Revised Nomenclature for Avian Telencephalon and Some Related Brainstem Nuclei

Anton Reiner, David J. Perkel, Laura L. Bruce, Ann B. Butler, A. Csillág, Wayne Kuenzel, Loreta Medina, George Paxinos, Toru Shimizu, Georg Striedter, Martin Wild, Gregory F. Ball, Sarah Durand, Onur Gütürkün, Diane W. Lee, Claudio V. Mello, Alice Powers, Stephanie A. White, Gerald Hough, Lubica KubikovaTom V. Smulders, Kazuhiro Wada, Jennifer Dugas-Ford, Scott Husband, Keiko Yamamoto, Jing Yu, Connie Siang, Erich D. Jarvis

Research output: Article

795 Citations (Scopus)

Abstract

The standard nomenclature that has been used for many telencephalic and related brainstem structures in birds is based on flawed assumptions of homology to mammals. In particular, the outdated terminology implies that most of the avian telencephalon is a hypertrophied basal ganglia, when it is now clear that most of the avian telencephalon is neurochemically, hodologically, and functionally comparable to the mammalian neocortex, claustrum, and pallial amygdala (all of which derive from the pallial sector of the developing telencephalon). Recognizing that this promotes misunderstanding of the functional organization of avian brains and their evolutionary relationship to mammalian brains, avian brain specialists began discussions to rectify this problem, culminating in the Avian Brain Nomenclature Forum held at Duke University in July 2002, which approved a new terminology for avian telencephalon and some allied brainstem cell groups. Details of this new terminology are presented here, as is a rationale for each name change and evidence for any homologies implied by the new names. Revisions for the brainstem focused on vocal control, catecholaminergic, cholinergic, and basal ganglia-related nuclei. For example, the Forum recognized that the hypoglossal nucleus had been incorrectly identified as the nucleus intermedius in the Karten and Hodos (1967) pigeon brain atlas, and what was identified as the hypoglossal nucleus in that atlas should instead be called the supraspinal nucleus. The locus ceruleus of this and other avian atlases was noted to consist of a caudal noradrenergic part homologous to the mammalian locus coeruleus and a rostral region corresponding to the mammalian A8 dopaminergic cell group. The midbrain dopaminergic cell group in birds known as the nucleus tegmenti pedunculopontinus pars compacta was recognized as homologous to the mammalian substantia nigra pars compacta and was renamed accordingly; a group of γ-aminobutyric acid (GABA)ergic neurons at the lateral edge of this region was identified as homologous to the mammalian substantia nigra pars reticulata and was also renamed accordingly. A field of cholinergic neurons in the rostral avian hindbrain was named the nucleus pedunculopontinus tegmenti, whereas the anterior nucleus of the ansa lenticularis in the avian diencephalon was renamed the subthalamic nucleus, both for their evident mammalian homologues. For the basal (i.e., subpallial) telencephalon, the actual parts of the basal ganglia were given names reflecting their now evident homologues. For example, the lobus parolfactorius and paleostriatum augmentatum were acknowledged to make up the dorsal subdivision of the striatal part of the basal ganglia and were renamed as the medial and lateral striatum. The paleostriatum primitivum was recognized as homologous to the mammalian globus pallidus and renamed as such. Additionally, the rostroventral part of what was called the lobus parolfactorius was acknowledged as comparable to the mammalian nucleus accumbens, which, together with the olfactory tubercle, was noted to be part of the ventral striatum in birds. A ventral pallidum, a basal cholinergic cell group, and medial and lateral bed nuclei of the stria terminalis were also recognized. The dorsal (i.e., pallial) telencephalic regions that had been erroneously named to reflect presumed homology to striatal parts of mammalian basal ganglia were renamed as part of the pallium, using prefixes that retain most established abbreviations, to maintain continuity with the outdated nomenclature. We concluded, however, that one-to-one (i.e., discrete) homologies with mammals are still uncertain for most of the telencephalic pallium in birds and thus the new pallial terminology is largely devoid of assumptions of one-to-one homologies with mammals. The sectors of the hyperstriatum composing the Wulst (i.e., the hyperstriatum accessorium intermedium, and dorsale), the hyperstriatum ventrale, the neostriatum, and the archistriatum have been renamed (respectively) the hyperpallium (hypertrophied pallium), the mesopallium (middle pallium), the nidopallium (nest pallium), and the arcopallium (arched pallium). The posterior part of the archistriatum has been renamed the posterior pallial amygdala, the nucleus taeniae recognized as part of the avian amygdala, and a region inferior to the posterior paleostriatum primitivum included as a subpallial part of the avian amygdala. The names of some of the laminae and fiber tracts were also changed to reflect current understanding of the location of pallial and subpallial sectors of the avian telencephalon. Notably, the lamina medularis dorsalis has been renamed the pallial-subpallial lamina. We urge all to use this new terminology, because we believe it will promote better communication among neuroscientists.

Original languageEnglish
Pages (from-to)377-414
Number of pages38
JournalJournal of Comparative Neurology
Volume473
Issue number3
DOIs
Publication statusPublished - máj. 31 2004

Fingerprint

Telencephalon
Terminology
Brain Stem
Amygdala
Basal Ganglia
Globus Pallidus
Birds
Names
Atlases
Brain
Corpus Striatum
Mammals
Locus Coeruleus
Cholinergic Agents
Subthalamus
Aminobutyrates
Neostriatum
Taenia
Subthalamic Nucleus
Diencephalon

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Reiner, A., Perkel, D. J., Bruce, L. L., Butler, A. B., Csillág, A., Kuenzel, W., ... Jarvis, E. D. (2004). Revised Nomenclature for Avian Telencephalon and Some Related Brainstem Nuclei. Journal of Comparative Neurology, 473(3), 377-414. https://doi.org/10.1002/cne.20118

Revised Nomenclature for Avian Telencephalon and Some Related Brainstem Nuclei. / Reiner, Anton; Perkel, David J.; Bruce, Laura L.; Butler, Ann B.; Csillág, A.; Kuenzel, Wayne; Medina, Loreta; Paxinos, George; Shimizu, Toru; Striedter, Georg; Wild, Martin; Ball, Gregory F.; Durand, Sarah; Gütürkün, Onur; Lee, Diane W.; Mello, Claudio V.; Powers, Alice; White, Stephanie A.; Hough, Gerald; Kubikova, Lubica; Smulders, Tom V.; Wada, Kazuhiro; Dugas-Ford, Jennifer; Husband, Scott; Yamamoto, Keiko; Yu, Jing; Siang, Connie; Jarvis, Erich D.

In: Journal of Comparative Neurology, Vol. 473, No. 3, 31.05.2004, p. 377-414.

Research output: Article

Reiner, A, Perkel, DJ, Bruce, LL, Butler, AB, Csillág, A, Kuenzel, W, Medina, L, Paxinos, G, Shimizu, T, Striedter, G, Wild, M, Ball, GF, Durand, S, Gütürkün, O, Lee, DW, Mello, CV, Powers, A, White, SA, Hough, G, Kubikova, L, Smulders, TV, Wada, K, Dugas-Ford, J, Husband, S, Yamamoto, K, Yu, J, Siang, C & Jarvis, ED 2004, 'Revised Nomenclature for Avian Telencephalon and Some Related Brainstem Nuclei', Journal of Comparative Neurology, vol. 473, no. 3, pp. 377-414. https://doi.org/10.1002/cne.20118
Reiner, Anton ; Perkel, David J. ; Bruce, Laura L. ; Butler, Ann B. ; Csillág, A. ; Kuenzel, Wayne ; Medina, Loreta ; Paxinos, George ; Shimizu, Toru ; Striedter, Georg ; Wild, Martin ; Ball, Gregory F. ; Durand, Sarah ; Gütürkün, Onur ; Lee, Diane W. ; Mello, Claudio V. ; Powers, Alice ; White, Stephanie A. ; Hough, Gerald ; Kubikova, Lubica ; Smulders, Tom V. ; Wada, Kazuhiro ; Dugas-Ford, Jennifer ; Husband, Scott ; Yamamoto, Keiko ; Yu, Jing ; Siang, Connie ; Jarvis, Erich D. / Revised Nomenclature for Avian Telencephalon and Some Related Brainstem Nuclei. In: Journal of Comparative Neurology. 2004 ; Vol. 473, No. 3. pp. 377-414.
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T1 - Revised Nomenclature for Avian Telencephalon and Some Related Brainstem Nuclei

AU - Reiner, Anton

AU - Perkel, David J.

AU - Bruce, Laura L.

AU - Butler, Ann B.

AU - Csillág, A.

AU - Kuenzel, Wayne

AU - Medina, Loreta

AU - Paxinos, George

AU - Shimizu, Toru

AU - Striedter, Georg

AU - Wild, Martin

AU - Ball, Gregory F.

AU - Durand, Sarah

AU - Gütürkün, Onur

AU - Lee, Diane W.

AU - Mello, Claudio V.

AU - Powers, Alice

AU - White, Stephanie A.

AU - Hough, Gerald

AU - Kubikova, Lubica

AU - Smulders, Tom V.

AU - Wada, Kazuhiro

AU - Dugas-Ford, Jennifer

AU - Husband, Scott

AU - Yamamoto, Keiko

AU - Yu, Jing

AU - Siang, Connie

AU - Jarvis, Erich D.

PY - 2004/5/31

Y1 - 2004/5/31

N2 - The standard nomenclature that has been used for many telencephalic and related brainstem structures in birds is based on flawed assumptions of homology to mammals. In particular, the outdated terminology implies that most of the avian telencephalon is a hypertrophied basal ganglia, when it is now clear that most of the avian telencephalon is neurochemically, hodologically, and functionally comparable to the mammalian neocortex, claustrum, and pallial amygdala (all of which derive from the pallial sector of the developing telencephalon). Recognizing that this promotes misunderstanding of the functional organization of avian brains and their evolutionary relationship to mammalian brains, avian brain specialists began discussions to rectify this problem, culminating in the Avian Brain Nomenclature Forum held at Duke University in July 2002, which approved a new terminology for avian telencephalon and some allied brainstem cell groups. Details of this new terminology are presented here, as is a rationale for each name change and evidence for any homologies implied by the new names. Revisions for the brainstem focused on vocal control, catecholaminergic, cholinergic, and basal ganglia-related nuclei. For example, the Forum recognized that the hypoglossal nucleus had been incorrectly identified as the nucleus intermedius in the Karten and Hodos (1967) pigeon brain atlas, and what was identified as the hypoglossal nucleus in that atlas should instead be called the supraspinal nucleus. The locus ceruleus of this and other avian atlases was noted to consist of a caudal noradrenergic part homologous to the mammalian locus coeruleus and a rostral region corresponding to the mammalian A8 dopaminergic cell group. The midbrain dopaminergic cell group in birds known as the nucleus tegmenti pedunculopontinus pars compacta was recognized as homologous to the mammalian substantia nigra pars compacta and was renamed accordingly; a group of γ-aminobutyric acid (GABA)ergic neurons at the lateral edge of this region was identified as homologous to the mammalian substantia nigra pars reticulata and was also renamed accordingly. A field of cholinergic neurons in the rostral avian hindbrain was named the nucleus pedunculopontinus tegmenti, whereas the anterior nucleus of the ansa lenticularis in the avian diencephalon was renamed the subthalamic nucleus, both for their evident mammalian homologues. For the basal (i.e., subpallial) telencephalon, the actual parts of the basal ganglia were given names reflecting their now evident homologues. For example, the lobus parolfactorius and paleostriatum augmentatum were acknowledged to make up the dorsal subdivision of the striatal part of the basal ganglia and were renamed as the medial and lateral striatum. The paleostriatum primitivum was recognized as homologous to the mammalian globus pallidus and renamed as such. Additionally, the rostroventral part of what was called the lobus parolfactorius was acknowledged as comparable to the mammalian nucleus accumbens, which, together with the olfactory tubercle, was noted to be part of the ventral striatum in birds. A ventral pallidum, a basal cholinergic cell group, and medial and lateral bed nuclei of the stria terminalis were also recognized. The dorsal (i.e., pallial) telencephalic regions that had been erroneously named to reflect presumed homology to striatal parts of mammalian basal ganglia were renamed as part of the pallium, using prefixes that retain most established abbreviations, to maintain continuity with the outdated nomenclature. We concluded, however, that one-to-one (i.e., discrete) homologies with mammals are still uncertain for most of the telencephalic pallium in birds and thus the new pallial terminology is largely devoid of assumptions of one-to-one homologies with mammals. The sectors of the hyperstriatum composing the Wulst (i.e., the hyperstriatum accessorium intermedium, and dorsale), the hyperstriatum ventrale, the neostriatum, and the archistriatum have been renamed (respectively) the hyperpallium (hypertrophied pallium), the mesopallium (middle pallium), the nidopallium (nest pallium), and the arcopallium (arched pallium). The posterior part of the archistriatum has been renamed the posterior pallial amygdala, the nucleus taeniae recognized as part of the avian amygdala, and a region inferior to the posterior paleostriatum primitivum included as a subpallial part of the avian amygdala. The names of some of the laminae and fiber tracts were also changed to reflect current understanding of the location of pallial and subpallial sectors of the avian telencephalon. Notably, the lamina medularis dorsalis has been renamed the pallial-subpallial lamina. We urge all to use this new terminology, because we believe it will promote better communication among neuroscientists.

AB - The standard nomenclature that has been used for many telencephalic and related brainstem structures in birds is based on flawed assumptions of homology to mammals. In particular, the outdated terminology implies that most of the avian telencephalon is a hypertrophied basal ganglia, when it is now clear that most of the avian telencephalon is neurochemically, hodologically, and functionally comparable to the mammalian neocortex, claustrum, and pallial amygdala (all of which derive from the pallial sector of the developing telencephalon). Recognizing that this promotes misunderstanding of the functional organization of avian brains and their evolutionary relationship to mammalian brains, avian brain specialists began discussions to rectify this problem, culminating in the Avian Brain Nomenclature Forum held at Duke University in July 2002, which approved a new terminology for avian telencephalon and some allied brainstem cell groups. Details of this new terminology are presented here, as is a rationale for each name change and evidence for any homologies implied by the new names. Revisions for the brainstem focused on vocal control, catecholaminergic, cholinergic, and basal ganglia-related nuclei. For example, the Forum recognized that the hypoglossal nucleus had been incorrectly identified as the nucleus intermedius in the Karten and Hodos (1967) pigeon brain atlas, and what was identified as the hypoglossal nucleus in that atlas should instead be called the supraspinal nucleus. The locus ceruleus of this and other avian atlases was noted to consist of a caudal noradrenergic part homologous to the mammalian locus coeruleus and a rostral region corresponding to the mammalian A8 dopaminergic cell group. The midbrain dopaminergic cell group in birds known as the nucleus tegmenti pedunculopontinus pars compacta was recognized as homologous to the mammalian substantia nigra pars compacta and was renamed accordingly; a group of γ-aminobutyric acid (GABA)ergic neurons at the lateral edge of this region was identified as homologous to the mammalian substantia nigra pars reticulata and was also renamed accordingly. A field of cholinergic neurons in the rostral avian hindbrain was named the nucleus pedunculopontinus tegmenti, whereas the anterior nucleus of the ansa lenticularis in the avian diencephalon was renamed the subthalamic nucleus, both for their evident mammalian homologues. For the basal (i.e., subpallial) telencephalon, the actual parts of the basal ganglia were given names reflecting their now evident homologues. For example, the lobus parolfactorius and paleostriatum augmentatum were acknowledged to make up the dorsal subdivision of the striatal part of the basal ganglia and were renamed as the medial and lateral striatum. The paleostriatum primitivum was recognized as homologous to the mammalian globus pallidus and renamed as such. Additionally, the rostroventral part of what was called the lobus parolfactorius was acknowledged as comparable to the mammalian nucleus accumbens, which, together with the olfactory tubercle, was noted to be part of the ventral striatum in birds. A ventral pallidum, a basal cholinergic cell group, and medial and lateral bed nuclei of the stria terminalis were also recognized. The dorsal (i.e., pallial) telencephalic regions that had been erroneously named to reflect presumed homology to striatal parts of mammalian basal ganglia were renamed as part of the pallium, using prefixes that retain most established abbreviations, to maintain continuity with the outdated nomenclature. We concluded, however, that one-to-one (i.e., discrete) homologies with mammals are still uncertain for most of the telencephalic pallium in birds and thus the new pallial terminology is largely devoid of assumptions of one-to-one homologies with mammals. The sectors of the hyperstriatum composing the Wulst (i.e., the hyperstriatum accessorium intermedium, and dorsale), the hyperstriatum ventrale, the neostriatum, and the archistriatum have been renamed (respectively) the hyperpallium (hypertrophied pallium), the mesopallium (middle pallium), the nidopallium (nest pallium), and the arcopallium (arched pallium). The posterior part of the archistriatum has been renamed the posterior pallial amygdala, the nucleus taeniae recognized as part of the avian amygdala, and a region inferior to the posterior paleostriatum primitivum included as a subpallial part of the avian amygdala. The names of some of the laminae and fiber tracts were also changed to reflect current understanding of the location of pallial and subpallial sectors of the avian telencephalon. Notably, the lamina medularis dorsalis has been renamed the pallial-subpallial lamina. We urge all to use this new terminology, because we believe it will promote better communication among neuroscientists.

KW - Basal ganglia

KW - Birds

KW - Brainstem

KW - Evolution

KW - Mammals

KW - Pallium

KW - Telencephalon

KW - Terminology

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