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Revised view of the avian brain 103
Why Can Birds Be So Smart?
Background, Signicance, and Implications of the Revised View of the Avian Brain
Toru Shimizu
University of South Florida
In the early twentieth century, the anatomical nomenclature of the avian telencephalon (cerebrum) was developed on the
basis of awed assumptions about homology to mammals. The classic terminology implied that the majority of the avian
telencephalon was basically composed of nuclei forming massive basal ganglia which controlled only simple, unlearned
behavior. Later research revealed that this assumption was inaccurate and that the avian telencephalon contains a well-
developed pallium in addition to basal ganglia. The avian pallium is equivalent to specic mammalian counterparts (e.g.,
neocortex, claustrum, and/or amygdala) that are responsible for complex and sophisticated behavior. In 2002, based on a
revised interpretation of the avian brain organization, the new nomenclature was proposed by comparative neuroscientists
who participated in the Avian Brain Nomenclature Forum. This paper presents the general background and signicance of
the revised view of the avian brain, as well as implications for understanding the remarkable cognitive abilities of birds.
Avian brain research was started by a handful of comparative
neuroanatomists in the early twentieth century. From a rela-
tively small eld with a limited audience, it has evolved into
a major biological eld supported by a large sum of research
money. Many scientists are involved in avian research, not
only to study birds for intrinsic reasons, but also to use the
avian brain as a model to investigate general principles of
the nervous system with regard to behavior, development,
anatomy, physiology, and molecular biology (e.g., Notte-
bohm, 2002; Thanos & Mey, 2001; Zeigler & Bischof, 1993;
Zeigler & Marler, 2008). In particular, as data accumulate
to reveal the remarkable cognitive prociencies of birds –
prociencies that were traditionally considered to be the sole
province of the mammalian brain – avian models now play a
major role in studies about the neural mechanisms underly-
ing various cognitive functions, such as learning, memory,
attention, and consciousness (e.g., Bingman & Able, 2002;
Butler & Cortterill, 2006; Doupe & Kuhl, 1999; Watanabe
& Hofman, 2008). Therefore, it is essential that scientists
in avian and mammalian research communities can easily
exchange information about their discoveries and readily
understand the signicance of their respective ndings.
In the past, scientic communication between the avian
and mammalian research communities was not easy. One
substantive obstacle was the confusing terminology used
to describe some critical structures in the avian brain (Jar-
vis et al., 2005; Reiner et al., 2004). The terminology was
adopted about 100 years ago by the pioneers of compara-
tive neuroanatomy based on the classic view of vertebrate
brain evolution and awed assumptions about homology to
mammals. Later studies revealed that the classic view was
fundamentally false and that the terminology was inaccu-
rate and misleading. Although avian brain researchers real-
ized these mistakes in the mid-twentieth century, no changes
were made in the nomenclature until the twenty-rst century.
Toru Shimizu, Department of Psychology, University of
South Florida.
I am grateful to the participants of the Avian Brain Nomen-
clature Forum in 2002 for their efforts, with particular grati-
tude to Erich Jarvis and Anton Reiner for their leadership in
this endeavor. I am also grateful to Tadd B. Patton, Frank Fish-
burn, Verner P. Bingman, and two anonymous reviewers for
their valuable comments on the manuscript. The title of this
paper was inspired by Karin Isler and Carel P. Van Schaik’s ar-
ticle “Why are there so few smart mammals (but so many smart
birds)?” (Biology Letters, 2009, 5, 125-129).
Correspondence concerning this article should be addressed
to Toru Shimizu, PCD 4118G, University of South Florida, 4202
E. Fowler Avenue, Tampa, FL 33620-7200, U.S.A. E-mail:
shimizu@cas.usf.edu
Volume 4, pp 103-1152009
ISSN: 1911-#### doi: 10.####/ccbr.2009.300## © Toru Shimizu 2009
Revised view of the avian brain 104
In July 2002, after two years of preparation, a group of com-
parative neuroscientists gathered for an international forum
held at Duke University in North Carolina. The purpose
of the forum was to abandon the old nomenclature of cer-
tain brain structures and to develop new and more accurate
names for the avian brain. The participants included experts
on the avian brain, as well as others who are specialized for
mammals, reptiles, and other vertebrates. The forum includ-
ed presentations of various hypotheses about brain evolution
and proposals for possible new name options. After three
days of intensive discussion, the participants adopted the
new nomenclature. It was welcomed and accepted in the
scientic community and sparked renewed interests among
avian and mammalian brain researchers alike.
This paper rst presents the classic interpretation of the
evolution of the vertebrate brain and the old avian nomen-
clature based on the classic view. The updated modern in-
terpretation of brain evolution is then introduced with the
new nomenclature. Also discussed are the implications of
the modern view for understanding the cognitive abilities of
birds. Throughout the paper the question and answer for-
mat is used to facilitate accessibility to issues of individu-
al interest. For the same reason, limited anatomical terms
and jargon are presented only when necessary and in-depth
discussion about minor issues is avoided. More detailed
information about the 2002 Forum and the anatomical sig-
nicance of the new nomenclature are presented elsewhere
(Jarvis et al., 2005; Reiner et al., 2004).
The Classic View of the Avian Brain
Who developed the classic view and the old nomenclature?
The old nomenclature was developed by early compara-
tive neuroanatomists about 100 years ago. At the end of
the nineteenth century and the beginning of the twentieth
century, new histological techniques were developed, such
as staining methods for nervous tissues by German patholo-
gist Franz Nissl (1860 – 1919) and Italian physician Camillo
Golgi (1843 – 1926). The new methods allowed early re-
searchers to observe detailed images of nerve cells and bers
for the rst time in history. Ludwig Edinger (1855 – 1918)
in Germany was one of the rst researchers to use these
techniques. Other pioneers, such as J. B. Johnston, G. C.
Huber, E. C. Crosby, C. U. Ariëns Kappers, and C. J. Her-
rick, also began to study and compare the brains of a variety
of animals, including different shes, amphibians, reptiles,
birds, and mammals.
Anatomical examinations with the new techniques led
early neuroanatomists to formulate the classic view of verte-
brate brain evolution, in which the brain expanded from an
underdeveloped form of “lower” animal to a more advanced
form of “higher” animal. The avian brain was believed to
be a more primitive brain compared to the well-developed,
advanced mammalian brain. The avian telencephalic struc-
tures were named in accordance with this classic view. Ed-
inger and his students (Edinger, 1908; Edinger, Wallenberg,
& Holmes, 1903) proposed the original names which were
later modied by Ariëns Kappers and his colleagues (Ariëns
Kappers, Huber, & Crosby, 1936).
The old nomenclature by Ariëns Kappers et al. was main-
tained in the inuential stereotaxic atlas of the pigeon brain
by Harvey J. Karten and William Hodos (1967). Despite the
fact that Karten and Hodos disproved the classic view of the
vertebrate brain evolution, they believed that the benet of
continuing to use the familiar old nomenclature (with a few
exceptions) outweighed the possibility of making changes
that could cause confusion. Subsequent atlases for other
avian species essentially followed the terminology used in
the Karten and Hodos atlas (e.g., Kuenzel & Masson, 1988;
Stokes et al., 1974).
What were the most signicant aspects of the classic view
and the old nomenclature?
No avian brains are alike just as no mammalian brains
are exactly the same. There are considerable variations in
the development of different brain structures within birds.
Nevertheless, the fundamental design of the avian brain is
consistent among all birds. As in other vertebrates, the bird
brain consists of the hindbrain, midbrain, and forebrain (thal-
amus and telencephalon). The classic view of the bird brain
asserted that the avian hindbrain, midbrain, and thalamus
were highly homologous to those same regions in mammals,
but not the telencephalon. As shown in Figure 1, the basic
organization of the mammalian telencephalon consists of a
group of nuclei forming basal ganglia (e.g., dorsal striatum
and globus pallidus) at the telencephalic oor and a pallium
(“cloak” in Latin; e.g., neocortex and hippocampus) at the
mantle of the telencephalon enveloping the basal ganglia.
The central notion of the classic view stated that the avian
and mammalian telencephalons were fundamentally differ-
ent with the belief that the avian telencephalon essentially
consisted of gigantic basal ganglia and a meager pallium, as
depicted in Figure 2A.
It is perhaps useful to clarify the term homology at this
point. Homology is a central concept used to describe the
evolutionary relationship between traits found in different
animals. The term indicates that certain traits in different
species can be evolutionally traced back to those of their
common ancestor, regardless of appearance or function. The
classic view implied that the major part of the avian telen-
cephalon was homologous to the mammalian basal ganglia
– meaning that both structures presumably evolved from the
same basal ganglia region of their common ancestor (which
is called the stem amniote).
Revised view of the avian brain 105
The avian telencephalon contains anatomically distinct
subdivisions. In the old nomenclature, many of these sub-
divisions were sufxed with the term “striatum” to indicate
that these structures were part of the basal ganglia (Fig.
2A). The striatum is the term used to describe the striated
appearance of a large part (caudate-putamen) of the mam-
malian basal ganglia because of the ber bundles passing
through this region. Since the avian “striatal” structures do
not appear to be striated, the old nomenclature was obvious-
ly based on inferred homology with the mammalian basal
ganglia, not based on the histological features of the avian
telencephalon.
Why did early neuroanatomists believe that the avian tel-
encephalon comprised massive basal ganglia?
There are two main reasons that early neuroanatomists
named the avian telencephalic structures after the mamma-
lian basal ganglia “striatum.” One is the theoretical inuence
of the Aristotelian concept of phylogenetic scale, scala natu-
rae, and the other is the cytoarchitectonic characteristics of
the avian telencephalon.
Theoretical reason: The thinking of early neuroanato-
mists was greatly biased by the scala naturae-based concept,
which holds that living animals are ranked in a continu-
ous ascending order from “lower, primitive, less evolved”
animals to “higher, advanced, more evolved” animals. The
ascending order would lead from shes to amphibians, to
reptiles, to birds, to mammals, to primates, and nally to hu-
mans at the pinnacle. When Charles Darwin introduced his
idea of evolution, early neuroanatomists interpreted this to
mean that the brain evolution of vertebrates also occurred
as a unilinear or unidimensional process from a simple form
to a complex advanced form through the evolutionary lad-
der. They proposed a type of accretionary theory, in which
they believed that brains evolved from a primitive brain to a
complex one by adding “new” parts on top of the “old” parts.
The “old” brain was called the palaeoencephalon, which ba-
sically corresponded to the basal ganglia or striatum at the
base of the telencephalon. The “new” brain was termed the
neoencephalon, which corresponded to the pallium or cortex
at the top of the telencephalon. In this view, the “old” brain
could control only reexive and instinctual behavior where-
as the “new” brain could produce more advanced, learned,
and complex behavior.
Anatomical reason: The majority of the avian telencepha-
lon consists of nuclear grey matter which appears similar
to the mammalian basal ganglia. In these nuclear masses,
neurons are not organized in a laminar fashion, but aggregat-
ed as distinct clusters or nuclei. In mammals, such nuclear
masses (basal ganglia) are surrounded by a thin and large
sheet of nerve cells (cerebral cortex), where neurons are ar-
ranged parallel to the surface as layers or laminae. No such
large laminated neural architecture is apparent in the avian
and other non-mammalian brains, a fact that led to the as-
sumption that a developed cerebral cortex is a unique char-
acteristic of the mammalian telencephalon.
Another similarity of the avian telencephalon with the
mammalian basal ganglia is the topographical location of
these nuclear masses in the brain. The nuclear mass of the
avian telencephalon is ventrolateral to the lateral ventricle
just as the mammalian basal ganglia are positioned to this
ventricle. The relationship of the nuclear masses relative to
the lateral ventricle can be seen in transverse brain sections
(Figs. 1, 2).
How was the classic view reected in the old nomencla-
ture?
In the original nomenclature, there were four major “stria-
tal” regions in the avian telencephalon: paleostriatum, arch-
istriatum, neostriatum, and hyperstriatum. The prexes “pa-
leo-”, “archi-”, and “neo-” were used to indicate the inferred
evolutionary order of the emergence of these structures.
According to the classic view, the oldest part of the avian
telencephalon was the paleostriatum; then the archistriatum
and the neostriatum evolved; and nally the hyperstriatum
Figure 1. A schematic gure showing a transverse telence-
phalic section of the right hemisphere of the rat. The red
portion represents the pallium; the blue portion represents
the striatal part of the basal ganglia; the green portion rep-
resents the pallidal part of the basal ganglia; and the black
portion represents the lateral ventricle. Note. From Figure
1, “Revised nomenclature for avian telencephalon and some
related brainstem nuclei,” by A. Reiner et al., Journal of
Comparative Neurology, 2004, 473, p. 380. Copyright 2004
by the John Wiley & Sons, Inc. Adapted with permission.
Revised view of the avian brain 106
emerged, which was considered to be the newest portion.
As Figure 2A shows, each “striatal” subdivision was further
divided into more subregions based on cytoarchitecture.
Paleostriatum: In the classic view, the paleostriatum
(“oldest” striatum) was found in all vertebrates including
shes. The sh paleostriatum was named the primitivum
(old part) and was believed to correspond to the mammalian
globus pallidus (a part of the basal ganglia). In reptiles and
birds, the paleostriatum developed further and differentiated
into two parts by adding an augmentatum region above the
primitivum.
Archistriatum: As amphibians evolved from shes, the
archistriatum (“old” striatum) emerged. It was positioned
above the paleostriatum, and was proposed to be a primitive
amygdala. This nucleus was located most caudally in the
avian telencephalon and therefore it is not included in Figure
2A.
Neostriatum: A “new” part above the paleostriatum and
archistriatum was called the neostriatum, which was not
present in shes, but was found in amphibians and expand-
ed signicantly in reptiles and birds. The neostriatum was
considered to correspond to the caudate-putamen part of the
mammalian basal ganglia. Although not shown in Figure
2A, the neostriatum was further divided into three regions
along the anterior-posterior axis: the neostriatum frontale,
intermediale, and caudale. Later studies revealed that sev-
eral distinct sensory-specic nuclei were embedded in the
neostriatum, most notably the visual ectostriatum and audi-
tory Field L (Karten, 1969). The presence of the sensory nu-
clei was a compelling observation that the avian neostriatum
was more than simply basal ganglia.
Hyperstriatum: The hyperstriatum (“hypertrophied” stria-
tum) was believed to be an overgrown striatum, which ex-
isted only in birds, but no other animals. It was divided into
several subregions including a ventrally located ventrale and
a dorsally located accessorium. The hyperstriatum ventrale
is nuclear, as are most “striatal” structures. Despite the “stri-
atal” name, the hyperstriatum accessorium was regarded as a
pallial structure by early neuroanatomists. This region has a
laminated neural organization, although it is not six-layered
like the mammalian neocortex. Edinger and his colleagues
(1903) named this part the ‘cortex frontalis’ and it was later
renamed as the hyperstriatum accessorium by Ariëns Kap-
pers et al. (1936). It was (and is) also called the wulst (from
a German word for “bump”) because it is an elevation on the
most dorsal surface of the telencephalon.
Figure 2. Schematic gures showing transverse telencephalic sections of the right hemispheres of the pigeon according to
the classic interpretation (A) and the modern interpretation (B). The red portions represent the pallium; the blue portions
represent the striatal parts of the basal ganglia; the green portions represent the pallidal parts of the basal ganglia; and
the black portions represent the lateral ventricles. Subdivisions in the avian telencephalon are identied using (A) the old
nomenclature (Ariëns Kappers et al., 1936; Karten & Hodos, 1969) and (B) the new nomenclature adopted by the Avian
Brain Nomenclature Forum in 2002 (Jarvis et al., 2005; Reiner et al., 2004). Note. From Figure 1, “Revised nomenclature
for avian telencephalon and some related brainstem nuclei,” by A. Reiner et al., Journal of Comparative Neurology, 2004,
473, p. 380. Copyright 2004 by the John Wiley & Sons, Inc. Adapted with permission.
Revised view of the avian brain 107
How did the classic view explain the cognitive abilities of
birds?
Only limited information about animal cognition was
available in the late nineteenth century and early twentieth
century with often excessively anthropomorphistic, unreli-
able anecdotes (Romanes, 1882). Due to the lack of sci-
entic data, early neuroanatomists (Ariëns Kappers et al.,
1936; Edinger, 1908; Edinger et al., 1903; Herrick, 1956)
and comparative biologists (Lloyd Morgan, 1894) consider-
ably underestimated the cognitive abilities of non-mammals.
Ironically, the misconception about animal behavior and
cognition was somewhat consistent with the classic view
of brain evolution. Early scientists believed that mammals
were capable of complex and intelligent behavior because
only mammals had a well-developed pallium. According to
the classic view, the pallial region of mammals evolved to
expand in size and complexity and eventually resulted in an
elaborated six-layered neocortex, the newest and thus most
advanced brain structure. In contrast, birds, as well as other
non-mammals, were presumed to be controlled by reexes
and instincts because their brains consisted of primarily bas-
al ganglia and a diminutive pallium.
The Modern View of the Avian Brain
Who developed the modern view and the new nomencla-
ture?
In the mid-twentieth century, comparative neuroscientists
including Karten and Hodos started to realize that the clas-
sic view of the avian brain was inaccurate and that the old
nomenclature was misleading (e.g., Karten, 1969; Karten &
Hodos, 1967). Gradually the modern interpretation of the
avian brain was developed in the updated framework of ver-
tebrate brain evolution. Despite this major shift in think-
ing, these scientists kept using the old nomenclature until the
early twenty-rst century, because the old nomenclature had
been entrenched in avian research for many decades. Some
researchers wanted to maintain the same nomenclature for
consistency. Others, who were more open to name changes,
could not reach a consensus on alternative terminology be-
cause there were various possible term options based on dif-
ferent hypotheses about the organization of the avian brain.
The new nomenclature was nally developed by the Avian
Brain Nomenclature Forum in 2002 (Jarvis et al., 2005;
Reiner et al., 2004). The participants included 28 compara-
tive neuroscientists, representing multidisciplinary exper-
tise, who are respected leaders in their research elds. The
names of the participants are available as the authors of the
two ofcial papers (Jarvis et al., 2005; Reiner et al., 2004).
Among them, the key players were Erich D. Jarvis at Duke
University, who envisioned the value of such a forum and
was the main organizer, and Anton Reiner at the University
of Tennessee, Memphis, who was the forerunner in this en-
deavor, having worked on the nomenclature issue since the
late 1990’s. In addition, many other scientists participated
in preparatory discussions through e-mail communications
during the two years prior to the Forum. Today, the new
nomenclature that was proposed by the 2002 Forum is gen-
erally well-accepted in the scientic community, including
avian researchers who did not participate in the Forum. The
ofcial nomenclature papers (Jarvis et al., 2005; Reiner et
al., 2004) have been cited over 400 times since they were
published.
What are the most signicant aspects of the modern view
and the new nomenclature?
Based on updated data, the modern view of vertebrate
brain evolution refutes the classic view. In the new interpre-
tation, all vertebrates share the same basic design of telen-
cephalic organization, which consists of both a pallium and
basal ganglia. The pallium of non-mammals like birds was
mistaken to be a part of the basal ganglia because it did not
show the same neural architecture (i.e., a laminar arrange-
ment) as the mammalian pallium – a six-layered neocortex.
This means that the avian telencephalon is not simply hy-
pertrophied basal ganglia. Of all the “striatal” structures in
the old nomenclature, only a small portion (i.e., “paleostria-
tum”) is homologous to the mammalian basal ganglia. The
remaining “striatal” parts derive from the pallial region of
the developing telencephalon despite their non-laminated
appearance. As shown in Figure 2B, about 75% of the entire
telencephalic volume is now considered to be pallial (Jarvis
et al., 2005).
The revision of the terminology became necessary be-
cause, by the end of the twentieth century, misconceptions
about the bird brain due to the old terminology became too
prevalent and common in the mammalian research commu-
nity. In past research papers, it was not unusual to nd mam-
malian researchers who incorrectly compared the whole avi-
an telencephalon to the mammalian basal ganglia and who
falsely assumed that birds without an enlarged, developed
pallium were decient in sophisticated neural computation
and cognitive abilities. Although avian research ourished
in many biological and psychological elds, the old nomen-
clature often impeded an easy exchange of information be-
tween avian and mammalian researchers.
During the 2002 Forum, terms were selected to represent
the updated understanding of the avian brain and the correct
homologies with the mammalian brain. The sufx “stria-
tum” was removed from many telencephalic structures that
were discovered to be pallial in nature. These structures
were renamed with the sufx “pallium.” The prexes that
Revised view of the avian brain 108
view is considered false is that new anatomical information
became available due to methodological development in
neurochemistry, hodology (the study of neural connections),
and molecular biology. For instance, using new histochemi-
cal techniques, the distribution of dopamine was analyzed
to compare mammals and birds (Jurio & Vogt, 1967). In
the mammalian basal ganglia, dopamine is abundant in the
caudate-putamen (striatum) compared to the cerebral cortex.
If the majority of the avian telencephalon was a striatum – as
the classic view suggested – dopamine should be found in all
the “striatal” regions in the avian telencephalon. Research
shows that only a small part of the telencephalon (the paleo-
striatum augmentatum) contains a high level of dopamine.
Similar results were obtained regarding the distributions of
other neurochemicals (e.g., acetylcholinesterase, substance
P, and enkephalin) to conclude that only the paleostriatum
augmentatum is equivalent to the mammalian caudate-pu-
tamen and that the paleostriatum primitivum corresponds to
the globus pallidus (Karten, 1969; Reiner, Medina, & Veen-
man, 1998). The conclusion is reinforced by hodological
and molecular evidence. Tract-tracing studies revealed that
the connection patterns of the paleostriatum with other brain
structures (e.g., midbrain and hindbrain) are similar to those
of the mammalian basal ganglia (Brauth & Kitt 1980; Karten
& Dubbeldam, 1973; Reiner, Brauth, & Karten, 1984). Em-
bryonic molecular studies supported the same conclusion
that the avian paleostriatum is homologous to the mamma-
lian basal ganglia in terms of the expression of certain genes
(Marin & Rubinstein, 2001; Puelles et al., 2000).
Behavioral evidence: The classic view presumed that non-
mammals like birds could only perform unlearned, instinc-
tual behavior because the majority of their telencephalon
was striatal. In this view, birds with a relatively small pal-
lium were not able to behave like mammals that could enjoy
complex and sophisticated behavior owing to the presence
of a large neocortex. For the past 50 years, a new picture
about the cognitive abilities of birds has emerged using sci-
entically rigorous methods (Wasserman & Zentall, 2006).
Some of the complex behaviors of birds are considered to
be comparable to those of primates (Emery, 2006). Pigeons
can memorize and discriminate more than 700 photographs
(Cook, Levison, Gillett, & Blaisdell, 2005) and discrimi-
nate between the paintings of cubistic and impressionistic
styles of painting (Watanabe, Sakamoto, & Wakita, 1995).
Songbirds, parrots, and hummingbirds show the abilities
of complicated vocal learning (Doupe & Kuhl, 1999; Jar-
vis et al., 2000; Pepperberg, 1999). Starlings can be trained
to acquire recursion grammar which had been considered to
be unique to human language (Gentner, Fenn, Margoliash,
& Nusbaum, 2006). New Caledonian crows manufacture
hook-tools with their bills and use them to search for prey in
holes in tree trunks (Hunt, 1996). Scrub-jays appear to form
episodic-like memory about a previous experience (Clayton
made inaccurate references to the evolutionary relationship
of structures (“paleo-”, “archi-”, “neo-”) were also eliminat-
ed.
Why do contemporary neuroscientists conclude that the
classic view is false?
Up until the mid-twentieth century, the classic view of the
evolution of the vertebrate brain widely prevailed. Although
there were early researchers who voiced their dissenting
opinions against the classic view (Holmgren, 1925; Käl-
lén, 1953; Kuhlenbeck, 1938; Rose, 1914), their views were
not predominant. Eventually, later researchers were able to
refute the classic view based on three lines of compelling
arguments: 1) theoretical, 2) anatomical, and 3) behavioral
evidence.
Theoretical evidence: The rst reason is the updated un-
derstanding of vertebrate evolution. Comparative neurosci-
entists accepted the revised and accurate view of vertebrate
brain evolution based on analyses of fossil records and com-
parative phyletic studies. Instead of a unilinear or unidimen-
sional process, evolution is characterized by divergence and
multi-linearity (Butler & Hodos, 2005; Campbell & Hodos,
1991; Hodos & Campbell, 1969; Northcutt, 1981).
These characteristics are seen in Figure 3, illustrating the
currently accepted evolutionary relationships among tetra-
pods (amphibians, reptiles, birds, and mammals) (Carroll,
1988). Briey, ancestral tetrapods diverged from one group
of bony sh in the Devonian period about 400 million years
ago (MYA). Tetrapods then gave rise to stem amniotes,
which further diverged into two major amniote groups by the
end of the Carboniferous period. They were synapsids and
diapsids, the ancestors of mammals and birds respectively.
Synapsids comprise two successive orders, pelycosaurs and
then therapsids. From the latter, early mammals arose in
the Late Triassic period more than 200 MYA. Diapsids be-
came the ancestors of the majority of living reptiles. The lin-
eage of diapsids diverged several times to produce multiple
groups, including dinosaurs, which were the most successful
vertebrates for more than 150 million years, beginning in
the Later Triassic period to the end of the Cretaceous period.
Birds arose most likely 140 MYA from the saurichian dino-
saurs in the Late Jurassic period.
Hence, unlike birds, mammals did not evolve from ances-
tral reptiles. The ancestors of mammals (synapsids) were
stem amniotes, which were also the ancestors of reptiles and
birds. The lineages leading to mammals and birds are sepa-
rate since synapsids and diapsids diverged from stem amni-
otes about 300 MYA. This means that each of the avian and
mammalian brains has an independent evolutionary history
of millions of years. The avian and reptilian brains are not
primitive, undeveloped versions of the mammalian brain.
Anatomical evidence: The second reason that the classic
Revised view of the avian brain 109
& Dickinson, 1998), upon which they can behave as if they
have predictions for the future (Clayton, Bussey, & Dickin-
son, 2003).
What are the major changes in the nomenclature?
During the 2002 Forum, new names were adopted for
over 30 brain areas. The majority of changes were made for
the telencephalic structures. Figure 2B represents the main
changes in the nomenclature for the telencephalon.
Paleostriatum - Lateral Striatum and Globus Pallidus:
The avian paleostriatum augmentatum and primitivum were
renamed as the lateral striatum and globus pallidus, respec-
tively. The avian lateral striatum is considered to be equiva-
lent to the mammalian dorsal striatum (caudate-putamen),
whereas the avian globus pallidus corresponds to the mam-
malian counterpart with the same name.
Archistriatum - Amygdala and Arcopallium: The archistri-
atum became the arcopallium (arched pallium). Parts of the
archistriatum were also renamed as the amygdala to indicate
that they belong to the amygdaloid complex.
Neostriatum - Nidopallium: The neostriatum became the
nidopallium. The term “nido-” means a nest, which implies
that this structure contains several anatomically distinct and
functionally different nuclei, such as the visual ectostriatum
and the auditory Field L. The ectostriatum was renamed as
the entopallium and Field L maintained the same name.
Hyperstriatum - Mesopallium and Hyperpallium: In the
hyperstriatum, the accessorium was renamed as the hyper-
pallium (hypertrophied pallium) whereas the ventrale be-
came the mesopallium (middle pallium). The hyperpallium
and mesopallium obtained different names because they are
distinguishable cytologically, chemically, hodologically,
functionally, and developmentally. The hyperpallium was
regarded as pallial by early neuroanatomists and this inter-
pretation was supported by the 2002 Forum participants. It
is believed to be homologous to part of the mammalian neo-
cortex.
Dorsal Ventricular Ridge: The nidopallium, arcopallium,
and the mesopallium are together designated as the dorsal
ventricular ridge (DVR), a voluminous nuclear mass pro-
truding into the lateral ventricle (Ulinski, 1983). Although
the origin of the DVR was proposed to be striatal (i.e., basal
ganglia) in the classic view, it is now considered to be palli-
al. The DVR is also found in reptiles, yet the reptilian DVR
is not as enlarged or as differentiated as the avian one.
Brainstem: At least nine structures in the brainstem ob-
tained new names based on the updated information. For
example, one of the brainstem structures is a cell group tra-
ditionally called the nucleus tegmenti pedunculo-pontinus,
pars compacta (TPc) in the midbrain (Karten & Hodos,
1967). The TPc name was based on the location and den-
sity of the cell group because there was then no other in-
formation about the nucleus. Later anatomical, chemical,
and physiological investigations revealed that TPc is directly
comparable to the substantia nigra pars compacta (SNc) of
mammals. Most notably, just like SNc, TPc sends major
dopaminergic projections to the avian counterpart of the
striatal region of the basal ganglia (Kitt & Brauth, 1986a,
b; Reiner et al., 2004). The participants of the 2002 Forum
decided that the common name SNc should be adopted to
clarify the homologous relationship between these nuclei.
Why is the nuclear pallium (DVR) categorized as a pallium
despite its non-laminar organization?
In mammals, the term pallium is often used synonymously
with a six-layered neocortex. Although the neocortex is the
largest structure derived from the pallial sector of the devel-
oping telencephalon, the pallium cannot be solely dened as
a six-layered laminar conguration. There are other pallial
structures in the mammalian brain that are laminated with
Figure 3. Probable phylogenetical relationships of bony shes, amphibians, reptiles, birds, and mammals. MYA: million
years ago. Note. From Figure 2, “Avian brains and a new understanding of vertebrate brain evolution,” by E.D. Jarvis et
al., Nature Reviews Neuroscience, 2005, 6, p. 156. Copyright 2005 by Nature Publishing Group. Adapted with permission.
Revised view of the avian brain 110
fewer than six layers, and still others that are not laminated
at all. Both the olfactory (piriform) cortex and hippocam-
pus have pallial origins, and are laminated with two to three
layers (Fig. 1). Recent studies showed that nuclear (non-
laminar) structures like the claustrum and lateral parts of the
amygdala (Fig. 1) also develop from the embryonic pallium
(Puelles et al., 2000; Swanson, 2000; see also Holmgren,
1925).
The DVR (the nidopallium, arcopallium, and mesopal-
lium) occupies a large part of the avian telencephalon and is
not organized in a laminar fashion. With a cursory glance,
no such huge nuclear structure is recognizable in the mam-
malian pallium. Nevertheless, the avian DVR and hyperpal-
lium are considered to be pallial since they show important
characteristics similar to the mammalian pallium – neocor-
tex, claustrum, and amygdala – in terms of anatomy and
function (Karten, 1969; Puelles et al., 2000; Reiner et al.,
1998).
Anatomical characteristics: There has been a voluminous
amount of hodological studies since the 1960s that showed
that the connection patterns of the avian DVR and hyperpal-
lium are similar to the mammalian pallium (Shimizu, 2001).
The sensory pathways connecting the thalamus and telen-
cephalon have especially been studied extensively. These
studies demonstrated that distinct cell groups in the DVR
(the nidopallium, in particular) and hyperpallium receive
massive afferent projections from visual, auditory, somato-
sensory, and related nuclei in the dorsal thalamus. This
pattern of projections is similar to the pattern in the mam-
malian brain, in which distinct modality-specic regions
within the pallium (the neocortex, in particular) receive dif-
ferent sensory projections from the dorsal thalamic nuclei
(Karten, 1969; Karten & Shimizu, 1989; Shimizu & Bow-
ers, 1999). In the avian brain, these primary sensory areas
then send projections to multiple nuclei in the telencephalon
to form closely interconnected circuits for further process-
ing (Doupe & Kuhl, 1999; Husband & Shimizu, 1999). As
for motor output from the telencephalon, both the DVR (the
arcopallium, in particular) and hyperpallium give rise to
long descending efferent projections to motor nuclei in the
brainstem and spinal cord. The projection pattern is reminis-
cent of the cortico-bulbar and cortico-spinal pathways from
the mammalian neocortex (Wild & Williams, 2000; Zeir &
Karten, 1971). Embryological and developmental molecu-
lar studies also show similarities between the mammalian
and avian pallia (Puelles et al., 2000; Smith-Fernandez et al.,
1998). During embryogenesis, pallial-specic transcription
factors, such as EMX1, PAX6, and TBR1, are present in the
DVR and hyperpallium, which is also true for the mamma-
lian pallium.
Functional characteristics: In mammals, the neocortex
plays an essential role in a variety of activities, including
sensation, perception, motor control, and cognition. Simi-
larly, the avian pallium is crucially involved in sensory pro-
cessing, such as visual analysis (Bischof & Watanabe, 1997;
Hodos, 1993; Patton, Husband, & Shimizu, 2008) and audi-
tory analysis (Jarvis, Mello, & Nottebohm, 1995; Mello &
Clayton, 1994) according to behavioral, physiological, and
gene expression studies. There are also ample data showing
that these regions are important for the production of highly
complex behavior, such as learning, memory, and attention
(Güntürkün & Durstewitz, 2001; Horn, 1985; Iwaniuk &
Hurd, 2005; Knudsen, 2002; Lefebvre, Reader, & Sol, 2004;
Mello, 2002; Nottebohm, Stokes, & Leonard, 1976; Sadan-
anda, Korte, & Bischof, 2007; Scharff & Nottebohm, 1991;
Shimizu & Hodos, 1989). For instance, songbirds have
distinct neural circuits in the pallium (and basal ganglia)
to learn and produce species-specic songs for communi-
cation (Nottebohm et al., 1976). Several pallial structures
are directly involved in lial imprinting learning of preco-
cial birds (e.g., ducks and chickens) (Horn, 1985) and sexual
imprinting of nches (Rollenhagen & Bischof, 2000). The
caudolateral nucleus of the nidopallium has been compared
to the mammalian prefrontal cortex (Güntürkün & Durstew-
itz, 2001). Behavioral and physiological studies show that
this nucleus plays a major role in working memory, which
is used to store and manipulate information for a short time
period to achieve behavioral goals. The size of the DVR
appears to be larger in some avian species, such as crows
and parrots (Iwaniuk & Hurd, 2005; Lefebvre et al., 2004),
which may be related to their ability to exhibit complex be-
havior more frequently than other birds (Emery, 2006; Hunt,
1996; Pepperburg, 1999).
What is the nuclear pallium (DVR) homologous to in the
mammalian pallium?
The terms hyperpallium, mesopallium, nidopallium, and
arcopallium exist only in the avian brain nomenclature, and
no other animals have such structures with the same names.
During the development of the new nomenclature, some
specic names for mammalian pallial structures (e.g., cor-
tex, neocortex) were intentionally avoided for use with the
avian DVR. This is because the participants of the 2002 Fo-
rum could not reach a consensus about which specic struc-
tures of the mammalian pallium (i.e., neocortex, claustrum,
or amygdala) correspond to the avian pallium. There are
diverse hypotheses regarding the homology of the DVR with
the mammalian pallium (Bruce & Neary, 1995; Butler, 1994;
Karten 1969, 1991; Karten & Shimizu, 1989; Northcutt
& Kaas, 1995; Puelles et al., 2000; Reiner, 1991; Reiner,
Yamamoto, & Karten, 2005; Striedter, 1997). The two main
hypotheses will be presented next. In these hypotheses, the
DVR is compared to either the neocortex or the claustrum/
amygdala of the mammalian pallium.
Neocortex: One possibility is that some neurons in the
Revised view of the avian brain 111
avian DVR correspond to those in the mammalian neocor-
tex. Massive thalamo-nidopallial projections are similar to
the connection patterns of the thalamo-neocortex in mam-
mals, and subsequent intrinsic circuits within the avian DVR
(i.e., nidopallium, mesopallium, and arcopallium) are simi-
lar to those between layers in the neocortex (Karten 1969,
1991; Karten & Shimizu, 1989). This hypothesis proposes
that some neurons of individual cell populations in the DVR
are equivalent to neurons in different layers of the mamma-
lian neocortex, despite the lack of a laminar organization of
the DVR as a whole. Several gene expression studies are
consistent with this hypothesis. For instance, certain genes
(the steroid transcription factor ROR-β and the potassium
channel EAG2) are expressed in neurons of layer IV of the
mammalian neocortex that receives thalamic input. Some of
the same genes are also found in specic regions in the DVR
(i.e., the entopallium and Field L) which receive projections
from the sensory thalamic nuclei (Dugas-Ford & Ragsdale,
2003). Several other researchers have supported and modi-
ed this hypothesis (e.g., Butler, 1994; Reiner, 1991; Reiner
et al., 2005).
Claustrum/Amygdala: It is also possible that neurons of
the avian DVR are equivalent to those in non-laminar por-
tions of the mammalian pallium – the claustrum and amyg-
dala in particular. The claustrum is a thin sheet of grey mat-
ter lying between the outer surface of the basal ganglia and
the inner surface of the lateral portion of the neocortex (Fig.
1). It is found in marsupials and placental mammals (Butler,
Molnár, & Manger, 2002) and some monotremes (Ashwell,
Hardman, & Paxinos, 2004). The mammalian amygdala is
located in the tip of the temporal lobe and consists of mul-
tiple distinct subdivisions including pallial (lateral anterior
and basolateral nuclei) and subpallial portions (Swanson &
Petrovich, 1998). The claustrum and pallial amygdala have
been compared to the avian DVR based on nuclear appear-
ance, lateral location, and connection patterns with the thala-
mus and brainstem nuclei (Bruce & Neary, 1995; Striedter,
1997). Based on developmental expression of homeobox
genes (EMX1 and PAX6), the nidopallium is suggested to
correspond to the mammalian ventral claustrum and lateral
anterior amygdala, whereas the mesopallium corresponds to
the dorsal claustrum and basolateral amygdala (Puelles et
al., 2000).
Neither hypothesis seems to be awless since either does
not satisfactorily explain all anatomical data available today.
Subsequent gene expression studies also revealed evidence
against each of these two hypotheses (Gorski et al., 2002;
Haesler et al., 2004). Some authors ponder the possibility
that the two hypotheses may not be mutually exclusive. But-
ler and Molnár proposed an alternative hypothesis that the
avian DVR is homologous to both the mammalian neocortex
and claustrum/amygdala as derivatives of a common embry-
onic eld (Butler & Molnár, 2002; Molnár & Butler, 2002).
Further studies about both the avian and mammalian pal-
lial structures are clearly warranted to clarify the nature of
the DVR and to identify the mammalian counterpart. The
avian DVR is a large and heterogeneous structure contain-
ing sensory-specic and non-sensory regions. Certainly,
more anatomical and functional information is needed about
the non-sensory regions, which have been scarcely studied
compared to the regions directly associated with sensory
processing. In the mammalian pallium, almost nothing is
known about the function of the claustrum which has been
suggested to be involved in the generation and control of
consciousness (Crick & Koch, 2005).
How does the revised view of the avian brain explain the
cognitive abilities of birds?
Almost daily, new information is learned about the com-
plex behavior of non-human animals – behavior that was tra-
ditionally considered to be uniquely human. Novel discov-
eries of animal cognition are no longer surprising because
they are consistent with the modern, revised interpretations
of the vertebrate brain.
In the particular case of birds, the modern view of the
avian brain provides several insights regarding their highly
sophisticated behavior and underlying neural systems. First,
the revised view supports the assumption that the existence
of a developed higher brain structure – the pallium – is di-
rectly related to the production of exible, learned, and com-
plex behavior. The cognitive abilities of birds are difcult
to explain from the mammalian-centric classic view of the
vertebrate brain evolution. This is because avian (and other
non-mammalian) brains were believed to lack the sufcient
hardware (a large laminated pallium or neocortex) necessary
to carry out complex behavior. The modern interpretation
states that the avian nuclear pallium is as anatomically de-
veloped and as functionally sophisticated as the mammalian
laminar pallium. Indeed, of all living vertebrates, birds and
mammals have proportionally large telencephalons com-
pared to any other animals due to the enlarged pallial region
of each (Northcutt, 1981). It is reasonable to assume that as
the avian pallium became enlarged and elaborated, despite
its non-laminated conguration, birds evolved to perform
remarkably complex behavior.
Second, an important insight resulting from the modern
view is that the evolutionary origins of the complex behav-
ior of birds and mammals are most likely different. In oth-
er words, birds and mammals independently evolved with
elaborated neural systems to generate similarly complex
behavior (Emery, 2006; Shimizu, 2001, 2007). The con-
vincing evidence to support this argument is that the devel-
opments of the avian and mammalian pallia were separate
(yet parallel) events in evolution. According to endocasts
of extinct animals, stem amniotes (the common ancestor of
Revised view of the avian brain 112
reptiles, birds, and mammals) in the Early Carboniferous pe-
riod had only a slender, elongated forebrain with no signs of
the pallial enlargement found in living birds and mammals
(Hopson, 1979; Ulinski, 1983). In the lineage leading mam-
mals, endocasts of early synapsids show that their forebrain
remained diminutive. Only early mammals of the Jurassic
period started to show an enlarged forebrain, which was
most likely correlated with the development of the cerebral
cortex. A gradual, but not necessarily impressive, expan-
sion of the reptilian forebrain was seen in the Late Triassic
period. The forebrain became substantially enlarged only
when birds emerged, suggesting that the signicant develop-
ment of the nuclear DVR occurred during the reptile-bird
transition. These observations about the distinct and sepa-
rate evolutions of the pallia in birds and mammals suggest
that their complex behaviors (as products of the enlarged and
elaborated pallia) also have distinct and separate evolution-
ary origins (Shimizu, 2001, 2007).
Finally, the modern view raises a question regarding the
indispensability of the laminated neural architecture for
the generation of complex behavior. In humans and other
mammals, a six-layered neocortex seems essential to accom-
plish complex behavior, and thus a lamination is often pre-
sumed to be the most optimal design for sophisticated neu-
ral computation. It is easy to refute this assertion since not
all mammals appear to exhibit complex behavior, whereas
many birds show such behavior without a six-layered neo-
cortex. The presence of a six-layered neocortex does not
guarantee the generation of behavioral complexity, which
can be achieved by an alternative design – a nuclear pal-
lium (DVR). In fact, the interconnections among specic
brain structures may be more important than the presence of
a tightly layered architecture (Jarvis et al., 2004; Shimizu,
2001, 2007). I hasten to state that this argument is not meant
to underestimate the advantage of a laminar organization.
The lamination is probably one of the most efcient designs
to process topographically mapped information. All verte-
brates, including non-mammals, have many laminated brain
structures, such as olfactory bulb, retina, and midbrain. The
avian optic tectum of the midbrain is particularly large and
differentiated. Although the tectum appears to be less di-
rectly involved in cognitive prociencies and complex be-
havior compared to the pallium, the tectum and DVR have
close anatomical and functional connections with each other
(Shimizu, 2001, 2007).
Why can birds be so smart?
In other words, how is it possible for birds to behave in
surprisingly intricate and exible ways? The modern view of
brain evolution provides a proximate explanation. In short,
birds, like mammals, have developed a high-level forebrain
structure – an enlarged and elaborated pallium – that is nec-
essary to support such remarkable behavior. The caveat is
that the avian pallium and mammalian counterpart are mark-
edly different in terms of the architectural organization of
neurons (i.e., nuclear vs. laminar). Although both types of
pallium are capable of generating behavioral complexity,
the exact signicance of the anatomical differences on the
underlying cognitive processes remains vastly unexplored
(Butler & Cortterill, 2006; Güntürükün & Durstewitz, 2001;
Shimizu & Bowers, 1999). Even when birds and mammals
exhibit similarly complex behavior, it is possible that the
DVR and neocortex involve qualitatively dissimilar compu-
tational principles and mechanisms to generate such behav-
ior. Without more information about the two types of pallial
organization, it is still presumptuous to assume that the su-
percial similarity of behavior between birds and mammals
is attributable to an essentially identical kind of underlying
process.
Concluding Question
What are the main lessons that comparative cognitive and
behavioral researchers can learn from the history of com-
parative neuroscience?
Perhaps the important lesson for researchers of animal
cognition and behavior is that the true nature of vertebrate
evolution – divergence and multi-linearity – needs to be
adamantly reasserted in the course of comparative investiga-
tions. Researchers should resist the temptation to fall back
on the familiar scala naturae-based views. The mammalian-
centric or anthropomorphic perspective, which has persis-
tently permeated comparative research despite the scientic
evidence, must be avoided (Campbell & Hodos, 1991; Hodos
& Campbell, 1969; Wynne, 2007). The early comparative
neuroanatomists who subscribed to such an assumption un-
intentionally set in motion the misguided nomenclature that
lasted about 100 years. With this lesson from comparative
neuroscience in mind, the cognition and behavior of animals
should be evaluated within the framework of the multi-linear
evolution, and not on the basis of an ascending continuum
toward mammals and humans. The complex cognitive and
behavioral abilities of birds which have enabled their suc-
cessful adaptation to the environment should be appreciated
in their own right, not because they resemble some aspects
of human behavior and cognition. The “bird brain” – despite
the rather insulting colloquial connotation of the term – is a
truly unique exceptional machine deserving of our respect.
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