of S1 to representing tactile receptors of its highly sensitive bill, and it has added inputs from electroreceptors. The starnosed mole devotes most of S1 to its long, fleshy nose appendages, rats mostly activate S1 with their facial whiskers, and human S1 has a large representation of the hand, lips, and mouth. In addition, the amount of neocortex varies greatly across species of mammals (Jerison, 2007), and some of this variation is due to differences in numbers of cortical areas present in different groups of mammals (Finlay and Brodsky, 2007; Kaas, 2007a). The number of sensory areas increased independently in several lines of evolution. For example, both cats and monkeys have a large number of visual areas, but the carnivore and primate lines appear to have acquired most of these areas independently rather than from a common ancestor. Thus, many of the visual areas in cats have no homologies in monkeys or humans. A similar situation holds for other regions of the brain. New areas were added, most commonly to sensory and motor regions of cortex rather than to multisensory “association” cortex as once thought. With new cortical areas, new connections between areas and subcortical structures emerged. Thus, 1027 mammals in various lines of descent evolved new cortical areas and connections, as well as other many specializations of previously existing ones. As a longrecognized example of the emergence of a new brain feature, the corpus callosum, the major pathway interconnecting the neocortex of the two cerebral hemispheres, is a derived character of placental mammals, having emerged in the ancestors of placentals after they diverged from marsupials. Whereas connections between the two hemispheres are mediated by the anterior commissure in marsupials and monotremes, most of these connections are carried in the shorter, more direct callosal pathway in placental mammals. EVOLUTION OF PRIMATE BRAINS Evolution of Primates Early primates emerged from small-brained, nocturnal, insect-eating mammals some 60 to 70 million years ago and soon branched into three main lines leading to present-day prosimians, tarsiers, and anthropoids (Fig. 44.4). The prosimian suborder of primates includes lorises, lemurs, and galagos; the anthropoid suborder consists of New World monkeys, Old World monkeys, and the ape–human group. Tarsiers are small, prosimian-like animals. Two main schemes of classification of primates have been in use, mainly because it has not been obvious where to place tarsiers. Many authors use a traditional classification and distinguish prosimian from anthropoid primates and include tarsiers with prosimians. However, this is now thought to be an unnatural paraphyletic grouping because tarsiers, despite their generally prosimianlike appearance, generally are considered to be more closely related to anthropoids than to lemurs, lorises, and galagos. This conclusion is reflected in the cladistic classification preferred by other authors, in which lemurs, lorises, and galagos are placed in the suborder, Strepsirhini, a group that has retained ancestral features, including a naked, moist rhinarum (wet nose). Tarsiers and anthropoids, which have a reduced olfactory system (and thus a dry nose), are placed in the suborder Haplorhini. The anthropoid primates are divided into the infraorders Platyrrhini (New World monkeys) and Catarrhini (Old World monkeys, apes, and humans). The earliest primates are thought to have been small-bodied, nocturnal visual predators living on insects and small vertebrates, as well as fruit. They adapted to the tropical rainforests by emphasizing vision and visually guided reaching and grasping. VII. BEHAVIORAL AND COGNITIVE NEUROSCIENCE 1028 44. HUMAN BRAIN EVOLUTION Evolution of Primates s chimps hu man gibbons Anthropoids (simians) gorillas Prosimians Myo 0 30 great apes Old World monkeys pe s cebids marmosets tarsiers galagos lorises 20 malagasy lemurs 10 a New World monkeys Hominins (apes & humans) catarrhines platyrrhines 40 50 monkeys 60 Stepsirrhines Haplorhines 70 FIGURE 44.4 The evolution and classification of primates. Tarsiers are generally considered to be prosimians, but they are related more closely to anthropoids, so they are recognized as haplorhine primates. Despite the ancient split of prosimian and anthropoid primates, they share many brain features that are unique to primates. Tree shrews and flying lemurs are thought to be close relatives of primates, and together with them constitute the superorder Archonta. See Preuss (2007) for discussion. This involved having larger, forward-facing eyes, opposable big toes and thumbs, and digits tipped with nails. These primates produced the largely nocturnal strepsirhine radiation with its varied forms, including some species now living in Madagascar that have become diurnal. The haplorine primates emerged about 60 million years ago in association with a shift from nocturnal to diurnal life, together with an increased emphasis on fruit eating (Ross, 1996). With the shift to diurnality came reduced dependence on olfaction, enhancement of the visual system, enlarged body size, and sometimes a more gregarious mode of life. Specifically, the olfactory apparatus was reduced in size, and the eyes enlarged and brought close together. Early haplorhines evolved a fovea, a specialized region of the retina filled with small photoreceptors and devoid of blood vessels, that enhances central visual acuity. The reflecting surface at the back of the eye (tapetum lucidum), an adaptation to nocturnal vision present in prosimians and many other nocturnal mammals, was lost. Anthropoids underwent further specializations, modifying cone morphology, increasing the proportion cones to rods, and filling the fovea with cones to the near-exclusion of rods. These adaptations enabled anthropoids to achieve a high degree of color discrimination. Nevertheless, whereas humans and other Old World anthropoid primates have three types of retinal cones, ancestral anthropoids probably possess the two types of cones, similar to most modern prosimians and New World monkeys. A VII. BEHAVIORAL AND COGNITIVE NEUROSCIENCE EVOLUTION OF PRIMATE BRAINS third cone type, enabling full trichromatic vision, appears to have evolved independently in the ancestors of Old World anthropoids and in several New World monkey groups. The enhancements of color vision in the anthropoids are plausibly regarded as adaptations for distinguishing ripe, edible fruits. The shift to diurnality was also marked by larger social groupings, which may offer enhanced protection from predation. These changes were accompanied by increased brain size, including increases in the temporal lobe visual region, and in regions of the parietal and frontal cortex mediating motor control and social interactions. The ancestors of present-day tarsiers evidently abandoned the diurnal niche to become nocturnal visual predators again. Tarsiers retain a fovea, but they have a rod-dominated retina and their enormous eyes are sensitive at low light levels without the aid of a reflecting tapetum. The primary visual cortex became very large relative to the rest of the brain and is extremely well differentiated, with a multiplicity of layers and sublayers (Collins et al., 2005). Tarsiers became such extremely specialized visual predators that they eat no plant food. Other haplorhines (anthropoids) remained diurnal and spread to many niches, including those outside the rainforest and niches based more on eating leaves as well as fruits. Some increased considerably in body size. Later anthropoids were able to process hard, husked fruits with their hands and teeth. Some early anthropoids managed to reach South America from Africa, apparently by rafting, to form the New World monkey radiation. All modern anthropoids are diurnal with the exception of owl monkeys, a New World monkey group, that has (like tarsiers) become secondarily nocturnal. In Africa, early anthropoids diverged some 25 to 30 million years ago into lines leading to modern Old World monkeys and to apes. At first, apes were the most successful radiation, coming to occupy a range of rainforest and open woodland environments, whereas monkeys were quite rare. Perhaps as many as 30 different types of apes existed at one time. This condition changed radically some 10 million years ago when monkeys became abundant and apes rare. This change may have resulted from the advent of a more seasonably variable and drier climate. Ancestral Old World monkeys acquired specialized teeth suited to a leaf and fruit diet in drier climates. Also, the more rapid reproduction of monkeys may have made them more resistant to extinction than apes. Some 5 or 6 million years ago, a line of apes diverged into two branches: one that gave rise to modern common chimpanzees and bonobos (pygmy chimpanzees), and a second branch that led to the group of 1029 bipedal apes, the “hominins,” that includes modern humans (Fig. 44.5). Traditionally members of the human branch were referred to as “hominids,” that is, as members of the Family Hominidae. Today, taking into account the close relationship of humans to the great apes, it is customary to extend the term “hominid” to the entire great ape clade, to use the term “hominines” (Subfamily Homininae) to refer to the African ape clade (chimpanzees, bonobos, humans, and gorillas), and to apply the term “hominins” (Tribe Hominini) to members of the human branch of the African ape clade. (A tribe is, taxonomically speaking, a sub-subfamily.) The oldest known hominins, the so-called australopithecines, date back at least 4 million years. These early hominins were bipedal, but skeletal traits suggest they retained considerable ability for climbing trees. Body size was rather small and males were much bigger than females. The brain was only slightly larger than for apes of similar body size. Hominin traits may have emerged as adaptations to a drier environment with grassland and savanna. Early australopithecines soon gave rise to a number of species differing in body size and limb proportions, as well as in characteristics of the jaws and teeth and brain size. Primitive members of our own genus began to emerge some 2 million years ago with Homo habilis (or “handy man,” due to its use of stone tools). Homo habilis had a slightly increased cranial capacity compared to australopithecines, reduced face and teeth, and pelvic modifications for improved bipedal locomotion and the birth of neonates with larger heads. About 1.7 million years ago, H. habilis appears to have been replaced by H. erectus, a larger hominin with a further reduction in face and teeth and a larger brain. Shortly thereafter, Homo erectus spread out of Africa to central Asia. Homo sapiens emerged from an African population of H. erectus some 250,000 to 300,000 years ago. Other members of the genus Homo coexisted with Homo sapiens until as recently as 35,000 years ago, notably the Neanderthals, who adapted to a colder Europe and southwest Asia over 130,000 years ago. They disappeared and were replaced by modern H. sapiens some 35,000 years ago. Neanderthals were shorter and more heavily built than modern humans, but had a comparable or slightly larger cranial capacity. Over the last 15,000 years, some populations of humans have become smaller and have reduced their brain size, possibly as a result of a poorer diet as agriculture replaced hunting and gathering. Chimpanzees and bonobos (also misleadingly known as “pygmy chimpanzees”) appear to be our closest surviving relatives. Humans and chimpanzees are 98 to 99% similar in the coding sequences of genes, VII. BEHAVIORAL AND COGNITIVE NEUROSCIENCE 1030 44. HUMAN BRAIN EVOLUTION Evolution of Hominins 7 myo 6 5 4 3 2 1 Hominins - Genus Homo 0 H. erectus larger brain, bipedal reduced teeth, culture H. sapiens H. antecessor H. heidelbergenis H. habilis Hominins - Genus Australopithecus Lucy Hominins - Genus Paranthropus H. neanderthalensis A. afarensis P. boisei P. aethiopicus P. robustus bipedal plus climbing A. africanus A. anamensis Apes Ardipithecus ramidus Bonobos 12 myo 18 Chimps Gorillas Orangutans myo Gibbo ns 7 myo 6 5 4 3 2 1 0 FIGURE 44.5 The evolution of apes and humans. Apes include living apes and a late fossil judged to not be bipedal (Ardipithecus ramidus). Australopithecus and Paranthropus appear to have been bipedal. The age of the famous fossil, Lucy, is indicated. Relationships are somewhat uncertain, and more branches on the tree exist (de Sousa and Wood, 2007). which is more similar than found among morphologically indistinguishable sister species of some genera. The bases for the great phenotypic differences between humans and chimpanzees, including those in brain size and presumably brain organization, are not well understood, but changes in patterns of gene expression are likely to be important. Homo sapiens Brains of Early Primates The brains of primates vary greatly in size and fissure patterns. Humans have the largest of primate brains, whereas mouse lemurs have the smallest (Fig. 44.6). Judging from fossil endocasts and other parts of the skeleton, early primates were lemur-like in body form, and their brains were shaped like those of present-day lemurs, although smaller. The modern mouse lemur has moderately expanded temporal and occipital lobes, indicating an emphasis on vision, a calcarine fissure or fold within the primary visual cortex, and a lateral (Sylvian) fissure separating 2cm Microcebus murinus FIGURE 44.6 Lateral views of the brains of a human and a small prosimian primate, the mouse lemur, to illustrate the great range of sizes for present-day primates. VII. BEHAVIORAL AND COGNITIVE NEUROSCIENCE 1031 EVOLUTION OF PRIMATE BRAINS somatosensory areas of the parietal lobe from auditory areas of the temporal lobe. Most modern primates share these two fissures. Many early as well as presentday primates also have an additional prominent fissure in the temporal lobe (the superior temporal sulcus). Other fissures are more variable. Among living prosimians, evidence about brain organization comes mostly from studies of galagos, nocturnal animals from Africa that are cat-sized or smaller and eat mainly fruit, tree gums, and insects. Their brains have only a few fissures (Fig. 44.7). Their visual system contains several features that are common to all primates that have been examined, including a distinctive type of lamination in the lateral geniculate nucleus of the visual thalamus (with magnocellular and parvocellular layers) and a pulvinar complex with the distinct inferior and lateral pulvinar divisions. As in other primates, the superior colliculus of the midbrain represents only the contralateral half of the visual field, whereas other mammals have a more extensive representation that includes the complete visual field of the contralateral eye. The visual Galago arm ac e PMV f S2 PV 5 mm R Lat. Sulcus Lat. Sulcus V1 DL MT A1 A AB th mou V3 V2 MS T hand T M1 MTc V3 FS F FE Sensorimotor trunk PMD Vi su al b 1 3a S1-3 SC Posterior parietal DM SR foot SMA ITc Visual cortex includes areas V1 and V2, both retained from nonprimate ancestors but with primate modifications including “blobs,” which are cytochrome oxidase-rich modules in V1, and band-like modules that span the width of V2. Other visual areas apparently shared with all other primates include V3, a dorsomedial area (DM), and a middle temporal visual area (MT), all of which receive direct inputs from V1. Other areas, such as the dorsolateral area (DL or V4), also are shared widely among primates, but not enough is known about visual cortex organization in the various primate species to be certain of how many of the more than 30 proposed visual areas are common among primates. Some or most of these areas, such as MT, are not found in nonprimates, or at least not in a primate-like form, and these areas are distinctive features of primate brains (Kaas, 2007b; Preuss, 2007). Organization of the auditory system of galagos and other prosimians is not well understood, but they appear to share two primary or primary-like areas, A1 and R (“rostral”), with other primates, and they likely share several nonprimary areas as well. A1 and possibly R are likely to have been retained from nonprimate ancestors. The somatosensory cortex appears to be relatively unchanged from nonprimate ancestors, as an S1, S2, and PV have been identified in galagos, and there are additional, narrow belts of somatosensory cortex along the rostral and caudal borders of S1. S2 and PV retain the primitive feature of being activated directly by inputs from the ventroposterior nucleus of the thalamus (Fig. 44.8). Motor cortex organization is surprisingly advanced, with the five or more premotor areas that are also found in anthropoid primates. ITr Ancestral state FIGURE 44.7 A lateral view of the brain of a prosimian primate, Galago garnetti, showing some of the proposed visual, somatosensory, auditory, and motor areas. Visual areas include the primary (V1) and secondary (V2) areas, common to most mammals, but with the modular subdivisions (blobs in V1; bands in V2) characteristic of primates. As in other primates, galagos have a third visual area (V3), a dorsomedial area (DM), a middle temporal area (MT), a dorsolateral area (DL), a fundal-sucal-temporal area (FST), an inferior temporal visual region (IT) with subdivisions. Posterior parietal cortex (PP) contains a caudal division with visual inputs and a rostral division with sensorimotor functions. The auditory cortex includes a primary field (A1), a rostral area (R), and an auditory belt (AB), which includes several areas and regions of the parabelt auditory cortex. The somatosensory cortex includes a primary area (S1 or 3b), a parietal ventral area (PV), a secondary area (S2), a somatosensory rostral belt (SR or 3a), and a somatosensory caudal belt (SC or possibly area 1 or areas 1 plus 2). Motor areas include a primary area (M1), ventral (PMV) and dorsal (PMD) premotor areas, a supplementary motor area (SMA), a frontal eye field (FEF), and other motor areas on the medial wall of the cerebral hemisphere. Modified from Kaas (2007b). Derived state Non-anthropoid mammals Anthropoid mammals (galagos, tree shrews, cats) (macaques, marmosets) Cortex S1 Thalamus S2 S2 S1 VP VP Cutaneous afferents Cutaneous afferents FIGURE 44.8 Somatosensory processing in prosimian primates and anthropoid primates. The processing in anthropoids is serial, rather than parallel and serial. Because the prosimian type also is found in a number of nonprimate mammals, we infer that this is the ancestral state. The ventroposterior nucleus (VP) of the somatosensory thalamus and the first (S1) and second (S2) somatosensory areas of the cortex are shown. VII. BEHAVIORAL AND COGNITIVE NEUROSCIENCE 1032 44. HUMAN BRAIN EVOLUTION Although the brains of prosimians are not especially large, they share a number of primate-specific areas with anthropoids over and above the complement inherited from their mammalian ancestors. Overall, prosimians and other primates share a large number of brain specializations that likely evolved in early primates or their immediate ancestors (Preuss, 2007). The study of prosimians is critical for understanding that features of brain organization are distinctive of primates. Brains of Early Anthropoids The anatomy of early anthropoids suggests that an emphasis on high-acuity, diurnal vision and reduced emphasis on smell were important in their evolution. The endocasts of the skulls of early anthropoids indicate that the visual cortex of the temporal lobe was more expansive than in prosimians. Collectively, present-day New World and Old World monkeys cover a wide range of body and brain sizes. The extent to which fissures develop on the brain surface of these primates depends largely on brain size. All primates, no matter how small, have a deep calcarine fissure in the occipital lobe. Most also have a deep lateral sulcus (Sylvian fissure). These are the only well-developed sulci in marmosets, the smallest of the New World monkeys. Slightly larger New World monkeys, such as owl monkeys and squirrel monkeys, also have a shallow central sulcus and a shallow superior temporal sulcus. The largest New World monkeys, such as spider monkeys and cebus monkeys (capuchins), have even more sulci and resemble (at least superficially) the well-fissured brains of Old World monkeys, such as macaques and baboons. Both Old World and New World monkeys have all the areas of the neocortex described for prosimians, as well as some additional areas. Most notably, the somatosensory cortex has been altered so that areas 3a, 3b, 1, and 2 are well differentiated from each other, with each area corresponding to a separate representation of receptors of the contralateral body surface (Kaas, 2007b). Within S1 (area 3b), the proportional representation of body parts varies somewhat across species, so that in some monkeys as much as half of the area is devoted to the face and oral cavity. The hand is also prominently represented, especially in monkeys such as macaques. Some New World monkeys, such as spider monkeys, have a large representation of their highly tactile, prehensile tail. Marmosets appear to have a relatively poorly differentiated somatosensory region, which lacks a definite area 2, a field that is responsive to tactile stimuli and muscle movements in other monkeys. This may be a consequence of brain size reduction in marmosets, which have evolved smaller brains and bodies from larger ancestors. In all anthropoids, S2 and PV appear to have lost activating inputs from the ventroposterior nucleus of the somatosensory thalamus, and they depend on inputs from areas 3a, 3b, 1, and 2 (Fig. 44.8). S2 and PV receive modulatory inputs from the ventroposterior inferior nucleus. Thus, processing in the somatosensory system became more serial than parallel with the advent of monkeys. Other differences likely exist between anthropoids and prosimians in the somatosensory portions of the lateral sulcus and posterior parietal cortex, but more research is needed. Both of these regions of somatosensory processing have expanded greatly in anthropoids compared to prosimians, and several areas involved in visually guided reaching have been described in macaque monkeys. Currently, there is much interest in how the visual system of monkeys is subdivided into cortical areas and how these visual areas function in behavior. Elaborate proposals have been presented, but considerable uncertainty remains. In Old World monkeys, over 30 visual areas have been proposed, and it seems likely that anthropoids in general have more visual areas than prosimians, although the full extent of this difference is not yet clear. In the auditory cortex, a core of three primary-like areas, a belt of seven to eight additional fields, and a “parabelt” of several additional areas have been proposed, but not enough is known about auditory cortex of prosimians to know what differences exist. The proposed subdivisions of the motor cortex in prosimians and simians are quite similar, although some of the premotor areas of prosimians have been subdivided into two or three areas in Old World monkeys. Finally, comparisons of cortical connections and architectonics in galagos and macaque monkeys have led to the conclusion that macaques have several areas of dorsolateral prefrontal cortex in addition to those found in galagos. Evolution of Hominin Brains In trying to determine the recent course of the evolution of the human brain, we depend more on the fossil record than on a comparative approach, as we are the only surviving hominin species. Human brains are much bigger than those of our closest living relatives, the African apes. From the fossil record (Fig. 44.9), we can see that early australopithecines had brains that were only 10–25% larger than the brains of present day African apes when body size is taken into account. However, brains increased rapidly in size as the various species of Homo evolved over the last 2 million years. Early hominins had brains in the 600- to VII. BEHAVIORAL AND COGNITIVE NEUROSCIENCE 1033 EVOLUTION OF PRIMATE BRAINS Brain size (in cm3) plotted against time (Myr) for specimens attributed to Hominidae Australopithecus afarensis Australopithecus africanus Australopithecus robustus Homo habilis Homo erectus Archaic Homo sapiens Neanderthals Early modern Homo sapiens Living Humans (Males) Living Humans (Females) 1600 1400 1200 1000 800 600 gorillas 400 chimpanzees 200 0 0.5 1 1.5 2 2.5 3 3.5 Estimated Age (Myr) FIGURE 44.9 Evidence for the rapid growth of brains of hominins over the last 2 million years. The brain sizes of modern chimpanzees and gorillas have been added for comparison. Modified from McHenry (1994). 800-cc range; H. erectus, about 500,000 years ago, had brain volumes close to 1000 cc; and soon thereafter brains reached the volumes within the range of modern H. sapiens, which averages about 1400 cc. In deducing the changes in internal organization that likely occurred over this remarkable increase in brain size, it would be useful to know more about the organization of the brains of the living apes. However, only limited information is available from early motor and somatosensory mapping experiments on apes, and further noninvasive studies, as in humans, are needed. Much can be learned by studying the histology of tissue from brains of apes that have died natural deaths using modern histochemical techniques (Preuss, 2001), but at the present time, we have only a limited understanding of how the brains of apes differ from those of monkeys. Traditionally, it was postulated that the higher-order “association” regions of the frontal, parietal, and temporal lobes underwent great expansion in human evolution. This view recently has been called into question by the finding that the relative proportions of the frontal, parietal, and temporal lobes are similar in great apes and humans, notwithstanding the much larger absolute size of the human brain. The fact remains, however, that the primary sensory cortical and thalamic structures are of roughly the same absolute size in humans and great apes, whereas the association regions of humans are much larger in absolute terms. This is consistent with classical accounts of human brain evolution that emphasize the expansion of higher-order regions. Changes in human evolution did not only involve an increase in brain size. Recent comparative studies have documented human specializations at the level of cellular and modular organization as well. At the present time, however, we do not know enough about the specializations of human brain organization to understand how brain changes are related to human specializations of cognitive organization, such as the capacity for conceptualizing the mental states of other individuals (“theory of mind”; Povinelli and Preuss, 1995). One of the signature specializations of Homo sapiens is of course language, and it often has been assumed that the evolution of language involved the evolution of specialized language areas in the brain, such as Wernicke’s area in the temporoparietal cortex and Broca’s area in the frontal lobe. Human brains are not symmetrical in shape, so that the planum temporale, the sheet of cortex on the lower surface of the lateral sulcus (the upper face of the temporal lobe), is usually larger in the left cerebral hemisphere than on the right. As the left hemisphere usually becomes dominant for language, the larger size of the left planum temporale has long been assumed to be related to language. Interestingly, however, great apes exhibit the same asymmetry of the temporal lobe as humans, despite their lack of language. When and how language emerged in hominins remain issues of much speculation, as does the nature of the changes in brain organization that support language (Deacon, 2007). What seems likely is that previously existing brain regions used for other, nonlinguistic functions in nonhuman primates, such as the ventral premotor area and dorsal-stream auditory areas, became specialized for language in the ancestors VII. BEHAVIORAL AND COGNITIVE NEUROSCIENCE 1034 44. HUMAN BRAIN EVOLUTION of humans, ultimately acquiring the functions of Broca’s and Wernicke’s areas. Presumably, the evolution of language involved changes in the internal organizations of these areas (see, for example, Buxhoeveden et al., 2001). WHY BRAIN SIZE IS IMPORTANT A general assumption is that larger brains are better because they can do more. This does not imply that brains of the same size (or same size in proportion to the body) do the same things, because brain organization is modified for different functions. Nevertheless, larger brains do have obvious design problems that are likely to have been solved in similar ways in the different lines of evolution. To some extent, neurons usually enlarge as brains get bigger, but dendrites and axons cannot enlarge much without compromising their functions. To maintain passive cable conduction in dendrites, Bekkers and Stevens (1970) calculated that dendrites would need to increase four times in diameter when they double in length. Similarly, when axons double in length, axon diameter must also double, to maintain conduction times. As brain size increases, some dendrites and axons do become longer and enlarge disproportionately. Given the problems associated with increasing neuron size, the major way of increasing brain size is to increase the number of neurons. This introduces a related problem as the number of neurons increases: it becomes more and more difficult to maintain each neuron’s connections with the same percentage of other neurons, since the required number of connections grows much faster than the number of neurons. Cell body densities typically decrease and cortical thickness increases, but the increase in connections is not nearly enough to maintain ratios of connectivity or to fully compensate for longer connection distances. As a result, larger brains generally devote much more of their mass to connections. There are two major ways in which larger brains can be modified to reduce the design problems produced by larger distances and more neurons. First, the brain can become more modular, so that most connections of individual neurons are with neighboring, rather than more distant, neurons. This can be done, for example, by increasing the number of processing areas so that areas are usually smaller. In addition, areas can be subdivided into smaller functional divisions (columns or modules), which likewise reduce the need for long connections. Thus, larger brains are likely to have larger numbers of cortical areas, and larger areas are likely to contain several types of modules. Second, connections that require long, thick axons should be reduced as much as possible. This can be done by grouping functionally related areas together so that necessary connections between areas are shorter. An effective way of reducing the need for long connections, as brains get bigger, is to increase the degree of specialization of each cerebral hemisphere. As regions and areas of each hemisphere become differently specialized, the major cortical connections become more focused within the same hemisphere, rather than between hemispheres. As a result, the size of the corpus callosum does not increase proportionately with the size of the brain. In addition, proportionately fewer of the callosal axons are of the larger diameters that would be needed to preserve fast conduction times. Therefore, large brains should be less symmetrical than small brains. The large human brain appears to be extreme in this respect. Another issue is that large cortical areas are unlikely to function in the same manner as small cortical areas. Unless neurons compensate with larger dendrites and intrinsic connections as areas get larger, the computational window or scope of neurons will decrease. For example, as a visual area gets bigger, individual neurons would evaluate information from less and less of the total visual field (Fig. 44.10). This implies that as areas get bigger, their neurons become less capable of global center-surround comparisons and more devoted to local center-surround comparisons. Thus, some of the integrative functions of large areas must be displaced to smaller areas. It is also apparent that changes in the sizes of dendritic arbors and the lengths of intrinsic axons in smaller areas would have more impact on the sizes of computational windows of neurons. Comparable changes in dendrites and axons would enlarge or reduce receptive field sizes more in a small than a large visual area (Fig. 44.10). Because their functions are more modifiable by small structural modifications, smaller areas may be specialized more easily for different functions. Recent measurements suggest that neurons in large areas typically do not have longer dendritic arbors and larger intrinsic connections, and indeed, they may have smaller dendritic arbors. In addition, although primary sensory areas are often larger in larger brains, they are not enlarged in proportion to the rest of cortex (Fig. 44.11). Thus, the primary visual cortex is less than three times larger in human brains than in the brains of macaque monkeys, whereas the neocortex as a whole is over 10 times larger (Fig. 44.10). In humans, primary visual cortex is about the same size as in the much smaller chimpanzee brain. The general lack of proportional growth of cortical areas with brain size reduces the VII. BEHAVIORAL AND COGNITIVE NEUROSCIENCE 1035 WHY BRAIN SIZE IS IMPORTANT A. Human 800 cm2 2. A. 10 5 20 5 40 2.5 10 20 1. 1. 2. Chipanzee 240 cm2 5 B. 5 1. 10 20 2.5 10 20 40 Macaque 72 cm2 Owl monkey 16cm2 5 C. 5 2.5 10 20 10 5 cm 20 Least Shrew 1.5 cm2 40 2. B. Human area 17 3000 mm2 FIGURE 44.10 The effects of varying the horizontal spread of dendritic arbors of neurons in large (A) and small (B and C) visual areas. An increase in arbor size (1 to 2) in a large area (A) produces little change in receptive field size (circles 1 to 2 in the central 20° of the visual hemifield on the right), whereas such a change (B to C) in a small area changes the scope of the receptive field greatly. Thus, the functions of small areas are changed more dramatically by small morphological adjustments. Surface view schematics of retinotopically organized visual areas are on the left, whereas schematics of receptive fields in the visual hemifield and the lower visual quadrant are on the right. From Kaas (2000). impact of the changing of functions of areas with size, and reflects the addition of other smaller cortical areas. Other size-related constraints relate to mechanisms of development. We often assume that natural selection can act independently on each brain trait, but this is unlikely to be the case. Instead, selection may operate on a few developmental mechanisms, such as those that control the number of neurons or the extent to which correlated activity levels maintain functional connections. Along this line of reasoning, Finlay and Darlington (1995) have provided evidence that latedeveloping brain structures such as neocortex have enlarged disproportionately in mammals with larger brains (“late makes large”). As we learn more about Macaque 1200 mm2 Mouse 4.5mm2 5 mm FIGURE 44.11 Species differences in (B) the surface area of the neocortex and (A) of the primary visual cortex in one cerebral hemisphere. The neocortex of humans is over 500 times larger in surface area and over twice as thick as the neocortex in the smallest mammals that resembled those leading to the first primates and over three times the surface area of our closest living relatives, the chimpanzees. Some of the areas of the brain are also larger in humans, but not to the extent expected from the great enlargement of the neocortex. From Kaas (2000). VII. BEHAVIORAL AND COGNITIVE NEUROSCIENCE 1036 44. HUMAN BRAIN EVOLUTION the genetics and mechanisms of development and how development is modified in evolution, we should be able to form more accurate models of brain evolution, and understand more fully how the human brain emerged from those of our ancestors. We might also benefit from considerations of other possible constraints on brain size. A larger brain creates more heat, and thus needs a better cooling system (Falk, 1990), and the higher metabolic costs of a larger brain may require a better diet or the reduction in size of other metabolically expensive tissues, such as the gut. Beyond Brain Size: Variations in Neuron Densities, Neuron Types, and Local Connections Although brain size has important implications for brain function, distantly related species of about the same brain size sometimes appear to have quite different behavioral capacities. One reason, of course, is that the brains may be organized differently; sharing for example, some cortical areas but not others, or specializing shared cortical areas in different ways. Although more comparative studies are needed, it seems unlikely that large rodents with brains as large as those of some monkeys have as many cortical areas as the monkeys. Specializations of shared (homologous) areas are probably quite common. Primates, for example, exhibit a number of variations in the organization of primary visual cortex, including specializations found in apes and humans, but not monkeys, as well as specializations that are restricted to humans (Preuss et al., 1999; Preuss and Coleman, 2002). At the cellular level, humans and apes are the only primates that have a type of neuron, the spindle cell, in the anterior cingulate and frontoinsular cortex (Watson and Allman, 2007). The functional significance of such variations in brain structure and organization is largely unknown, but these variations indicate that there is much to consider besides brain size. Another important factor is that recent studies indicate that primate brains simply have many more neurons than rodent brains (and probably the brains of other taxanomic groups) of the same size (Herculano-Houzel et al., 2007). This is because as the brains of rodents increase in size from small to large species, the density of neurons in the brain decreases, and so, the gain in neuronal numbers is not as great as one might expect. However, in primates, the neuronal density does not change very much with brain size so that more neurons are gained with each increase in brain size. If the same scaling rules relating numbers of neurons to brain size in rodents applied to primates, a human brain with about 100 billion neurons would have to weigh over 45 kg., and be supported by a body the size of a blue whale. The greater neuronal densities in the brains of larger primates would seem to present an advantage in processing capacity that gives primates with larger brains a considerable advantage over rodents with large brains. CONCLUSIONS Based on comparative studies and the fossil record, we conclude that early mammals had small brains with little neocortex and few functional subdivisions (areas or fields) of cortex. Vision was emphasized in the early primates, and the visual cortex in the temporal and occipital lobes enlarged. These primates also had several unique features of the visual system, including new visual areas such as MT, distinctive kinds of modules in V1 (blobs) and V2 (bands), separate magnocellular and parvocellular layers in the lateral geniculate nucleus, and a representation in the superior colliculus restricted to the contralateral visual hemifield. Several premotor areas were present, whereas the somatosensory system was relatively primitive. Later anthropoid primates had larger brains, more neocortex, and more areas of neocortex. The somatosensory cortex had expanded and included the four strip-like areas on the anterior parietal lobe, areas 3a, 3b, 1, and 2. We know little about possible specializations of the brains of apes. However, over the last 6 million years of evolution in the human lineage, brains increased three to four times in size, due mainly to the enlargement of the cortex. Although the relative proportions of the different cortical lobes remain similar in humans and apes, the available evidence suggests that the cortex did not expand uniformly in human evolution: the association regions of frontal, temporal, and parietal lobes are much larger in absolute terms in humans than in apes, whereas human primary sensory areas are about the same absolute size as those of apes. The expansion of nonprimary cortex was probably accompanied by a further increase in the number of cortical areas, modifications leading to functional and anatomical asymmetries in the two cerebral hemispheres, specializations for language and cognition, and larger expanses of prefrontal, parietal, and temporal cortex. The larger brains had many more neurons with a greater proportion of tissue devoted to connections relative to cell bodies, and presumably had a higher ratio of local connections to long-distance connections. Further progress in understanding the course of the evolution of the human brain can be achieved with VII. BEHAVIORAL AND COGNITIVE NEUROSCIENCE 1037 CONCLUSIONS current methods of investigation. We have the opportunity to learn much about the similarities and differences among the brains of various primates. Neuroscientists have generally concentrated on studies of brain features that are widely shared, but we need to know more about the differences in brain structure and function that make us distinctively human. References Beck, P. D., Pospichal, M. W., and Kaas, J. H. (1996). Topography, architecture, and connections of somatosensory cortex in opossums: Evidence for five somatosensory areas. J. Comp. Neurol. 366, 109–133. Bekkers, J. M. and Stevens, C. F. (1970). Two different ways evolution makes neurons larger. Prog. Brain Res. 83, 37–45. Brodmann, K. (1909). “Vergleichende Lokalisationslehre der Grosshirnrhinde.” Barth, Leipzig. [Reprinted as Brodmann’s “Localisation in the Cerebral cortex,” translated and edited by L. J. Garey, Smith-Gordon, London, 1994.] Buxhoeveden, D. P., Switala, A. E., Roy, E., Litaker, M. and Casanova, M. F. (2001). Morphological differences between minicolumns in human and nonhuman primate cortex. Am. J. Phys. Anthropol. 115, 361–371. Collins, C. E., Hendrickson, A., and Kaas, J. H. (2005). Overview of the visual system of Tarsius. Anat. Rec. 287A, 1013–1025. Darwin, C. (1859). “On the Origin of Species.” John Murray, London. [Facsimile of the first edition: Harvard Univ. Press, Cambridge, MA, 1984]. Deacon. (2007). The Evolution of Language Systems in the Human Brain. In “Evolution of Nervous Systems,” Vol. 3 (J. H. Kaas and L. H. Krubitzer, eds.), pp. 529–547. Elsevier, London. De Sousa, A., and Wood, B. (2007). The hominin fossil record and the emergence of the modern human central nervous system. In “Evolution of Nervous Systems,” Vol. 4 (J. H. Kaas and T. M. Preuss, eds.), pp. 292–336. Elsevier, London. Falk, D. (1990). Brain evolution in Homo: The “radiator” theory. Behav. Brain Sci. 13, 339–381. Finlay, B. L., and Brodsky, P. (2007). Cortical evolution as the expression of a program for disproportionate growth and the proliferation of areas. In “Evolution of Nervous Systems,” Vol. 3 (J. H. Kaas and L. A. Krubitzer, eds.), pp. 73–96. Elsevier, London. Finlay, B. L., and Darlington, R. B. (1995). Linked regularities in the development and evolution of mammalian brains. Science 268, 1578–1584. Hennig, W. (1966). “Phylogenetic Systematics.” University of Illinois Press, Urbana. Herculano-Houzel, S., Collins, C., Wong P., and Kaas, J. H. (2007). Cellular scaling rules for primate brains. Proc. Natl. Acad. Sci. USA. In press. Jerison, H. J. (2007). What fossils tell us about the evolution of the neocortex. In “Evolution of Nervous Systems,” Vol. 3 (J. H. Kaas and L. A. Krubitzer, eds.), pp. 1–12. Elsevier, London. Kaas, J. H. (2000). Why is brain size so important: Design problems and solutions as neocortex gets bigger or smaller. Brain Mind 1, 7–23. Kaas, J. H. (2007a). Reconstructing the organization of neocortex of the first mammals and subsequent modifications. In “Evolution of Nervous Systems,” Vol. 3 (J. H. Kaas and L. A. Krubitzer, eds.), pp. 27–48. Elsevier, London. Kaas, J. H. (2007b). The evolution of sensory and motor systems in primates. In “Evolution of Nervous Systems,” Vol. 4 ( J. H. Kaas and T. M. Preuss, eds.), pp. 35–57. Elsevier, London. McHenry, H. M. (1994). Tempo and mode in human evolution. Proc. Natl. Acad. Sci. USA 91, 6780–6786. Povinelli, D. J. and Preuss, T. M. (1995). Theory of mind: Evolutionary history of a cognitive specialization. Trends Neurosci. 18, 418–424. Preuss, T. M. (2001). The discovery of cerebral diversity: An unwelcome scientific revolution. In “Evolutionary Anatomy of the Primate Cerebral Cortex” (D. Falk and K. R. Gibson, eds.), pp. 138–164. Preuss, T. M. (2007). Primate brain evolution in phylogenetic context. In “Evolution of Nervous Systems,” Vol. 4 (J. H. Kaas and T. M. Preuss, eds.), pp. 1–34. Elsevier, London. Preuss, T. M., and Coleman, G. Q. (2002). Human specific organization of primary visual cortex: alternating compartments of dense Cat-301 and calbindin immunoreactivity in layer 4A. Cereb. Cortex, 12, 671–691. Preuss, T. M., Qi, H., and Kaas, J. H. (1999). Distinctive compartmental organization of human primary visual cortex. Proc. Natl. Acad. Sci. USA 96, 11601–11606. Ross, C. (1996). Adaptive explanation for the origins of the Anthropoidea (Primates). Am. J. Primatol. 40, 205–230. Springer, M. S., and deJong, W. W. (2001). Which mammalian supertree to bark up. Science 291, 1709–1711. Striedter, G. F. (1998). Progress in the study of brain evolution: From speculative theories to testable hypotheses. Anat. Rec. (New Anat.) 253, 105–112. Van Essen, D. C. (1997). A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385, 313–318. Van Essen, D. C. (2007). Cerebral cortical folding patterns in primates: Why they vary and what they signify. In “Evolution of Nervous Systems,” Vol. 4 (J. H. Kaas and T. M. Preuss, eds.), pp. 267–289. Elsevier, London. Watson, K. K., and Allman, J. M. (2007). Role of spindle cells in the social cognition of apes and humans. In “Evolution of Nervous Systems,” Vol. 4 (J. H. Kaas and T. M. Preuss, eds.), pp. 479–484. Elsevier, London. Suggested Readings Allman, J. M. (1999). “Evolving Brains.” Freeman, New York. Butler, A. B., and Hodos, W. (1996). “Comparative Vertebrate Neuroanatomy.” Wiley-Liss, New York. Deacon, T. W. (1997). “The Symbolic Species: The Co-Evolution of Language and the Brain.” Norton, New York. Falk D., and Gibson, K. R. (2001). “Evolutionary Anatomy of the Primate Cerebral Cortex.” Cambridge University Press, Cambridge. Fleagle, J. G. (1999). “Primate Adaptation and Evolution,” 2nd ed. Academic Press, San Diego. Kaas, J. H. (2007). “Evolution of Nervous Systems,” 4 Vols. (J. H. Kaas series ed.). Elsevier, London. Northcutt, R. G. and Kaas, J. H. (1995). The emergence and evolution of mammalian neocortex. Trends Neurosci. 18, 373–379. Preuss, T. M., ed. (2000). “The Diversity of Cerebral Cortex.” Brain Behav. Evol. 55, 283–347. Preuss, T. M. (2004). What is it like to be a human? In “The Cognitive Neurosciences,” 3rd ed. (M. S. Gazzaniga, ed.), pp. 5–22. MIT Press, Cambridge, MA. Striedter, G. F. (2005). “Principles of Brain Evolution.” Sinauer Associates, Sunderland, MA. Jon H. Kaas and Todd M. Preuss VII. BEHAVIORAL AND COGNITIVE NEUROSCIENCE