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Qt0hj8b785.Pdf UCLA UCLA Previously Published Works Title Avian brains and a new understanding of vertebrate brain evolution. Permalink https://escholarship.org/uc/item/0hj8b785 Journal Nature reviews. Neuroscience, 6(2) ISSN 1471-003X Authors Jarvis, Erich D Güntürkün, Onur Bruce, Laura et al. Publication Date 2005-02-01 DOI 10.1038/nrn1606 Peer reviewed eScholarship.org Powered by the California Digital Library University of California PERSPECTIVES reptiles, to birds and mammals, to primates OPINION and, finally, to humans — ascending from ‘lower’ to ‘higher’ intelligence in a chrono- logical series. They believed that the brains Avian brains and a new understanding of extant vertebrates retained ancestral structures, and, therefore, that the origin of of vertebrate brain evolution specific human brain subdivisions could be traced back in time by examining the brains of extant non-human vertebrates. In The Avian Brain Nomenclature Consortium* making such comparisons, they noted that the main divisions of the human CNS — Abstract | We believe that names have a pallium is nuclear, and the mammalian the spinal cord, hindbrain, midbrain, thala- powerful influence on the experiments we cortex is laminar in organization, the avian mus, cerebellum and cerebrum or telen- do and the way in which we think. For this pallium supports cognitive abilities similar cephalon — were present in all vertebrates reason, and in the light of new evidence to, and for some species more advanced than, (FIG. 1a). Edinger, however, noted that the about the function and evolution of the those of many mammals. To eliminate these internal organization of the telencephala vertebrate brain, an international consortium misconceptions, an international forum of showed the most pronounced differences of neuroscientists has reconsidered the neuroscientists (BOX 1) has, for the first time between species. In mammals, the outer traditional, 100-year-old terminology that is in 100 years, developed new terminology that part of the telencephalon was found to have used to describe the avian cerebrum. Our more accurately reflects our current under- prominently layered grey matter (FIG. 1b, current understanding of the avian brain — standing of the avian cerebrum and its green) whereas the inner part had nuclear in particular the neocortex-like cognitive homologies with mammals. This change in grey matter (FIG. 1b, purple). The inner part functions of the avian pallium — requires a terminology is part of a new understanding was located ventrally to the lateral ventricle. new terminology that better reflects these of vertebrate brain evolution. The outer part was more elaborate and functions and the homologies between In this article, we summarize the tradi- folded in humans than in smaller mammals. avian and mammalian brains. tional view of telencephalic evolution before In non-mammals, the outer and inner parts reviewing more recent findings and insights. of the telencephala were mainly composed One hundred years ago, Edinger, the father We then present the new nomenclature that of nuclear grey matter, most of which was of comparative neuroanatomy, formulated has been developed by the Avian Brain located ventrally to the lateral ventricle in a unified theory of brain evolution that Nomenclature Forum, and discuss its implica- reptiles and birds (FIG. 1b, purple). formed the basis of a nomenclature that has tions for our understanding of vertebrate On the basis of these considerations, been used to define the cerebral subdivisions brain evolution and its associated homologies. Edinger proposed that telencephalic evolu- of all vertebrates1.This resulted in terms and tion occurred in progressive stages of associated concepts such as palaeostriatum, The classical view increasing complexity and size, culminating archistriatum, neostriatum and neocortex The classical view of telencephalic evolution, with the human cerebrum. He suggested that that are still in common use. According to which is still prevalent in classrooms and text- the stages proceeded in a ventral-to-dorsal this theory, the avian cerebrum is almost books, began in the late nineteenth and early direction, with each new vertebrate group entirely composed of basal ganglia, the basal twentieth centuries after the publication of acquiring a more advanced cerebral subdi- ganglia is involved in only instinctive be- The Origin of Species by Darwin2.Inspired by vision, much as the earth’s geological strata haviour, and the malleable behaviour that Darwin’s theory, between 1885 and 1908 formed over time. He proposed that, first, is thought to typify mammals exclusively Edinger formulated an influential, evolution- there was the old brain, the palaeoencephalon requires the so-called neocortex. However, based model of brain organization1,3,4.Edinger (also called the basal ganglia or subpallium at towards the end of the twentieth century, and other early comparative neurobiologists the telencephalic base), which controlled there accumulated a wealth of evidence that combined Darwin’s concept of ‘evolution’ instinctive behaviour, followed by the addi- these viewpoints were incorrect. The avian with the nineteenth-century version of tion of a new brain, the neoencephalon (also cerebrum has a large pallial territory that Aristotle’s ‘scala naturae’, w hich resulted in called the pallium or mantle at the top of the performs functions similar to those of the the view that evolution was progressive and telecephalon), which controlled learned and mammalian cortex. Although the avian unilinear5 — from fish, to amphibians, to intelligent behaviour4.He, Ariëns Kappers NATURE REVIEWS | NEUROSCIENCE VOLUME 6 | FEBRUARY 2005 | 151 PERSPECTIVES Box 1 | Avian Brain Nomenclature Consortium this input originated from neurons in the midbrain19,20.During the following decades, Authors are ordered alphabetically in two groups: the first group, along with the first two and using new methods in double-label immuno- last two authors, are the core Avian Brain Nomenclature Forum Thinktank group; the second histochemistry and tract tracing, the mam- group are professors, postdoctoral fellows and students who also participated in the Avian Brain malian neostriatum was found to be enriched Nomenclature Forum. (For author affiliations see online supplementary information S1 (box).) in two types of neuron: those containing the Erich D. Jarvis, Onur Güntürkün, Laura Bruce, András Csillag, Harvey Karten, Wayne Kuenzel, neuropeptide substance P (SP), which project Loreta Medina, George Paxinos, David J. Perkel, Toru Shimizu, Georg Striedter, J. Martin Wild. to the internal part of the globus pallidus Gregory F.Ball, Jennifer Dugas-Ford, Sarah E. Durand, Gerald E. Hough, Scott Husband, Lubica and substantia nigra, and those containing Kubikova, Diane W. Lee, Claudio V.Mello, Alice Powers, Connie Siang, Tom V.Smulders, the neuropeptide enkephalin (ENK), which Kazuhiro Wada, Stephanie A. White, Keiko Yamamoto, Jing Yu, Anton Reiner and Ann B. Butler. project to the external part of the globus pallidus21–24.In birds, SP and ENK neurons are and others named the telencephalic subdivi- The fish pallium was named ‘palaeocortex’, enriched in the palaeostriatum augmentatum sions within each vertebrate group with the and was proposed to be the antecedent of (including the LPO)24,25, and, like the equiva- prefixes ‘palaeo’ (oldest),‘archi’ (archaic) and the human olfactory cortex. Reptiles were lent neurons in mammals, project to different ‘neo’ (new) to designate the presumed rela- thought to have evolved an ‘archicortex’,also cell types within the adjacent avian palaeo- tive order of evolutionary appearance of thought to be olfactory and primitive, that striatum primitivum. In both birds and mam- each subdivision. In Greek,‘archi’ means the was said to be the antecedent of the human mals, the SP neurons seem to be involved in oldest, the first, or the most primitive, hippocampus. Birds were thought not to promoting planned movement, whereas the whereas ‘palaeo’ means ancient, primitive or have evolved any further pallial regions. By ENK neurons seem to have a role in inhibiting old, but not necessarily the oldest. Both contrast, mammals were thought to have unwanted movement. Further functional Edinger and Ariëns Kappers misinterpreted evolved the latest and greatest achievement, a studies revealed that both the mammalian the meaning of these prefixes and reversed ‘neocortex’, from the palaeocortex and/or neostriatum and the avian palaeostriatum aug- them, naming structures with ‘palaeo-’ to archicortex6.The archicortex and/or palaeo- mentatum (including the LPO) participate not indicate the oldest or first and ‘archi-’ to indi- cortex,with their 2–3 cell layers, were assumed only in instinctive behaviour and movement, cate old. They added to these prefixes the root to be primitive; the neocortex, with its 6 lay- but also in motor learning 26,27. word ‘striatum’ for the presumed palaeo- ers, was assumed to be more recently evolved These apparent relationships between the encephalic subdivisions and ‘pallium’ or and a substrate for more sophisticated subpallia of mammals and birds have been ‘cortex’ for the presumed neoencephalic sub- behaviour. supported by molecular embryology stud- divisions1,4,6–8.The term ‘striatum’ was used There were dissenting voices to the clas- ies24,28–31.The developing subpallium in birds because a large part of the basal ganglia sical view10–12.Some of its proponents also and mammals consists of two separate histo- (palaeoencephalon) in mammals,
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