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Why Can Birds Be So Smart? Background, Significance, and Implications of the Revised View of the Avian Brain

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In the early twentieth century, the anatomical nomenclature of the avian telencephalon (cerebrum) was developed on the basis of flawed 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 welldeveloped pallium in addition to basal ganglia. The avian pallium is equivalent to specific 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 significance of the revised view of the avian brain, as well as implications for understanding the remarkable cognitive abilities of birds.
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Revised view of the avian brain
103
2009
Volume 4, pp 103-115
Why Can Birds Be So Smart?
Background, Significance, 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 flawed 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 specific 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 significance 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 Zeigler & Marler, 2008). In particular, as data accumulate
neuroanatomists in the early twentieth century. From a rela- to reveal the remarkable cognitive proficiencies of birds –
tively small field with a limited audience, it has evolved into proficiencies that were traditionally considered to be the sole
a major biological field supported by a large sum of research province of the mammalian brain – avian models now play a
money. Many scientists are involved in avian research, not major role in studies about the neural mechanisms underly-
only to study birds for intrinsic reasons, but also to use the ing various cognitive functions, such as learning, memory,
avian brain as a model to investigate general principles of attention, and consciousness (e.g., Bingman & Able, 2002;
the nervous system with regard to behavior, development, Butler & Cortterill, 2006; Doupe & Kuhl, 1999; Watanabe
anatomy, physiology, and molecular biology (e.g., Notte- & Hofman, 2008). Therefore, it is essential that scientists
bohm, 2002; Thanos & Mey, 2001; Zeigler & Bischof, 1993; in avian and mammalian research communities can easily
exchange information about their discoveries and readily
Toru Shimizu, Department of Psychology, University of
understand the significance of their respective findings.
South Florida.
In the past, scientific communication between the avian
I am grateful to the participants of the Avian Brain Nomen-
and mammalian research communities was not easy. One
clature Forum in 2002 for their efforts, with particular grati-
substantive obstacle was the confusing terminology used
tude to Erich Jarvis and Anton Reiner for their leadership in
to describe some critical structures in the avian brain (Jar-
this endeavor. I am also grateful to Tadd B. Patton, Frank Fish-
vis et al., 2005; Reiner et al., 2004). The terminology was
burn, Verner P. Bingman, and two anonymous reviewers for
adopted about 100 years ago by the pioneers of compara-
their valuable comments on the manuscript. The title of this
tive neuroanatomy based on the classic view of vertebrate
paper was inspired by Karin Isler and Carel P. Van Schaik’s ar-
brain evolution and flawed assumptions about homology to
ticle “Why are there so few smart mammals (but so many smart
mammals. Later studies revealed that the classic view was
birds)?” (Biology Letters, 2009, 5, 125-129).
fundamentally false and that the terminology was inaccu-
Correspondence concerning this article should be addressed
to Toru Shimizu, PCD 4118G, University of South Florida, 4202 rate and misleading. Although avian brain researchers real-
E. Fowler Avenue, Tampa, FL 33620-7200, U.S.A. E-mail:
ized these mistakes in the mid-twentieth century, no changes
shimizu@cas.usf.edu
were made in the nomenclature until the twenty-first century.
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- be a more primitive brain compared to the well-developed,
parative neuroscientists gathered for an international forum advanced mammalian brain. The avian telencephalic struc-
held at Duke University in North Carolina. The purpose tures were named in accordance with this classic view. Ed-
of the forum was to abandon the old nomenclature of cer- inger and his students (Edinger, 1908; Edinger, Wallenberg,
tain brain structures and to develop new and more accurate & Holmes, 1903) proposed the original names which were
names for the avian brain. The participants included experts later modified by Ariëns Kappers and his colleagues (Ariëns
on the avian brain, as well as others who are specialized for Kappers, Huber, & Crosby, 1936).
mammals, reptiles, and other vertebrates. The forum includ- The old nomenclature by Ariëns Kappers et al. was main-
ed presentations of various hypotheses about brain evolution tained in the influential stereotaxic atlas of the pigeon brain
and proposals for possible new name options. After three by Harvey J. Karten and William Hodos (1967). Despite the
days of intensive discussion, the participants adopted the fact that Karten and Hodos disproved the classic view of the
new nomenclature. It was welcomed and accepted in the vertebrate brain evolution, they believed that the benefit of
scientific community and sparked renewed interests among continuing to use the familiar old nomenclature (with a few
avian and mammalian brain researchers alike.
exceptions) outweighed the possibility of making changes
This paper first presents the classic interpretation of the that could cause confusion. Subsequent atlases for other
evolution of the vertebrate brain and the old avian nomen- avian species essentially followed the terminology used in
clature based on the classic view. The updated modern in- the Karten and Hodos atlas (e.g., Kuenzel & Masson, 1988;
terpretation of brain evolution is then introduced with the Stokes et al., 1974).
new nomenclature. Also discussed are the implications of
the modern view for understanding the cognitive abilities of What were the most significant aspects of the classic view
birds. Throughout the paper the question and answer for- and the old nomenclature?
mat is used to facilitate accessibility to issues of individu-
al interest. For the same reason, limited anatomical terms No avian brains are alike just as no mammalian brains
and jargon are presented only when necessary and in-depth are exactly the same. There are considerable variations in
discussion about minor issues is avoided. More detailed the development of different brain structures within birds.
information about the 2002 Forum and the anatomical sig- Nevertheless, the fundamental design of the avian brain is
nificance of the new nomenclature are presented elsewhere consistent among all birds. As in other vertebrates, the bird
(Jarvis et al., 2005; Reiner et al., 2004).
brain consists of the hindbrain, midbrain, and forebrain (thal-
amus and telencephalon). The classic view of the bird brain
The Classic View of the Avian Brain
asserted that the avian hindbrain, midbrain, and thalamus
were highly homologous to those same regions in mammals,
Who developed the classic view and the old nomenclature? but not the telencephalon. As shown in Figure 1, the basic
organization of the mammalian telencephalon consists of a
The old nomenclature was developed by early compara- group of nuclei forming basal ganglia (e.g., dorsal striatum
tive neuroanatomists about 100 years ago. At the end of and globus pallidus) at the telencephalic floor and a pallium
the nineteenth century and the beginning of the twentieth (“cloak” in Latin; e.g., neocortex and hippocampus) at the
century, new histological techniques were developed, such mantle of the telencephalon enveloping the basal ganglia.
as staining methods for nervous tissues by German patholo- The central notion of the classic view stated that the avian
gist Franz Nissl (1860 – 1919) and Italian physician Camillo and mammalian telencephalons were fundamentally differ-
Golgi (1843 – 1926). The new methods allowed early re- ent with the belief that the avian telencephalon essentially
searchers to observe detailed images of nerve cells and fibers consisted of gigantic basal ganglia and a meager pallium, as
for the first time in history. Ludwig Edinger (1855 – 1918) depicted in Figure 2A.
in Germany was one of the first researchers to use these It is perhaps useful to clarify the term homology at this
techniques. Other pioneers, such as J. B. Johnston, G. C. point. Homology is a central concept used to describe the
Huber, E. C. Crosby, C. U. Ariëns Kappers, and C. J. Her- evolutionary relationship between traits found in different
rick, also began to study and compare the brains of a variety animals. The term indicates that certain traits in different
of animals, including different fishes, amphibians, reptiles, species can be evolutionally traced back to those of their
birds, and mammals.
common ancestor, regardless of appearance or function. The
Anatomical examinations with the new techniques led classic view implied that the major part of the avian telen-
early neuroanatomists to formulate the classic view of verte- cephalon was homologous to the mammalian basal ganglia
brate brain evolution, in which the brain expanded from an – meaning that both structures presumably evolved from the
underdeveloped form of “lower” animal to a more advanced same basal ganglia region of their common ancestor (which
form of “higher” animal. The avian brain was believed to is called the stem amniote).

Revised view of the avian brain
105
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 fishes to amphibians, to
reptiles, to birds, to mammals, to primates, and finally 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
Figure 1. A schematic figure showing a transverse telence- could control only reflexive and instinctual behavior where-
phalic section of the right hemisphere of the rat. The red as the “new” brain could produce more advanced, learned,
portion represents the pallium; the blue portion represents and complex behavior.
the striatal part of the basal ganglia; the green portion rep- Anatomical reason: The majority of the avian telencepha-
resents the pallidal part of the basal ganglia; and the black lon consists of nuclear grey matter which appears similar
portion represents the lateral ventricle. Note. From Figure to the mammalian basal ganglia. In these nuclear masses,
1, “Revised nomenclature for avian telencephalon and some neurons are not organized in a laminar fashion, but aggregat-
ed as distinct clusters or nuclei. In mammals, such nuclear
related brainstem nuclei,” by A. Reiner et al., Journal of masses (basal ganglia) are surrounded by a thin and large
Comparative Neurology, 2004, 473, p. 380. Copyright 2004 sheet of nerve cells (cerebral cortex), where neurons are ar-
by the John Wiley & Sons, Inc. Adapted with permission.
ranged parallel to the surface as layers or laminae. No such
The avian telencephalon contains anatomically distinct large laminated neural architecture is apparent in the avian
subdivisions. In the old nomenclature, many of these sub- and other non-mammalian brains, a fact that led to the as-
divisions were suffixed with the term “striatum” to indicate sumption that a developed cerebral cortex is a unique char-
that these structures were part of the basal ganglia (Fig. acteristic of the mammalian telencephalon.
2A). The striatum is the term used to describe the striated Another similarity of the avian telencephalon with the
appearance of a large part (caudate-putamen) of the mam- mammalian basal ganglia is the topographical location of
malian basal ganglia because of the fiber bundles passing these nuclear masses in the brain. The nuclear mass of the
through this region. Since the avian “striatal” structures do avian telencephalon is ventrolateral to the lateral ventricle
not appear to be striated, the old nomenclature was obvious- just as the mammalian basal ganglia are positioned to this
ly based on inferred homology with the mammalian basal ventricle. The relationship of the nuclear masses relative to
ganglia, not based on the histological features of the avian the lateral ventricle can be seen in transverse brain sections
telencephalon.
(Figs. 1, 2).
Why did early neuroanatomists believe that the avian tel- How was the classic view reflected in the old nomencla-
encephalon comprised massive basal ganglia?
ture?
There are two main reasons that early neuroanatomists In the original nomenclature, there were four major “stria-
named the avian telencephalic structures after the mamma- tal” regions in the avian telencephalon: paleostriatum, arch-
lian basal ganglia “striatum.” One is the theoretical influence istriatum, neostriatum, and hyperstriatum. The prefixes “pa-
of the Aristotelian concept of phylogenetic scale, scala natu- leo-”, “archi-”, and “neo-” were used to indicate the inferred
rae, and the other is the cytoarchitectonic characteristics of evolutionary order of the emergence of these structures.
the avian telencephalon.
According to the classic view, the oldest part of the avian
Theoretical reason: The thinking of early neuroanato- telencephalon was the paleostriatum; then the archistriatum
mists was greatly biased by the scala naturae-based concept, and the neostriatum evolved; and finally the hyperstriatum

Revised view of the avian brain
106
Figure 2. Schematic figures 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 identified 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.
emerged, which was considered to be the newest portion. 2A, the neostriatum was further divided into three regions
As Figure 2A shows, each “striatal” subdivision was further along the anterior-posterior axis: the neostriatum frontale,
divided into more subregions based on cytoarchitecture.
intermediale, and caudale. Later studies revealed that sev-
Paleostriatum: In the classic view, the paleostriatum eral distinct sensory-specific nuclei were embedded in the
(“oldest” striatum) was found in all vertebrates including neostriatum, most notably the visual ectostriatum and audi-
fishes. The fish paleostriatum was named the primitivum tory Field L (Karten, 1969). The presence of the sensory nu-
(old part) and was believed to correspond to the mammalian clei was a compelling observation that the avian neostriatum
globus pallidus (a part of the basal ganglia). In reptiles and was more than simply basal ganglia.
birds, the paleostriatum developed further and differentiated Hyperstriatum: The hyperstriatum (“hypertrophied” stria-
into two parts by adding an augmentatum region above the tum) was believed to be an overgrown striatum, which ex-
primitivum.
isted only in birds, but no other animals. It was divided into
Archistriatum: As amphibians evolved from fishes, the several subregions including a ventrally located ventrale and
archistriatum (“old” striatum) emerged. It was positioned a dorsally located accessorium. The hyperstriatum ventrale
above the paleostriatum, and was proposed to be a primitive is nuclear, as are most “striatal” structures. Despite the “stri-
amygdala. This nucleus was located most caudally in the atal” name, the hyperstriatum accessorium was regarded as a
avian telencephalon and therefore it is not included in Figure pallial structure by early neuroanatomists. This region has a
2A.
laminated neural organization, although it is not six-layered
Neostriatum: A “new” part above the paleostriatum and like the mammalian neocortex. Edinger and his colleagues
archistriatum was called the neostriatum, which was not (1903) named this part the ‘cortex frontalis’ and it was later
present in fishes, but was found in amphibians and expand- renamed as the hyperstriatum accessorium by Ariëns Kap-
ed significantly in reptiles and birds. The neostriatum was pers et al. (1936). It was (and is) also called the wulst (from
considered to correspond to the caudate-putamen part of the a German word for “bump”) because it is an elevation on the
mammalian basal ganglia. Although not shown in Figure most dorsal surface of the telencephalon.

Revised view of the avian brain
107
University, who envisioned the value of such a forum and
How did the classic view explain the cognitive abilities of was the main organizer, and Anton Reiner at the University
birds?
of Tennessee, Memphis, who was the forerunner in this en-
deavor, having worked on the nomenclature issue since the
Only limited information about animal cognition was late 1990’s. In addition, many other scientists participated
available in the late nineteenth century and early twentieth in preparatory discussions through e-mail communications
century with often excessively anthropomorphistic, unreli- during the two years prior to the Forum. Today, the new
able anecdotes (Romanes, 1882). Due to the lack of sci- nomenclature that was proposed by the 2002 Forum is gen-
entific data, early neuroanatomists (Ariëns Kappers et al., erally well-accepted in the scientific community, including
1936; Edinger, 1908; Edinger et al., 1903; Herrick, 1956) avian researchers who did not participate in the Forum. The
and comparative biologists (Lloyd Morgan, 1894) consider- official nomenclature papers (Jarvis et al., 2005; Reiner et
ably underestimated the cognitive abilities of non-mammals. al., 2004) have been cited over 400 times since they were
Ironically, the misconception about animal behavior and published.
cognition was somewhat consistent with the classic view
of brain evolution. Early scientists believed that mammals What are the most significant aspects of the modern view
were capable of complex and intelligent behavior because and the new nomenclature?
only mammals had a well-developed pallium. According to
the classic view, the pallial region of mammals evolved to Based on updated data, the modern view of vertebrate
expand in size and complexity and eventually resulted in an brain evolution refutes the classic view. In the new interpre-
elaborated six-layered neocortex, the newest and thus most tation, all vertebrates share the same basic design of telen-
advanced brain structure. In contrast, birds, as well as other cephalic organization, which consists of both a pallium and
non-mammals, were presumed to be controlled by reflexes basal ganglia. The pallium of non-mammals like birds was
and instincts because their brains consisted of primarily bas- mistaken to be a part of the basal ganglia because it did not
al ganglia and a diminutive pallium.
show the same neural architecture (i.e., a laminar arrange-
ment) as the mammalian pallium – a six-layered neocortex.
The Modern View of the Avian Brain
This means that the avian telencephalon is not simply hy-
pertrophied basal ganglia. Of all the “striatal” structures in
Who developed the modern view and the new nomencla- the old nomenclature, only a small portion (i.e., “paleostria-
ture?
tum”) is homologous to the mammalian basal ganglia. The
remaining “striatal” parts derive from the pallial region of
In the mid-twentieth century, comparative neuroscientists the developing telencephalon despite their non-laminated
including Karten and Hodos started to realize that the clas- appearance. As shown in Figure 2B, about 75% of the entire
sic view of the avian brain was inaccurate and that the old telencephalic volume is now considered to be pallial (Jarvis
nomenclature was misleading (e.g., Karten, 1969; Karten & et al., 2005).
Hodos, 1967). Gradually the modern interpretation of the The revision of the terminology became necessary be-
avian brain was developed in the updated framework of ver- cause, by the end of the twentieth century, misconceptions
tebrate brain evolution. Despite this major shift in think- about the bird brain due to the old terminology became too
ing, these scientists kept using the old nomenclature until the prevalent and common in the mammalian research commu-
early twenty-first century, because the old nomenclature had nity. In past research papers, it was not unusual to find mam-
been entrenched in avian research for many decades. Some malian researchers who incorrectly compared the whole avi-
researchers wanted to maintain the same nomenclature for an telencephalon to the mammalian basal ganglia and who
consistency. Others, who were more open to name changes, falsely assumed that birds without an enlarged, developed
could not reach a consensus on alternative terminology be- pallium were deficient in sophisticated neural computation
cause there were various possible term options based on dif- and cognitive abilities. Although avian research flourished
ferent hypotheses about the organization of the avian brain. in many biological and psychological fields, the old nomen-
The new nomenclature was finally developed by the Avian clature often impeded an easy exchange of information be-
Brain Nomenclature Forum in 2002 (Jarvis et al., 2005; tween avian and mammalian researchers.
Reiner et al., 2004). The participants included 28 compara- During the 2002 Forum, terms were selected to represent
tive neuroscientists, representing multidisciplinary exper- the updated understanding of the avian brain and the correct
tise, who are respected leaders in their research fields. The homologies with the mammalian brain. The suffix “stria-
names of the participants are available as the authors of the tum” was removed from many telencephalic structures that
two official papers (Jarvis et al., 2005; Reiner et al., 2004). were discovered to be pallial in nature. These structures
Among them, the key players were Erich D. Jarvis at Duke were renamed with the suffix “pallium.” The prefixes that

Revised view of the avian brain
108
made inaccurate references to the evolutionary relationship view is considered false is that new anatomical information
of structures (“paleo-”, “archi-”, “neo-”) were also eliminat- became available due to methodological development in
ed.
neurochemistry, hodology (the study of neural connections),
and molecular biology. For instance, using new histochemi-
Why do contemporary neuroscientists conclude that the cal techniques, the distribution of dopamine was analyzed
classic view is false?
to compare mammals and birds (Jurio & Vogt, 1967). In
the mammalian basal ganglia, dopamine is abundant in the
Up until the mid-twentieth century, the classic view of the caudate-putamen (striatum) compared to the cerebral cortex.
evolution of the vertebrate brain widely prevailed. Although If the majority of the avian telencephalon was a striatum – as
there were early researchers who voiced their dissenting the classic view suggested – dopamine should be found in all
opinions against the classic view (Holmgren, 1925; Käl- the “striatal” regions in the avian telencephalon. Research
lén, 1953; Kuhlenbeck, 1938; Rose, 1914), their views were shows that only a small part of the telencephalon (the paleo-
not predominant. Eventually, later researchers were able to striatum augmentatum) contains a high level of dopamine.
refute the classic view based on three lines of compelling Similar results were obtained regarding the distributions of
arguments: 1) theoretical, 2) anatomical, and 3) behavioral other neurochemicals (e.g., acetylcholinesterase, substance
evidence.
P, and enkephalin) to conclude that only the paleostriatum
Theoretical evidence: The first reason is the updated un- augmentatum is equivalent to the mammalian caudate-pu-
derstanding of vertebrate evolution. Comparative neurosci- tamen and that the paleostriatum primitivum corresponds to
entists accepted the revised and accurate view of vertebrate the globus pallidus (Karten, 1969; Reiner, Medina, & Veen-
brain evolution based on analyses of fossil records and com- man, 1998). The conclusion is reinforced by hodological
parative phyletic studies. Instead of a unilinear or unidimen- and molecular evidence. Tract-tracing studies revealed that
sional process, evolution is characterized by divergence and the connection patterns of the paleostriatum with other brain
multi-linearity (Butler & Hodos, 2005; Campbell & Hodos, structures (e.g., midbrain and hindbrain) are similar to those
1991; Hodos & Campbell, 1969; Northcutt, 1981).
of the mammalian basal ganglia (Brauth & Kitt 1980; Karten
These characteristics are seen in Figure 3, illustrating the & Dubbeldam, 1973; Reiner, Brauth, & Karten, 1984). Em-
currently accepted evolutionary relationships among tetra- bryonic molecular studies supported the same conclusion
pods (amphibians, reptiles, birds, and mammals) (Carroll, that the avian paleostriatum is homologous to the mamma-
1988). Briefly, ancestral tetrapods diverged from one group lian basal ganglia in terms of the expression of certain genes
of bony fish in the Devonian period about 400 million years (Marin & Rubinstein, 2001; Puelles et al., 2000).
ago (MYA). Tetrapods then gave rise to stem amniotes, Behavioral evidence: The classic view presumed that non-
which further diverged into two major amniote groups by the mammals like birds could only perform unlearned, instinc-
end of the Carboniferous period. They were synapsids and tual behavior because the majority of their telencephalon
diapsids, the ancestors of mammals and birds respectively. was striatal. In this view, birds with a relatively small pal-
Synapsids comprise two successive orders, pelycosaurs and lium were not able to behave like mammals that could enjoy
then therapsids. From the latter, early mammals arose in complex and sophisticated behavior owing to the presence
the Late Triassic period more than 200 MYA. Diapsids be- of a large neocortex. For the past 50 years, a new picture
came the ancestors of the majority of living reptiles. The lin- about the cognitive abilities of birds has emerged using sci-
eage of diapsids diverged several times to produce multiple entifically rigorous methods (Wasserman & Zentall, 2006).
groups, including dinosaurs, which were the most successful Some of the complex behaviors of birds are considered to
vertebrates for more than 150 million years, beginning in be comparable to those of primates (Emery, 2006). Pigeons
the Later Triassic period to the end of the Cretaceous period. can memorize and discriminate more than 700 photographs
Birds arose most likely 140 MYA from the saurichian dino- (Cook, Levison, Gillett, & Blaisdell, 2005) and discrimi-
saurs in the Late Jurassic period.
nate between the paintings of cubistic and impressionistic
Hence, unlike birds, mammals did not evolve from ances- styles of painting (Watanabe, Sakamoto, & Wakita, 1995).
tral reptiles. The ancestors of mammals (synapsids) were Songbirds, parrots, and hummingbirds show the abilities
stem amniotes, which were also the ancestors of reptiles and of complicated vocal learning (Doupe & Kuhl, 1999; Jar-
birds. The lineages leading to mammals and birds are sepa- vis et al., 2000; Pepperberg, 1999). Starlings can be trained
rate since synapsids and diapsids diverged from stem amni- to acquire recursion grammar which had been considered to
otes about 300 MYA. This means that each of the avian and be unique to human language (Gentner, Fenn, Margoliash,
mammalian brains has an independent evolutionary history & Nusbaum, 2006). New Caledonian crows manufacture
of millions of years. The avian and reptilian brains are not hook-tools with their bills and use them to search for prey in
primitive, undeveloped versions of the mammalian brain.
holes in tree trunks (Hunt, 1996). Scrub-jays appear to form
Anatomical evidence: The second reason that the classic episodic-like memory about a previous experience (Clayton

Revised view of the avian brain
109
Figure 3. Probable phylogenetical relationships of bony fishes, 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.
& Dickinson, 1998), upon which they can behave as if they is believed to be homologous to part of the mammalian neo-
have predictions for the future (Clayton, Bussey, & Dickin- cortex.
son, 2003).
Dorsal Ventricular Ridge: The nidopallium, arcopallium,
and the mesopallium are together designated as the dorsal
What are the major changes in the nomenclature?
ventricular ridge (DVR), a voluminous nuclear mass pro-
truding into the lateral ventricle (Ulinski, 1983). Although
During the 2002 Forum, new names were adopted for the origin of the DVR was proposed to be striatal (i.e., basal
over 30 brain areas. The majority of changes were made for ganglia) in the classic view, it is now considered to be palli-
the telencephalic structures. Figure 2B represents the main al. The DVR is also found in reptiles, yet the reptilian DVR
changes in the nomenclature for the telencephalon.
is not as enlarged or as differentiated as the avian one.
Paleostriatum - Lateral Striatum and Globus Pallidus: Brainstem: At least nine structures in the brainstem ob-
The avian paleostriatum augmentatum and primitivum were tained new names based on the updated information. For
renamed as the lateral striatum and globus pallidus, respec- example, one of the brainstem structures is a cell group tra-
tively. The avian lateral striatum is considered to be equiva- ditionally called the nucleus tegmenti pedunculo-pontinus,
lent to the mammalian dorsal striatum (caudate-putamen), pars compacta (TPc) in the midbrain (Karten & Hodos,
whereas the avian globus pallidus corresponds to the mam- 1967). The TPc name was based on the location and den-
malian counterpart with the same name.
sity of the cell group because there was then no other in-
Archistriatum - Amygdala and Arcopallium: The archistri- formation about the nucleus. Later anatomical, chemical,
atum became the arcopallium (arched pallium). Parts of the and physiological investigations revealed that TPc is directly
archistriatum were also renamed as the amygdala to indicate comparable to the substantia nigra pars compacta (SNc) of
that they belong to the amygdaloid complex.
mammals. Most notably, just like SNc, TPc sends major
Neostriatum - Nidopallium: The neostriatum became the dopaminergic projections to the avian counterpart of the
nidopallium. The term “nido-” means a nest, which implies striatal region of the basal ganglia (Kitt & Brauth, 1986a,
that this structure contains several anatomically distinct and b; Reiner et al., 2004). The participants of the 2002 Forum
functionally different nuclei, such as the visual ectostriatum decided that the common name SNc should be adopted to
and the auditory Field L. The ectostriatum was renamed as clarify the homologous relationship between these nuclei.
the entopallium and Field L maintained the same name.
Hyperstriatum - Mesopallium and Hyperpallium: In the Why is the nuclear pallium (DVR) categorized as a pallium
hyperstriatum, the accessorium was renamed as the hyper- despite its non-laminar organization?
pallium (hypertrophied pallium) whereas the ventrale be-
came the mesopallium (middle pallium). The hyperpallium In mammals, the term pallium is often used synonymously
and mesopallium obtained different names because they are with a six-layered neocortex. Although the neocortex is the
distinguishable cytologically, chemically, hodologically, largest structure derived from the pallial sector of the devel-
functionally, and developmentally. The hyperpallium was oping telencephalon, the pallium cannot be solely defined as
regarded as pallial by early neuroanatomists and this inter- a six-layered laminar configuration. There are other pallial
pretation was supported by the 2002 Forum participants. It structures in the mammalian brain that are laminated with

Revised view of the avian brain
110
fewer than six layers, and still others that are not laminated larly, the avian pallium is crucially involved in sensory pro-
at all. Both the olfactory (piriform) cortex and hippocam- cessing, such as visual analysis (Bischof & Watanabe, 1997;
pus have pallial origins, and are laminated with two to three Hodos, 1993; Patton, Husband, & Shimizu, 2008) and audi-
layers (Fig. 1). Recent studies showed that nuclear (non- tory analysis (Jarvis, Mello, & Nottebohm, 1995; Mello &
laminar) structures like the claustrum and lateral parts of the Clayton, 1994) according to behavioral, physiological, and
amygdala (Fig. 1) also develop from the embryonic pallium gene expression studies. There are also ample data showing
(Puelles et al., 2000; Swanson, 2000; see also Holmgren, that these regions are important for the production of highly
1925).
complex behavior, such as learning, memory, and attention
The DVR (the nidopallium, arcopallium, and mesopal- (Güntürkün & Durstewitz, 2001; Horn, 1985; Iwaniuk &
lium) occupies a large part of the avian telencephalon and is Hurd, 2005; Knudsen, 2002; Lefebvre, Reader, & Sol, 2004;
not organized in a laminar fashion. With a cursory glance, Mello, 2002; Nottebohm, Stokes, & Leonard, 1976; Sadan-
no such huge nuclear structure is recognizable in the mam- anda, Korte, & Bischof, 2007; Scharff & Nottebohm, 1991;
malian pallium. Nevertheless, the avian DVR and hyperpal- Shimizu & Hodos, 1989). For instance, songbirds have
lium are considered to be pallial since they show important distinct neural circuits in the pallium (and basal ganglia)
characteristics similar to the mammalian pallium – neocor- to learn and produce species-specific songs for communi-
tex, claustrum, and amygdala – in terms of anatomy and cation (Nottebohm et al., 1976). Several pallial structures
function (Karten, 1969; Puelles et al., 2000; Reiner et al., are directly involved in filial imprinting learning of preco-
1998).
cial birds (e.g., ducks and chickens) (Horn, 1985) and sexual
Anatomical characteristics: There has been a voluminous imprinting of finches (Rollenhagen & Bischof, 2000). The
amount of hodological studies since the 1960s that showed caudolateral nucleus of the nidopallium has been compared
that the connection patterns of the avian DVR and hyperpal- to the mammalian prefrontal cortex (Güntürkün & Durstew-
lium are similar to the mammalian pallium (Shimizu, 2001). itz, 2001). Behavioral and physiological studies show that
The sensory pathways connecting the thalamus and telen- this nucleus plays a major role in working memory, which
cephalon have especially been studied extensively. These is used to store and manipulate information for a short time
studies demonstrated that distinct cell groups in the DVR period to achieve behavioral goals. The size of the DVR
(the nidopallium, in particular) and hyperpallium receive appears to be larger in some avian species, such as crows
massive afferent projections from visual, auditory, somato- and parrots (Iwaniuk & Hurd, 2005; Lefebvre et al., 2004),
sensory, and related nuclei in the dorsal thalamus. This which may be related to their ability to exhibit complex be-
pattern of projections is similar to the pattern in the mam- havior more frequently than other birds (Emery, 2006; Hunt,
malian brain, in which distinct modality-specific regions 1996; Pepperburg, 1999).
within the pallium (the neocortex, in particular) receive dif-
ferent sensory projections from the dorsal thalamic nuclei What is the nuclear pallium (DVR) homologous to in the
(Karten, 1969; Karten & Shimizu, 1989; Shimizu & Bow- mammalian pallium?
ers, 1999). In the avian brain, these primary sensory areas
then send projections to multiple nuclei in the telencephalon The terms hyperpallium, mesopallium, nidopallium, and
to form closely interconnected circuits for further process- arcopallium exist only in the avian brain nomenclature, and
ing (Doupe & Kuhl, 1999; Husband & Shimizu, 1999). As no other animals have such structures with the same names.
for motor output from the telencephalon, both the DVR (the During the development of the new nomenclature, some
arcopallium, in particular) and hyperpallium give rise to specific names for mammalian pallial structures (e.g., cor-
long descending efferent projections to motor nuclei in the tex, neocortex) were intentionally avoided for use with the
brainstem and spinal cord. The projection pattern is reminis- avian DVR. This is because the participants of the 2002 Fo-
cent of the cortico-bulbar and cortico-spinal pathways from rum could not reach a consensus about which specific struc-
the mammalian neocortex (Wild & Williams, 2000; Zeir & tures of the mammalian pallium (i.e., neocortex, claustrum,
Karten, 1971). Embryological and developmental molecu- or amygdala) correspond to the avian pallium. There are
lar studies also show similarities between the mammalian diverse hypotheses regarding the homology of the DVR with
and avian pallia (Puelles et al., 2000; Smith-Fernandez et al., the mammalian pallium (Bruce & Neary, 1995; Butler, 1994;
1998). During embryogenesis, pallial-specific transcription Karten 1969, 1991; Karten & Shimizu, 1989; Northcutt
factors, such as EMX1, PAX6, and TBR1, are present in the & Kaas, 1995; Puelles et al., 2000; Reiner, 1991; Reiner,
DVR and hyperpallium, which is also true for the mamma- Yamamoto, & Karten, 2005; Striedter, 1997). The two main
lian pallium.
hypotheses will be presented next. In these hypotheses, the
Functional characteristics: In mammals, the neocortex DVR is compared to either the neocortex or the claustrum/
plays an essential role in a variety of activities, including amygdala of the mammalian pallium.
sensation, perception, motor control, and cognition. Simi- 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- Further studies about both the avian and mammalian pal-
tex. Massive thalamo-nidopallial projections are similar to lial structures are clearly warranted to clarify the nature of
the connection patterns of the thalamo-neocortex in mam- the DVR and to identify the mammalian counterpart. The
mals, and subsequent intrinsic circuits within the avian DVR avian DVR is a large and heterogeneous structure contain-
(i.e., nidopallium, mesopallium, and arcopallium) are simi- ing sensory-specific and non-sensory regions. Certainly,
lar to those between layers in the neocortex (Karten 1969, more anatomical and functional information is needed about
1991; Karten & Shimizu, 1989). This hypothesis proposes the non-sensory regions, which have been scarcely studied
that some neurons of individual cell populations in the DVR compared to the regions directly associated with sensory
are equivalent to neurons in different layers of the mamma- processing. In the mammalian pallium, almost nothing is
lian neocortex, despite the lack of a laminar organization of known about the function of the claustrum which has been
the DVR as a whole. Several gene expression studies are suggested to be involved in the generation and control of
consistent with this hypothesis. For instance, certain genes consciousness (Crick & Koch, 2005).
(the steroid transcription factor ROR-? and the potassium
channel EAG2) are expressed in neurons of layer IV of the How does the revised view of the avian brain explain the
mammalian neocortex that receives thalamic input. Some of cognitive abilities of birds?
the same genes are also found in specific regions in the DVR
(i.e., the entopallium and Field L) which receive projections Almost daily, new information is learned about the com-
from the sensory thalamic nuclei (Dugas-Ford & Ragsdale, plex behavior of non-human animals – behavior that was tra-
2003). Several other researchers have supported and modi- ditionally considered to be uniquely human. Novel discov-
fied this hypothesis (e.g., Butler, 1994; Reiner, 1991; Reiner eries of animal cognition are no longer surprising because
et al., 2005).
they are consistent with the modern, revised interpretations
Claustrum/Amygdala: It is also possible that neurons of of the vertebrate brain.
the avian DVR are equivalent to those in non-laminar por- In the particular case of birds, the modern view of the
tions of the mammalian pallium – the claustrum and amyg- avian brain provides several insights regarding their highly
dala in particular. The claustrum is a thin sheet of grey mat- sophisticated behavior and underlying neural systems. First,
ter lying between the outer surface of the basal ganglia and the revised view supports the assumption that the existence
the inner surface of the lateral portion of the neocortex (Fig. of a developed higher brain structure – the pallium – is di-
1). It is found in marsupials and placental mammals (Butler, rectly related to the production of flexible, learned, and com-
Molnár, & Manger, 2002) and some monotremes (Ashwell, plex behavior. The cognitive abilities of birds are difficult
Hardman, & Paxinos, 2004). The mammalian amygdala is to explain from the mammalian-centric classic view of the
located in the tip of the temporal lobe and consists of mul- vertebrate brain evolution. This is because avian (and other
tiple distinct subdivisions including pallial (lateral anterior non-mammalian) brains were believed to lack the sufficient
and basolateral nuclei) and subpallial portions (Swanson & hardware (a large laminated pallium or neocortex) necessary
Petrovich, 1998). The claustrum and pallial amygdala have to carry out complex behavior. The modern interpretation
been compared to the avian DVR based on nuclear appear- states that the avian nuclear pallium is as anatomically de-
ance, lateral location, and connection patterns with the thala- veloped and as functionally sophisticated as the mammalian
mus and brainstem nuclei (Bruce & Neary, 1995; Striedter, laminar pallium. Indeed, of all living vertebrates, birds and
1997). Based on developmental expression of homeobox mammals have proportionally large telencephalons com-
genes (EMX1 and PAX6), the nidopallium is suggested to pared to any other animals due to the enlarged pallial region
correspond to the mammalian ventral claustrum and lateral of each (Northcutt, 1981). It is reasonable to assume that as
anterior amygdala, whereas the mesopallium corresponds to the avian pallium became enlarged and elaborated, despite
the dorsal claustrum and basolateral amygdala (Puelles et its non-laminated configuration, birds evolved to perform
al., 2000).
remarkably complex behavior.
Neither hypothesis seems to be flawless since either does Second, an important insight resulting from the modern
not satisfactorily explain all anatomical data available today. view is that the evolutionary origins of the complex behav-
Subsequent gene expression studies also revealed evidence ior of birds and mammals are most likely different. In oth-
against each of these two hypotheses (Gorski et al., 2002; er words, birds and mammals independently evolved with
Haesler et al., 2004). Some authors ponder the possibility elaborated neural systems to generate similarly complex
that the two hypotheses may not be mutually exclusive. But- behavior (Emery, 2006; Shimizu, 2001, 2007). The con-
ler and Molnár proposed an alternative hypothesis that the vincing evidence to support this argument is that the devel-
avian DVR is homologous to both the mammalian neocortex opments of the avian and mammalian pallia were separate
and claustrum/amygdala as derivatives of a common embry- (yet parallel) events in evolution. According to endocasts
onic field (Butler & Molnár, 2002; Molnár & Butler, 2002). 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- essary to support such remarkable behavior. The caveat is
riod had only a slender, elongated forebrain with no signs of that the avian pallium and mammalian counterpart are mark-
the pallial enlargement found in living birds and mammals edly different in terms of the architectural organization of
(Hopson, 1979; Ulinski, 1983). In the lineage leading mam- neurons (i.e., nuclear vs. laminar). Although both types of
mals, endocasts of early synapsids show that their forebrain pallium are capable of generating behavioral complexity,
remained diminutive. Only early mammals of the Jurassic the exact significance of the anatomical differences on the
period started to show an enlarged forebrain, which was underlying cognitive processes remains vastly unexplored
most likely correlated with the development of the cerebral (Butler & Cortterill, 2006; Güntürükün & Durstewitz, 2001;
cortex. A gradual, but not necessarily impressive, expan- Shimizu & Bowers, 1999). Even when birds and mammals
sion of the reptilian forebrain was seen in the Late Triassic exhibit similarly complex behavior, it is possible that the
period. The forebrain became substantially enlarged only DVR and neocortex involve qualitatively dissimilar compu-
when birds emerged, suggesting that the significant develop- tational principles and mechanisms to generate such behav-
ment of the nuclear DVR occurred during the reptile-bird ior. Without more information about the two types of pallial
transition. These observations about the distinct and sepa- organization, it is still presumptuous to assume that the su-
rate evolutions of the pallia in birds and mammals suggest perficial similarity of behavior between birds and mammals
that their complex behaviors (as products of the enlarged and is attributable to an essentially identical kind of underlying
elaborated pallia) also have distinct and separate evolution- process.
ary origins (Shimizu, 2001, 2007).
Finally, the modern view raises a question regarding the
Concluding Question
indispensability of the laminated neural architecture for
the generation of complex behavior. In humans and other What are the main lessons that comparative cognitive and
mammals, a six-layered neocortex seems essential to accom- behavioral researchers can learn from the history of com-
plish complex behavior, and thus a lamination is often pre- parative neuroscience?
sumed to be the most optimal design for sophisticated neu-
ral computation. It is easy to refute this assertion since not Perhaps the important lesson for researchers of animal
all mammals appear to exhibit complex behavior, whereas cognition and behavior is that the true nature of vertebrate
many birds show such behavior without a six-layered neo- evolution – divergence and multi-linearity – needs to be
cortex. The presence of a six-layered neocortex does not adamantly reasserted in the course of comparative investiga-
guarantee the generation of behavioral complexity, which tions. Researchers should resist the temptation to fall back
can be achieved by an alternative design – a nuclear pal- on the familiar scala naturae-based views. The mammalian-
lium (DVR). In fact, the interconnections among specific centric or anthropomorphic perspective, which has persis-
brain structures may be more important than the presence of tently permeated comparative research despite the scientific
a tightly layered architecture (Jarvis et al., 2004; Shimizu, evidence, must be avoided (Campbell & Hodos, 1991; Hodos
2001, 2007). I hasten to state that this argument is not meant & Campbell, 1969; Wynne, 2007). The early comparative
to underestimate the advantage of a laminar organization. neuroanatomists who subscribed to such an assumption un-
The lamination is probably one of the most efficient designs intentionally set in motion the misguided nomenclature that
to process topographically mapped information. All verte- lasted about 100 years. With this lesson from comparative
brates, including non-mammals, have many laminated brain neuroscience in mind, the cognition and behavior of animals
structures, such as olfactory bulb, retina, and midbrain. The should be evaluated within the framework of the multi-linear
avian optic tectum of the midbrain is particularly large and evolution, and not on the basis of an ascending continuum
differentiated. Although the tectum appears to be less di- toward mammals and humans. The complex cognitive and
rectly involved in cognitive proficiencies and complex be- behavioral abilities of birds which have enabled their suc-
havior compared to the pallium, the tectum and DVR have cessful adaptation to the environment should be appreciated
close anatomical and functional connections with each other in their own right, not because they resemble some aspects
(Shimizu, 2001, 2007).
of human behavior and cognition. The “bird brain” – despite
the rather insulting colloquial connotation of the term – is a
Why can birds be so smart?
truly unique exceptional machine deserving of our respect.
In other words, how is it possible for birds to behave in
References
surprisingly intricate and flexible ways? The modern view of
brain evolution provides a proximate explanation. In short, Ariëns Kappers, C.U., Huber, C.G. & Crosby, E.C. (1960).
birds, like mammals, have developed a high-level forebrain
Comparative Anatomy of the Nervous System of Verte-
structure – an enlarged and elaborated pallium – that is nec-
brates, Including Man. (Original work published 1936).

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