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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
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© 2008, 2003, 1999 Elsevier Inc.
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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
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21 Tree shrews
20 Flying lemurs
19 Mega bats
18 Old world
microbats
17 New world
microbats
16 Pangolins Pholi
dot
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15 Cats, dogs Carnivo
ra
14 Rhinos,tapirs Perisso
dacty
horses
la
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22 Primates
es
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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
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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.
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Jon H. Kaas and Todd M. Preuss
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