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The Avian Brain Nomenclature Forum: Terminology for a New Century in Comparative Neuroanatomy

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Abstract

Many of the assumptions of homology on which the standard nomenclature for the cell groups and fiber tracts of avian brains have been based are in error, and as a result that terminology promotes misunderstanding of the functional organization of avian brains and their evolutionary relationship to mammalian brains. Recognizing this problem, a number of avian brain researchers began an effort to revise the terminology, which culminated in the Avian Brain Nomenclature Forum, held at Duke University from July 18 to 20, 2002. In the new terminology approved at this Forum, the flawed conception that the telencephalon of birds consists nearly entirely of a hypertrophied basal ganglia has been purged from the telencephalic terminology, and the actual parts of the basal ganglia and its brainstem afferent cell groups have been given names reflecting their now evident homologies. The telencephalic regions that were erroneously named to reflect presumed homology to mammalian basal ganglia were renamed as parts of the pallium, using prefixes that retained most established abbreviations (to maintain continuity with the replaced nomenclature). Details of this meeting and its major conclusions are presented in this paper, and the details of the new terminology and its basis are presented in a longer companion paper. We urge all to use this new terminology, because we believe it will promote better communication among neuroscientists.
The Avian Brain Nomenclature Forum:
Terminology for a New Century in
Comparative Neuroanatomy
ANTON REINER,
1
*DAVID J. PERKEL,
2
LAURA L. BRUCE,
3
ANN B. BUTLER,
4
ANDRA
´S CSILLAG,
5
WAYNE KUENZEL,
6
LORETA MEDINA,
7
GEORGE PAXINOS,
8
TORU SHIMIZU,
9
GEORG STRIEDTER,
10
MARTIN WILD,
11
GREGORY F. BALL,
12
SARAH DURAND,
13
ONUR GU
¨TU
¨RKU
¨N,
14
DIANE W. LEE,
15
CLAUDIO V. MELLO,
16
ALICE POWERS,
17
STEPHANIE A. WHITE,
18
GERALD HOUGH,
19
LUBICA KUBIKOVA,
20
TOM V. SMULDERS,
21
KAZUHIRO WADA,
20
JENNIFER DUGAS-FORD,
22
SCOTT HUSBAND,
9
KEIKO YAMAMOTO,
1
JING YU,
20
CONNIE SIANG,
20
AND ERICH D. JARVIS
20
*
1
Department of Anatomy and Neurobiology, University of Tennessee Health Science
Center, Memphis, Tennessee 38163
2
Departments of Biology and Otolaryngology, University of Washington,
Seattle Washington 98195-6515
3
Department of Biomedical Sciences, Creighton University School of Medicine,
Omaha, Nebraska 68178
4
Krasnow Institute and Department of Psychology, George Mason University,
Fairfax, Virginia 22030-4444
5
Department of Anatomy, Semmelweis University, Faculty of Medicine,
H-1094 Budapest, Hungary
6
Department of Poultry Science, Poultry Science Center, University of Arkansas,
Fayetteville, Arkansas 72701
7
Department of Human Anatomy, Faculty of Medicine, University of Murcia,
Murcia E-30100, Spain
8
Prince of Wales Medical Research Institute, Sydney, New South Wales 2031, Australia
9
Department of Psychology, University of South Florida, Tampa, Florida 33620-8200
10
Department of Neurobiology and Behavior, University of California at Irvine,
Irvine, California 92697-4550
11
Division of Anatomy, Faculty of Medical and Health Sciences, University of Auckland,
Auckland 92019, New Zealand
12
Department of Psychological and Brain Sciences, Johns Hopkins University,
Baltimore, Maryland 21218
13
Department of Biology, Queens College–City University of New York,
Flushing, New York 11367-1597
14
Department of Biopsychology, Institute of Cognitive Neuroscience, Faculty of Psychology,
Ruhr-Universita¨t Bochum, 44780 Bochum, Germany
15
Department of Psychology, California State University, Long Beach,
Long Beach, California 90840-0901
16
Neurological Sciences Institute, Oregon Health and Science University, West Campus,
Beaverton, Oregon 97006-3499
17
Department of Psychology, St John’s University, Jamaica, New York 11439
18
Department of Physiological Science, University of California, Los Angeles,
Los Angeles, California 90095-1606
19
Department of Psychology, Bowling Green State University, Bowling Green, Ohio 43403
20
Department of Neurobiology, Duke University Medical Center,
Durham, North Carolina 27710
21
School of Biology, University of Newcastle, Newcastle upon Tyne
NE2 4HH, United Kingdom
22
Department of Organismal Biology and Anatomy, University of Chicago,
Chicago, Illinois 60637
THE JOURNAL OF COMPARATIVE NEUROLOGY 473:E1–E6 (2004)
©2004 WILEY-LISS, INC.
ABSTRACT
Many of the assumptions of homology on which the standard nomenclature for the cell
groups and fiber tracts of avian brains have been based are in error, and as a result that
terminology promotes misunderstanding of the functional organization of avian brains and
their evolutionary relationship to mammalian brains. Recognizing this problem, a number of
avian brain researchers began an effort to revise the terminology, which culminated in the
Avian Brain Nomenclature Forum, held at Duke University from July 18 to 20, 2002. In the
new terminology approved at this Forum, the flawed conception that the telencephalon of
birds consists nearly entirely of a hypertrophied basal ganglia has been purged from the
telencephalic terminology, and the actual parts of the basal ganglia and its brainstem
afferent cell groups have been given names reflecting their now evident homologies. The
telencephalic regions that were erroneously named to reflect presumed homology to mam-
malian basal ganglia were renamed as parts of the pallium, using prefixes that retained most
established abbreviations (to maintain continuity with the replaced nomenclature). Details of
this meeting and its major conclusions are presented in this paper, and the details of the new
terminology and its basis are presented in a longer companion paper. We urge all to use this
new terminology, because we believe it will promote better communication among neurosci-
entists. More information is available at the Avian Brain Nomenclature Exchange website
http://avianbrain.org. J. Comp. Neurol. 473:E1–E6, 2004. ©2004 Wiley-Liss, Inc.
Indexing terms: pallium; basal ganglia; telencephalon; brainstem; evolution; terminology; birds;
mammals
The view of telencephalic evolution that became wide-
spread during the first 60 years of the 20th century was
that both birds and mammals shared several basal gan-
glia structures, namely, an older structure inherited from
fish called the paleostriatum (now called the globus palli-
dus in mammals) and a newer basal ganglia structure
that evolved in amphibians but expanded in reptiles and
more so in birds, called the neostriatum (then considered
equivalent to the supposedly newer parts of the caudate
and putamen; Edinger et al., 1903; Edinger, 1908; Arie¨ns-
Kapper 1922, 1928; Johnston, 1923; Arie¨ns-Kappers et al.,
1936; Herrick, 1948, 1956). Reptiles were thought to have
also elaborated the two parts of the paleostriatum of fish,
the primitivum and the augmentatum (the latter consid-
ered equivalent to older parts of mammalian caudatopu-
tamen) into distinct regions and passed on this trait to
birds, whereas the neostriatum in birds was thought to
have given rise to a novel overlying structure called the
hyperstriatum. Birds and mammals were also thought to
share a caudobasal subcortical structure termed the arch-
istriatum, now called the amygdala in mammals. Because
an equivalent of laminated mammalian neocortex was not
evident in birds, their telencephalon was considered to
consist primarily of a hypertrophied basal ganglia. Al-
though some investigators such as Kuhlenbeck, Rose,
and Ka¨lle´n dissented from these views of avian brain
organization and evolution (Rose, 1914; Kuhlenbeck,
1938; Ka¨lle´n, 1953), the accretionary theory of verte-
brate brain evolution, as espoused in major books by
Arie¨ns-Kappers et al. (1936) and Herrick (1948, 1956),
became the prevailing view and led to the predominant
use of the terms neostriatum, archistriatum, and hyper-
striatum to refer to the major sectors of the telenceph-
alon above the so-called paleostriatum in birds and to
the term neocortex for the major telencephalic sector in
mammals.
In 1967, Karten and Hodos published their stereotaxic
atlas of the pigeon brain, which provided the first compre-
hensive effort to identify and name all parts of the brain in
birds. For the diverse subtelencephalic structures, prior
studies offered simple and uncontroversial terms that
Karten and Hodos adopted (Huber and Crosby, 1929;
Craigie, 1931; Kuhlenbeck, 1937, 1939; Meessen and Ol-
szewski, 1949; Olszewski and Baxter, 1954). Karten and
Hodos, however, recognized that the choice of a terminol-
ogy for avian telencephalon was more problematic, be-
cause they were aware that the structures termed the
archistriatum, neostriatum, ectostriatum, and hyperstria-
tum by Arie¨ns-Kappers et al. (1936) were unlikely to be
parts of the basal ganglia. Despite their misgivings,
Karten and Hodos chose to use these terms because they
were already entrenched. Subsequent atlases for other
avian species (Kuenzel and Masson, 1988) largely used
the same terminology as Karten and Hodos. Although
much of this terminology has stood the test of time, many
Grant sponsor: National Science Foundation; Grant number: IBN-
0110894; Grant sponsor: National Institutes of Health; Grant number:
1R13-MH-64400-01.
*Correspondence to: Anton Reiner, Department of Anatomy & Neurobi-
ology, University of Tennessee Health Science Center, 855 Monroe Avenue,
Memphis, TN 38163. E-mail: areiner@utmem.edu and/or Erich D. Jarvis,
Department of Neurobiology, Box 3209, Duke University Medical Center,
Durham, NC 27710. E-mail:jarvis@neuro.duke.edu
Received 18 April 2003; Revised 11 December 2003; Accepted 21 January
2004
DOI 10.1002/cne.20119
Published online in Wiley InterScience (www.interscience.wiley.com).
E2 A. REINER ET AL.
of the interpretations of telencephalic homology implied
by the terminology of Arie¨ns-Kappers et al. (1936) have
been overwhelmingly shown to be erroneous. Additionally,
the mammalian homologues of some brainstem cell groups
connected with the telencephalon, which were not known
at the time the Karten and Hodos atlas was completed,
have also become clear. As deeper insight has been gained
into the evolution, development, and function of the brains
of birds and mammals, the awed homologies implied by
the terms of Arie¨ns-Kappers et al. for avian telencephalon
and some now evident errors in brainstem terminology
have greatly hindered communication among avian and
mammalian brain research specialists and perpetuated an
outdated view of avian brain evolution.
This issue came to be of increasing concern to avian
neurobiologists over the past 10 years, and formal efforts
to revise avian brain nomenclature were begun 5 years
ago by a small group of avian brain specialists. To develop
widely acceptable new terms, this group sought to involve
a greater number of researchers than had participated in
two previous attempts to standardize avian neuroana-
tomical nomenclature (Baumel, 1979, 1993). Accordingly,
the group discussing such a revision eventually grew to an
international collection of multidisciplinary neuroscien-
tists, and 2 years ago the group decided to hold an open
Nomenclature Forum, at which a new terminology would
be adopted. This Forum was held July 18 20, 2002 at
Duke University in Durham, North Carolina, and it was
preceded by in-depth discussions by E-mail and telephone
of the need for a terminology change and specic recom-
mendations as to the nature of the new terms. This report
describes the pre-Forum preparatory period, the Forum
logistics, and the decision-making process. The new ter-
minology itself and the rationale for individual changes
are presented in detail in a companion paper (Reiner et
al., 2004).
AVIAN BRAIN NOMENCLATURE FORUM
Rationale and overview of meeting
Armed with 2 years of formal preparation, an interna-
tional team of experts in the elds of avian, mammalian,
reptilian, and sh brain research assembled at Duke Uni-
versity and took on the task of devising a new avian
telencephalic nomenclature. This group critically evalu-
ated the evidence, as detailed in various published and
soon-to-be-published studies, for specic, possible new
terms. We concluded that an overwhelming body of data
supports the interpretation that most of the dorsal three-
fourths of the cerebrum in birds (including what has been
termed the neostriatum, hyperstriatum, and archistria-
tum) is pallial in nature and therefore homologous as a
eld to the brain sector that in mammals includes the
neocortex, claustrum, piriform cortex, and pallial amyg-
dala (Karten, 1969, 1991; Gu¨ntu¨rku¨n, 1991; Butler, 1994;
Reiner et al., 1998; Smith-Fernandez et al., 1998; Medina
and Reiner, 2000; Puelles et al., 2000). Accordingly, we
have now designated the major subdivisions of the dorsal
three-fourths of the telencephalon in birds with terms that
contain the root word -palliumrather than the Arie¨ns-
Kappers et al. term -striatum.We have also revised
prexes with questionable evolutionary implications. We
further concluded that the approximately ventral one-
fourth of the cerebrum in birds contains the homologues of
such subpallial structures in mammals as the basal gan-
glia proper (including dorsal striatal and pallidal subdivi-
sions), the more ventrally located limbic striato-pallidal
complex (sometimes called the ventral basal ganglia), the
medial and lateral bed nuclei of the stria terminalis, the
basal nucleus of Meynert, and part of the subpallial amyg-
dala. The new names chosen for these subpallial struc-
tures reect these homologies.
Meeting planning and preparation
In organizing and planning the Nomenclature Forum,
several goals were paramount. First, it was necessary to
devise means by which the researchers interested in the
issue of nomenclature change could communicate and de-
velop their thoughts about suitable name changes. This
was achieved through two E-mail list servers, one for all
avian brain researchers and one for songbird specialists.
Typically messages were posted to both lists. By means of
these two E-mail list servers, the discussion of nomencla-
ture change was open to the broad community of avian
brain researchers, and all had the opportunity to contrib-
ute. Additionally, those interested in nomenclature
change met as a group one evening at the annual Society
for Neuroscience Meeting for each of the several years
preceding the Forum and discussed issues related to avian
brain nomenclature revision.
Second, a planning group of 13 neurobiologists was es-
tablished for the Nomenclature Forum. This group also
communicated openly by E-mail, supplemented by indi-
vidual face-to-face or telephone conversations. In forming
this group, which constituted the core of those attending
the Forum, we sought to include major experts in avian
neurobiology, as well as in sh, amphibian, reptilian, and
mammalian neurobiology. This group included Laura L.
Bruce, Ann B. Butler, Andra´s Csillag, Erich D. Jarvis,
Harvey J. Karten, Wayne Kuenzel, Loreta Medina,
George Paxinos, David J. Perkel, Anton Reiner, Toru
Shimizu, Georg Striedter, and Martin Wild. Many mem-
bers of this group possess expertise in more than one
vertebrate group, some have considerable experience in
brain atlas construction, and some are conversant with
classical languages.
Third, to provide concrete ideas for nomenclature revi-
sion, proposals for specic nomenclature change were so-
licited by the core group and then extensively discussed
(principally by E-mail) as to their strengths and weak-
nesses prior to the meeting. The open nature of the E-mail
communication within the avian brain research commu-
nity made it possible to gauge the reactions of diverse
members of the community to specic proposals.
Fourth, to foster planning for the meeting and dissem-
ination of ideas and information related to the nomencla-
ture revision effort, a website called the Avian Brain No-
menclature Exchange (http://jarvis.neuro.duke.edu/nomen/
index.html, renamed recently to http://avianbrain.org/
nomen/index.html) was established. The expectation was
that Forum attendees would be well versed in the need for
the terminology change, in specic suggestions as to which
structures needed a name change, specic proposals as to
the new names, and the rationale or data supporting any
given proposed name change.
Meeting format
Schedule. The 3-day Forum was organized into three
major goal-oriented blocks. On the rst day, the rationales
E3AVIAN BRAIN NOMENCLATURE FORUM
for specic suggested name changes for subpallial and
some related brainstem cell groups were reviewed and
evaluated, and the Forum voted on the name changes. For
the subpallium and related brainstem cell groups, the
parties recommending name changes differed little among
each other in the cell groups recommended for name
change or in the specics of the proposed new names. The
discussion mainly focused on the evidence for the homol-
ogies underpinning the specic recommended name
changes. On the second day, the rationales and merits for
various specic suggested name changes for the neostria-
tum and hyperstriatum were presented and discussed.
Voting was completed on new names for these structures
on the morning of the third day, and the remainder of the
third day was devoted to the rationales for specic pro-
posed name changes for the archistriatal complex and
voting for new names for this region. The discussion about
the pallial terminology focused on cytoarchitectonic
boundaries, the limits of what the data could conclusively
prove about homology to mammalian structures, and the
esthetics and practicalities (impact on the accessibility of
the avian brain literature) of the specic proposed name
changes for the pallium. The overall discussion and eval-
uation process on each day involved use of computers,
projectors, video-interfaced microscopes, and internet con-
nections to display the data and images required to assess
published and unpublished data favoring or opposing par-
ticular proposals. Discussion was open, and focus was
maintained by a moderator for each session. Discussion/
Data sessions typically were 23 hours in length, sepa-
rated by 1530-minute breaks that were largely charac-
terized by spontaneous small group discussions on the
topic of the preceding formal session.
Attendees. The meeting was attended by 19 faculty-
level neuroscientists (Gregory F. Ball, Laura L. Bruce,
Ann B. Butler, Andra´s Csillag, Sarah Durand, Onur Gu¨n-
tu¨rku¨n, Erich D. Jarvis, Wayne Kuenzel, Diane Lee,
Loreta Medina, Claudio V. Mello, George Paxinos, David
J. Perkel, Alice Powers, Anton Reiner, Toru Shimizu,
Georg Striedter, Stephanie White, and Martin Wild), four
postdoctoral fellows (Gerald Hough, Lubica Kubikova,
Tom V. Smulders, and Kazuhiro Wada), ve graduate
students (Jennifer Dugas-Ford, Haruhito Horita, Scott
Husband, Keiko Yamamoto, and Jing Yu), and one under-
graduate student (Connie Siang). All Forum attendees are
co-authors of this and the companion paper (Reiner et al.,
2004). Attendance at the meeting was open to all who
wished to attend, and travel and lodging costs, as well as
the costs of the meeting itself, were supported by awards
from NSF and NIH for the Forum. An additional 12 indi-
viduals assisted in technical aspects of the Forum, includ-
ing computer network specialists, audio-visual specialists,
a web specialist, microscopy specialists, administrators,
and graduate and undergraduate student assistants.
These persons are listed in the acknowledgments. Erich
Jarvis and Anton Reiner served as co-organizers of the
meeting.
Voting. The planning committee had decided prior to
the meeting that any nomenclature change needed a high
degree of concurrence among Forum attendees if it was to
be widely accepted by the eld as a replacement for any
existing term. We therefore decided changes on a
structure-by-structure basis, with 80% approval required
for acceptance of each new term. Each faculty member
attending was accorded a full vote and each postdoctoral
fellow a half vote. Graduate and undergraduate students
did not vote, but their input was considered. The limits on
student voting were put in place because of the perception
that students were not yet adequately conversant with the
issues of relevance to the terminology revision, whereas
postdoctoral fellows were considered at least partly famil-
iar. For pallial structures, it proved necessary to eliminate
some of the proposed options by simple majority votes,
before a nal vote of approval for a given name change
could be conducted. The nal set of approved new names
for pallial structures was largely an amalgam of the most
highly favored choices from the different sets of proposals.
Guiding principles. In adopting a new terminology,
several guiding principles were embraced. The overall
goals were to remove inaccurate implications of homology
where they existed (notably for the pallium) and to recog-
nize homology where it was amply demonstrated (notably
for brainstem and subpallial structures). Because our in-
tent was to improve communication among avian and
mammalian brain specialists, in the case of instances in
which one-to-one homology (also termed discrete homol-
ogy by Smith, 1967) had been clearly demonstrated, we
believed it highly advantageous to adopt for birds the
same name as used for that structure in mammals (e.g.,
globus pallidus instead of paleostriatum primitivum). The
gain in communication and the already established famil-
iarity of the new avian term (because of its use in mam-
mals) were thought to far outweigh any disadvantages
inherent in abandoning the old name and old abbrevia-
tion. For the pallium, we confronted the issue of whether
sufcient data were available to conclude safely and un-
equivocally that given structures possessed one-to-one ho-
mology with specic structures in mammals. In the end,
we concluded that sufcient evidence did not exist for such
one-to-one equivalences at the pallial level, other than for
the piriform cortex (Karten, 1969, 1991; Bruce and Neary,
1995; Striedter, 1997; Smith-Fernandez et al., 1998; Me-
dina and Reiner, 2000; Puelles et al., 2000; Reiner, 2000;
Butler and Molna´r, 2002; Butler et al., 2002; Wada et al.,
2001).
The goal then became to remove any incorrect connota-
tion of homology to the basal ganglia in the case of those
pallial structures with the term striatumin the name.
Although it was agreed by all that the new names for
these structures should have pallium in the name, several
issues needed to be considered in renaming the pallial
structures that possessed -striatumas a root word in
their outdated name. One major issue was the extent to
which developing new names that allowed retention of
existing abbreviations was desirable and could be
achieved with esthetically pleasing new terms. Alterna-
tively, consideration needed to be given to the possibility
that a new and simple descriptive terminology that did not
retain abbreviations could make avian brain structures
easy to learn and more broadly accessible to neuroscien-
tists. As is clear from the region-by-region commentary in
the companion paper (Reiner et al., 2004), in the end,
retention of abbreviations was found to be highly desirable
for the most intensely studied structures of avian pallium,
so there would be easy linkage and clear continuity be-
tween the literature using old and new terms. Further
information and avian brain images depicting this new
nomenclature are available in Reiner et al. (2004) and on
the Avian Brain Nomenclature Exchange website: http://
avianbrain.org. Further details on the terminology op-
E4 A. REINER ET AL.
tions discussed during the Forum meeting by its attendees
will be presented in a later publication, in a special edition
of Brain, Behavior and Evolution dedicated to the nomen-
clature revision.
Final comments
The Avian Brain Nomenclature Forum was the result of
growing awareness of the communication problems
caused by the faulty and outdated avian brain terminol-
ogy. The Forum sought to devise a new terminology that is
free of errors and promotes accurate understanding of
avian brain organization and evolution. We have been
scrupulous to use only names implying homology that we
are certain would not themselves later prove to be in error.
We believe that the nomenclature changes we have de-
vised can serve the eld well, and we urge all investigators
to use this new terminology. In making its recommenda-
tions for terminology change for specic structures, the
Forum does not mean to imply that the names for all other
structures in the avian brain are adequate and suitable.
Nonetheless, we believe that the names changed by the
Forum are those that were in greatest need of change and
were the greatest hindrance to accurate understanding of
avian brain organization.
ACKNOWLEDGMENTS
Individuals at Duke University who helped with admin-
istrative, technical, and logistical support for the Forum
include: Deepa Bharanidharan (Jarvis Laboratory Associ-
ate in Research), Eunice Chang (Graduate Student), Mar-
garet Couvillon (Graduate Student), Haruhito Horita
(Graduate Student), Susan Havrilesky (Department of
Neurobiology Manager), Michael McElroy (Jarvis Labora-
tory Research Technician), Dawn Kernagis (Jarvis Labo-
ratory Associate in Research), Lisa Moore (Jarvis Labora-
tory Manager), Martha Musson (Department of
Neurobiology Secretary), and Netfriends computer assis-
tants, Ann Sink (Department of Neurobiology coordina-
tor), David Stokes (Web designer), and Tony Zimmermann
(Jarvis Laboratory Research Analyst). We note the valu-
able contributions of Drs. Harvey J. Karten and Luis
Puelles to the discussions on avian brain organization,
development, and evolution that preceded the nomencla-
ture meeting, and we thank Drs. Steve Brauth and Todd
Roberts for making their data on the parrot telencephalon
available to us prior to its publication. A number of other
researchers, too numerous to list here, made valuable
on-line contributions to the discussions in the years lead-
ing up to the Forum. Preparation for the Forum, the
Forum itself, and the dissemination of the conclusions of
the Forum were supported by grants from National Sci-
ence Foundation (NSF) and National Institutes of Health
(NIH). We thank Dr. Israel Lederhendler of National In-
stitute of Mental Health and Drs. Carol van Hartesveldt
and Christopher Platt of NSF for their support and en-
couragement of the Forum enterprise. We also thank the
following who did not attend the Forum for their letters of
support in applying for NIH and NSF funding for the
Forum: Verner P Bingman, Chao Deng, Timothy De-
Voogd, Alison Doupe, Barrie Frost, William Hodos, Gab-
riel Horn, Harvey Karten, Lubor Kostal, Daniel Margo-
liash, Richard Mooney, Sarah Newman, Mary Ottinger,
Giancarlo Panzica, Luis Puelles, Christoph Redies, Lesley
Rogers, and Constance Scharff.
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E6 A. REINER ET AL.
... Visual centers like the Wulst provide spatially mediated associative learning inputs (Atoji and Wild, 2019). The hyperpallium, analogous to parts of the mammalian neocortex, offers processed sensory information (Reiner et al., 2004). Other sources include the nidopallium for somatosensory and auditory inputs, and the dorsolateral corticoid area receiving olfactory inputs, along with projections from numerous other brain regions (Atoji and Wild, 2004). ...
... Subsequent studies have revealed even more diverse connection pathways (Atoji et al., 2016). Despite anatomical differences, significant homologies exist between avian and mammalian hippocampal structures, both of which are pallial in origin (Reiner et al., 2004;Jarvis et al., 2005). Similar to mammals, avian hippocampal subdivisions communicate chemically (Atoji and Wild, 2006;Herold et al., 2015). ...
... Similar data were obtained in E14.5 and E18.5 specimens as well. the correlative chicken LPall sector defined by Puelles et al. [2000] (which had been renamed "mesopallium" in the meantime; Reiner et al. [2004]) for a possible Nr4a2-positive claustrum homolog. We expected to detect a precociously born LPall cell population expressing Nr4a2 selectively. ...
... This subsumes the classical HD and HI components of the Wulst (old densocellular and intermediate hyperstriatum) under a modified "dorsal mesopallium" concept (Md) introduced by Jarvis et al. [2013], as done likewise by Desfilis et al. [2018]. This in principle lumps the former dorsal and ventral parts of the mesopallium (distinguished for instance in the chick brain atlas of Puelles et al. [2007Puelles et al. [ , 2019b, as well as by Reiner et al. [2004]) within the new concept of "ventral mesopallium" (Mv); we already gave some comments on this confusing terminological reclassification in Puelles et al. [2016aPuelles et al. [ , 2017, as well as above in the present essay. The reorganization just brings under the same "mesopallium" classification the otherwise histologically distinct Wulst and mesopallium areas that happen to co-express the selected 5 TFs, probably among many others. ...
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The author worked before on the wide problem of the evolution of the vertebrate pallium. He proposed various Bauplan models based in the definition of a set of pallial sectors with characteristic (topologically invariant) mutual relationships and distinct molecular profiles. Out of one of these models, known as the ‘updated tetrapartite pallium model’, a modified definition of the earlier lateral pallium sector (LPall) emerged, which characterized it in mammals as consisting of an unitary claustro-insular transitional (mesocortical) complex intercalated between neocortex or dorsal pallium (DPall) above and olfactory cortex or ventral pallium (VPall) underneath. A distinctive molecular marker of the early-born deep claustral component of the LPall was found to be the transcription factor Nr4a2, which is not expressed significantly in the overlying insular cortex or in adjoining cortical territories (Puelles 2014). Given that earlier comparative studies had identified molecularly and topologically comparable VPall, LPall and DPall sectors in the avian pallium, an avian Nr4a2 probe was applied aiming to identify the reportedly absent avian claustro-insular complex. An early-born superficial subpopulation of the avian LPall that expresses selectively this marker through development was indeed found. This was proposed to be a claustrum homolog, whereas the remaining Nr4a2-negative avian LPall cells were assumed to represent a possible insular homolog (Puelles et al. 2016a). This last notion was supported by comparable selective expression of the mouse insular marker Cyp26b, also found restricted to the avian LPall (Puelles 2017). Some published data suggested that similar molecular properties and structure apply at the reptilian LPall. This analysis was reviewed in Puelles et al. (2017). The present commentary discusses 3-4 years later some international publications accrued in the interval that touch on the claustro-insular homology hypothesis. Some of them are opposed to the hypothesis whereas others corroborate or support it. This raises a number of secondary issues of general interest.
... The term dorsal medullary lamina was adopted from a similarly located structure identified in birds (designated as the lamina medullaris dorsalis by Karten and Hodos 1967; and renamed lamina pallio-subpallialis, Reiner et al. 2004). Most likely, it is identical to the zona limitans in lizards and crocodiles (Lanuza et al., 1998;Novejarque, Lanuza, and Martínez-García 2004;Billings et al. 2020) and the pallial-subpallial boundary ) of lizards. ...
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The telencephalon of reptiles has been suggested to be the key to understanding the evolution of the forebrain. Nevertheless, a meaningful framework to organize the telencephalon in any reptile has, with rare exception, yet to be presented. To address this gap in knowledge, the telencephalon was investigated in two species of crocodiles. A variety of morphological stains were used to examine tissue in transverse, horizontal, and sagittal planes of sections. Besides providing a description of individual nuclei, brain parts were organized based on two features. One was related to two fixed, internal structures: the lateral ventricle and the dorsal medullary lamina. The other was the alignment of neurons into either layers, cortex, or not, nucleus. Viewed from this perspective, all structures, with limited exceptions, could be accurately placed within the telencephalon regardless of the plane of section. Furthermore, this framework can be applied to other reptiles. A further extension of this scheme suggests that all structures in the telencephalon could be grouped into one of two categories: pallial or basal.
... This theory engendered a lack of communication between avian and mammalian neuroscientists until the beginning of the twenty-first century. To counter this problem a large group of international experts organized the Avian Brain Nomenclature Consortium (Reiner et al. 2004b), and radically changed the popular view of avian brains (Reiner et al. 2004a). Although the avian and the mammalian pallia are organized differently (nuclear versus laminar), they share similarities in neurophysiological functions that are involved in complex cognitive processes. ...
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Psittacines, along with corvids, are commonly referred to as ‘feathered apes’ due to their advanced cognitive abilities. Until rather recently, the research effort on parrot cognition was lagging behind that on corvids, however current developments show that the number of parrot studies is steadily increasing. In 2018, M. L. Lambert et al. provided a comprehensive review on the status of the most important work done so far in parrot and corvid cognition. Nevertheless, only a little more than 4 years after this publication, more than 50 new parrot studies have been published, some of them chartering completely new territory. On the 25th anniversary of Animal Cognition we think this warrants a detailed review of parrot cognition research over the last 4 years. We aim to capture recent developments and current trends in this rapidly expanding and diversifying field.
... The neuroanatomical nomenclature for VTA, SN, and nucleus accumbens were adapted from previous reports in T. guttata and other birds (Bottjer 1993;Székely et al. 1994;Roberts et al. 2002;Reiner et al. 2004;Person et al. 2008;Nordeen et al. 2009;Barr and Woolley 2018). While TH immunofluorescence served as a reliable tool to identify the VTA and SN TH neurons in T. guttata, the stereotaxic atlases of zebra finch brain (Nixdorf-Bergweiler and Bischof 2007; Karten et al. 2013) were used to confirm the location of the VTA/SN in the brain sections. ...
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The mesolimbic dopamine (DA)-pathway regulates food-reward, feeding-related behaviour and energy balance. Evidence underscores the importance of feeding-related neuropeptides in modulating activity of these DA neurons. The neuropeptide, CART, a crucial regulator of energy balance, modulates DA-release, and influences the activity of ventral tegmental area (VTA) DAergic neurons in the mammalian brain. Whether CART- and DA-containing systems interact at the level of VTA to regulate energy balance, however, is poorly understood. We explored the interaction between CART- and DA-containing systems in midbrain of the zebra finch, Taeniopygia guttata, an interesting model to study dynamic changes in energy balance due to higher BMR/daytime body temperature, and rapid responsiveness of the feeding-related neuropeptides to changes in energy state. Further, its midbrain DA-neurons share similarities with those in mammals. In the midbrain, tyrosine hydroxylase-immunoreactive (TH-i) neurons were seen in the substantia nigra (SN) and VTA [anterior (VTAa), mid (VTAm) and caudal (VTAc)]; those in VTA were smaller. In the VTA, CART-immunoreactive (CART-i)-fibers densely innervated TH-i neurons, and both CART-immunoreactivity (CART-ir) and TH-immunoreactivity (TH-ir) responded to energy status-dependent changes. Compared to fed and fasted birds, refeeding dramatically enhanced TH-ir and the percentage of TH-i neurons co-expressing FOS in the VTA. Increased prepro-CART-mRNA, CART-ir and a transient appearance of CART-i neurons was observed in VTAa of fasted, but not fed birds. To test the functional interaction between CART- and DA-containing systems, ex-vivo superfused midbrain-slices were treated with CART-peptide and changes in TH-ir analysed. Compared to control tissues, CART-treatment increased TH-ir in VTA but not SN. We propose that CART is a potential regulator of VTA DA-neurons and energy balance in T. guttata.
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The globus pallidus (GP) of primates is divided conventionally into distinct internal and external parts. The literature repeats since 1930 the opinion that the homolog of the primate internal pallidum in rodents is the hypothalamic entopeduncular nucleus (embedded within fiber tracts of the cerebral peduncle). To test this idea, we explored its historic fundaments, checked the development and genoarchitecture of mouse entopeduncular and pallidal neurons, and examined relevant comparative connectivity data. We found that the extratelencephalic mouse entopeduncular structure consists of four different components arrayed along a dorsoventral sequence in the alar hypothalamus. The ventral entopeduncular nucleus (EPV), with GABAergic neurons expressing Dlx5&6 and Nkx2-1, lies within the hypothalamic peduncular subparaventricular area. Three other formations-the dorsal entopeduncular nucleus (EPD), the prereticular entopeduncular nucleus (EPPRt ), and the preeminential entopeduncular nucleus (EPPEm )-lie within the overlying paraventricular area, under the subpallium. EPD contains glutamatergic neurons expressing Tbr1, Otp, and Pax6. The EPPRt has GABAergic cells expressing Isl1 and Meis2, whereas the EPPEm population expresses Foxg1 and may be glutamatergic. Genoarchitectonic observations on relevant areas of the mouse pallidal/diagonal subpallium suggest that the GP of rodents is constituted as in primates by two adjacent but molecularly and hodologically differentiable telencephalic portions (both expressing Foxg1). These and other reported data oppose the notion that the rodent extratelencephalic entopeduncular nucleus is homologous to the primate internal pallidum. We suggest instead that all mammals, including rodents, have dual subpallial GP components, whereas primates probably also have a comparable set of hypothalamic entopeduncular nuclei. Remarkably, there is close similarity in some gene expression properties of the telencephalic internal GP and the hypothalamic EPV. This apparently underlies their notable functional analogy, sharing GABAergic neurons and thalamopetal connectivity.
Chapter
Brain morphology has become a key element to predict a wide array of cognitive and behavioral, sensory and motor abilities, and to determine evolutionary rates of phenotypic transformation. Our information on early bird brain morphology comes of natural endocasts or studies of the intracranial cavity. Although the first studies of fossil bird brains were published almost two centuries ago, there is still relatively little known about the avian brain and its evolution compared with other groups such as mammals. This is due primarily to the fact that few three-dimensionally preserved skulls of early birds are recognized. The avian brain occupies the entire intracranial cavity, so that it is possible to reconstruct high-quality 3D virtual endocast models that can be used as excellent proxies for both volume and morphology of the brain. This technique has driven advances in avian paleoneurology from 2000 onwards. In this chapter, we provide a holistic view of the main features of the avian brain and senses, its disparity and potential use in paleobiological inferences, and discuss the main changes across the transition from non-avian theropods to derived Neornithes.
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Hummingbirds exhibit complex vocal repertoires that they use in their social interactions. Furthermore, they are capable of vocal production learning, an ability they share with songbirds, parrots, some non-oscine birds, and some mammals including humans. Despite these characteristics, hummingbirds have not received the same attention as other birds, especially songbirds and parrots in the study of vocal communication. Recent studies are advancing our knowledge of vocal communication in hummingbirds showing that these birds exhibit complex social learning and extraordinary abilities for vocal production. Moreover, vocal production learning in hummingbirds provides opportunities to study the evolution and diversification of vocal signals because of the presence of dialects in some species. In addition, the presence of high-frequency vocalizations in some hummingbirds underscores the relevance of these birds to study the evolution of communication signals and sensory adaptations. Not only do some species vocalize at unusually high frequencies compared to other birds, but evidence shows that at least one hummingbird species can hear these sounds, defying what we knew about avian hearing capabilities. Detailed descriptions of the hummingbird syrinx have shown that this organ exhibits homologous structures to those found in the syrinx of oscines, showing that vocal complexity in hummingbirds requires complex syringeal musculature. However, more research is needed to determine whether hummingbirds have unique adaptations that confer exceptional vocal and hearing abilities that exceed those found in other groups of birds.
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Comparative analysis of higher cognitive abilities in animals provides for assessment of the evolutionary underpinnings of the formation of human thought and language. This review will address the main approaches to studies of thought in animals and analyze the data obtained using these approaches. The results of a diversity of tests indicate that animals with high levels of brain development have a wide spectrum of cognitive abilities. As expected, the widest spectrum is found in the great apes. A quite similar spectrum is found in higher members of the class Aves (corvids and psittacines) despite their different brain structure. Convergent similarity in the level of development of cognitive abilities in higher mammals and birds reflects the operation of common factors determining their evolution. Comparison of several corvid and psittacine species indicates that the high levels of development of their cognitive abilities are due to the high levels of organization of the brains of these species rather than ecological characteristics.
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We recently reported that artificial light at night (ALAN), at ecologically relevant intensities (1.5, 5 lux), increases cell proliferation in the ventricular zone and recruitment of new neurons in several forebrain regions of female zebra finches (Taeniopygia guttata), along with a decrease of total neuronal densities in some of these regions (indicating possible neuronal death). In the present study, we exposed male zebra finches to the same ALAN intensities, treated them with 5′-bromo-2′-deoxyuridine, quantified cell proliferation and neuronal recruitment in several forebrain regions, and compared them to controls that were kept under dark nights. ALAN increased cell proliferation in the ventricular zone, similar to our previous findings in females. We also found, for the first time, that ALAN increased new neuronal recruitment in HVC and Area X, which are part of the song system in the brain and are male-specific. In other brain regions, such as the medial striatum, nidopallium caudale, and hippocampus, we recorded an increased neuronal recruitment only in the medial striatum (unlike our previous findings in females), and relative to the controls this increase was less prominent than in females. Moreover, the effect of ALAN duration on total neuronal densities in the studied regions varied between the sexes, supporting the suggestion that males are more resilient to ALAN than females. Suppression of nocturnal melatonin levels after ALAN exhibited a light intensity-dependent decrease in males in contrast to females, another indication that males might be less affected by ALAN. Taken together, our study emphasizes the importance of studying both sexes when considering ALAN effects on brain plasticity.
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Homologies between vertebrate forebrain subdivisions are still uncertain. In particular the identification of homologs of the mammalian neocortex or the dorsal ventricular ridge (DVR) of birds and reptiles is still a matter of dispute. To get insight about the organization of the primordia of the main telencephalic subdivisions along the anteroposterior axis of the neural tube, a fate map of the dorsal prosencephalon was obtained in avian chimeras at the 8- to 9-somite stage. At this stage, the primordia of the pallium, DVR and striatum were located on the dorsal aspect of the prosencephalon and ordered caudorostrally along the longitudinal axis of the brain. Expression of homeobox-containing genes of the Emx, Dlx and Pax families were used as markers of anteroposterior developmental subdivisions of the forebrain in mouse, chick, turtle and frog. Their expression domains delineated three main telencephalic subdivisions in all species at the onset of neurogenesis: the pallial, intermediate and striatal neuroepithelial domains. The fate of the intermediate subdivisions diverged, however, between species at later stages of development. Homologies between forebrain subdivisions are proposed based on the conservation and divergence of these gene expression patterns.
Article
The telencephalon of mammals is characterized by the presence of a hexalaminated structure on its external surface, with specific auditory, visual, somatosensory and motor regions. Due to its seeming unique presence in mammals, it is frequently designated as the neocortex. The evolutionary origins of the so-called neocortex have long puzzled comparative neuroanatomists, in view of the seeming absence of a neocortical-like anlage in nonmammalian amniotes. The resolution of this puzzle requires analysis of both adult and embryonic brains. Experimental neuroanatomical, physiological and behavioral methods applied to adult avian and reptilian brains have finally clarified several fundamental questions regarding the origins of 'neocortex' and have indicated that these origins can be viewed as consequent to two separate events: (1) The elaboration of constituent neuronal populations and their associated connections that are common to the telencephalae of both nonmammalian and mammalian amniotes. In mammals these populations are found within the so-called neocortex. In birds and reptiles, most of these neurons are found within the dorsal and dorsolateral ventricular ridges (DVR and DLVR). (2) In mammals, the components of the DVR and DLVR are incorporated into the thin overlying pallium to form a laminated 'neocortex'. Analysis of development in domestic chicks suggests that the DVR is one of several prosencephalic neuromeres ('Prosomeres') that contribute to the ontogeny of comparable structures in birds. Perhaps in mammals, as well, cortical development is consequent to incorporation of these several prosomeres into proliferative ependyma of the pallial mantle.
Article
The large body of evidence that supports the hypothesis that the dorsal cortex and dorsal ventricular ridge of non-mammalian (non-synapsid) amniotes form the dorsal pallium and are homologous as a set of specified populations of cells to respective sets of cells in mammalian isocortex is reviewed. Several recently taken positions that oppose this hypothesis are examined and found to lack a solid foundation. A cladistic analysis of multiple features of the dorsal pallium in amniotes was carried out in order to obtain a morphotype for the common ancestral stock of all living amniotes, i.e., a captorhinomorph amniote. A previous cladistic analysis of the dorsal thalamus (Butler, A.B., The evolution of the dorsal thalamus of jawed vertebrates, including mammals: cladistic analysis and a new hypothesis, Brain Res. Rev., 19 (1994) 29-65; this issue, previous article) found that two fundamental divisions of the dorsal thalamus can be recognized--termed the lemnothalamus in reference to predominant lemniscal sensory input and the collothalamus in reference to predominant input from the midbrain roof. These two divisions are both elaborated in amniotes in that their volume is increased and their nuclei are laterally migrated in comparison with anamniotes. The present cladistic analysis found that two corresponding, fundamental divisions of the dorsal pallium were present in captorhinomorph amniotes and were expanded relative to their condition in anamniotes. Both the lemnothalamic medial pallial division and the collothalamic lateral pallial division were subsequently further markedly expanded in the synapsid line leading to mammals, along with correlated expansions of the lemnothalamus and collothalamus. Only the collothalamic lateral pallial division--along with the collothalamus--was subsequently further markedly expanded in the non-synapsid amniote line that gave rise to diapsid reptiles, birds and turtles. In the synapsid line leading to mammals, an increase in the degree of radial organization of both divisions of the dorsal pallium also occurred, resulting in an 'outside-in' migration pattern during development. The lemnothalamic medial division of the dorsal pallium has two parts. The medial part forms the subicular, cingulate, prefrontal, sensorimotor, and related cortices in mammals and the medial part of the dorsal cortex in non-synapsid amniotes. The lateral part forms striate cortex in mammals and the lateral part of dorsal cortex (or pallial thickening or visual Wulst) in non-synapsid amniotes. Specific fields within the collothalamic lateral division of the dorsal pallium form the extrastriate, auditory, secondary somatosensory, and related cortices in mammals and the visual, auditory, somatosensory, and related areas of the dorsal ventricular ridge in non-synapsid amniotes.
Article
The evolution of the dorsal thalamus in various vertebrate lineages of jawed vertebrates has been an enigma, partly due to two prevalent misconceptions: the belief that the multitude of nuclei in the dorsal thalamus of mammals could be meaningfully compared neither with the relatively few nuclei in the dorsal thalamus of anamniotes nor with the intermediate number of dorsal thalamic nuclei of other amniotes and a definition of the dorsal thalamus that too narrowly focused on the features of the dorsal thalamus of mammals. The cladistic analysis carried out here allows us to recognize which features are plesiomorphic and which apomorphic for the dorsal thalamus of jawed vertebrates and to then reconstruct the major changes that have occurred in the dorsal thalamus over evolution. Embryological data examined in the context of Von Baerian theory (embryos of later-descendant species resemble the embryos of earlier-descendant species to the point of their divergence) supports a new 'Dual Elaboration Hypothesis' of dorsal thalamic evolution generated from this cladistic analysis. From the morphotype for an early stage in the embryological development of the dorsal thalamus of jawed vertebrates, the divergent, sequential stages of the development of the dorsal thalamus are derived for each major radiation and compared. The new hypothesis holds that the dorsal thalamus comprises two basic divisions--the collothalamus and the lemnothalamus--that receive their predominant input from the midbrain roof and (plesiomorphically) from lemniscal pathways, including the optic tract, respectively. Where present, the collothalamic, midbrain-sensory relay nuclei are homologous to each other in all vertebrate radiations as discrete nuclei. Within the lemnothalamus, the dorsal lateral geniculate nucleus of mammals and the dorsal lateral optic nucleus of non-synapsid amniotes (diapsid reptiles, birds and turtles) are homologous as discrete nuclei; most or all of the ventral nuclear group of mammals is homologous as a field to the lemniscal somatosensory relay and motor feedback nuclei of non-synapsid amniotes; the anterior, intralaminar and medial nuclear groups of mammals are collectively homologous as a field to both the dorsomedial and dorsolateral (including perirotundal) nuclei of non-synapsid amniotes; the anterior, intralaminar, medial and ventral nuclear groups and the dorsal lateral geniculate nucleus of mammals are collectively homologous as a field to the nucleus anterior of anamniotes, as are their homologues in non-synapsid amniotes. In the captorhinomorph ancestors of extant land vertebrates, both divisions of the dorsal thalamus were elaborated to some extent due to an increase in proliferation and lateral migration of neurons during development.(ABSTRACT TRUNCATED AT 400 WORDS)