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 In particular, the outdated terminology implies that most of the avian telencephalon is a hypertrophied basal ganglia, when it is now clear that most of the avian telencephalon is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 ␥-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...
We believe that names have a powerful influence on the experiments we do and the way in which we think. For this reason, and in the light of new evidence about the function and evolution of the vertebrate brain, an international consortium of neuroscientists has reconsidered the traditional, 100-year-old terminology that is used to describe the avian cerebrum. Our current understanding of the avian brain -in particular the neocortex-like cognitive functions of the avian pallium -requires a new terminology that better reflects these functions and the homologies between avian and mammalian brains.One hundred years ago, Edinger, the father of comparative neuroanatomy, formulated a unified theory of brain evolution that formed the basis of a nomenclature that has been used to define the cerebral subdivisions of all vertebrates 1 . This resulted in terms and associated concepts such as palaeostriatum, archistriatum, neostriatum and neocortex that are still in common use. According to this theory, the avian cerebrum is almost entirely composed of basal ganglia, the basal ganglia is involved in only instinctive behaviour, and the malleable behaviour that is thought to typify mammals exclusively requires the so-called neocortex. However, towards the end of the twentieth century, there accumulated a wealth of evidence that these viewpoints were incorrect. The avian cerebrum has a large pallial territory that performs functions similar to those of the mammalian cortex. Although the avian pallium is nuclear, and the mammalian cortex is laminar in organization, the avian pallium supports cognitive abilities similar to, and for some species more advanced than, those of many mammals. To eliminate these misconceptions, an international forum of neuroscientists (BOX 1) has, for the first time in 100 years, developed new terminology that more accurately reflects our current understanding of the avian cerebrum and its homologies with mammals. This change in terminology is part of a new understanding of vertebrate brain evolution.In this article, we summarize the traditional view of telencephalic evolution before reviewing more recent findings and insights. We then present the new nomenclature that has been Correspondence to Erich Jarvis at the
Brain evolution is a complex weave of species similarities and differences, bound by diverse rules and principles. This book is a detailed examination of these principles, using data from a wide array of vertebrates but minimizing technical details and terminology. It is written for advanced undergraduates, graduate students, and more senior scientists who already know something about "the brain," but want a deeper understanding of how diverse brains evolved. The book's central theme is that evolutionary changes in absolute brain size tend to correlate with many other aspects of brain structure and function, including the proportional size of individual brain regions, their complexity, and their neuronal connections. To explain these correlations, the book delves into rules of brain development and asks how changes in brain structure impact function and behavior. Two chapters focus specifically on how mammal brains diverged from other brains and how Homo sapiens evolved a very large and "special" brain.
Previous studies concluded that parrots and oscine songbirds, two taxa that have independently evolved the ability to learn vocalizations, possess similar neural circuits for vocal control. These investigations suggested, however, that the vocal control systems of parrots and songbirds may also differ in several respects. Most importantly, auditory inputs to the vocal control system derive from Field L in songbirds, but this area does not appear to project to the vocal control system in parrots. The principal aims in the present study were, therefore, to determine 1) exactly how similar the vocal control system in budgerigars is to that in songbirds and 2) whether the vocal control system in budgerigars receives auditory inputs from areas other than Field L. Biotinylated and fluorescently labeled dextrans were injected into five telencephalic nuclei of the vocal control system in budgerigars and into the physiologically identified auditory portions of the frontal neostriatum and nucleus basalis. The results indicate that the forebrain vocal control system in budgerigars is only superficially similar to that in songbirds. Many of the vocal control nuclei differ between the two taxa in both cytoarchitecture and connections. The nuclei in budgerigars that are comparable to those of the accessory loop of the vocal control system in songbirds, for example, do not form an accessory loop in budgerigars. The vocal control systems in the two taxa differ most significantly in the source of their auditory inputs. In songbirds, auditory information is conveyed to the vocal control system via Field L, whereas, in budgerigars, the auditory inputs to the vocal control system derive from nucleus basalis and the frontal neostriatum. A phylogenetic analysis suggests that the midbrain and medullary vocal control pathways are homologous across all birds, but that most of the vocal control circuits in the forebrain have probably evolved independently in parrots and songbirds.
Although the hippocampus is structurally quite different among reptiles, birds, and mammals, its function in spatial memory is said to be highly conserved. This is surprising, given that structural differences generally reflect functional differences. Here I review this enigma in some detail, identifying several evolutionary changes in hippocampal cytoarchitecture and connectivity. I recognize a lepidosaurid pattern of hippocampal organization (in lizards, snakes, and the tuatara Sphenodon) that differs substantially from the pattern of organization observed in the turtle/archosaur lineage, which includes crocodilians and birds. Although individual subdivisions of the hippocampus are difficult to homologize between these two patterns, both lack a clear homolog of the mammalian dentate gyrus. The strictly trilaminar organization of the ancestral amniote hippocampus was gradually lost in the lineage leading to birds, and birds expanded the system of intrahippocampal axon collaterals, relative to turtles and lizards. These expanded collateral axon branches resemble the extensive collaterals in CA3 of the mammalian hippocampus but probably evolved independently of them. Additional examples of convergent evolution between birds and mammals are the loss of direct inputs to the hippocampus from the primary olfactory cortex and the general expansion of telencephalic regions that communicate reciprocally with the hippocampus. Given this structural convergence, it seems likely that some similarities in the function of the hippocampus between birds and mammals, notably its role in the ability to remember many different locations without extensive training, likewise evolved convergently. The currently available data do not allow for a strong test of this hypothesis, but the hypothesis itself suggests some promising new research directions.
The forebrain auditory, electrosensory, and mechanosensory lateral line pathways in the channel catfish, Ictalurus punctatus, were examined by applying the fluorescent tracer DiI to 1) the auditory part of the torus semicircularis, 2) the electrosensory part of the torus semicircularis, 3) the lateral preglomerular nucleus, and 4) the anterior tuberal nucleus. Three distinct pathways ascend from the torus semicircularis to the telencephalon; they course through either 1) the lateral preglomerular nucleus of the posterior tuberculum, 2) the anterior tuberal nucleus of the hypothalamus, or 3) the central posterior nucleus of the dorsal thalamus. The anatomical data suggest that each of these ascending pathways carries information from more than one sensory modality. The lateral preglomerular nucleus receives an electrosensory input from nucleus electrosensorius in the diencephalon, but it also receives auditory and mechanosensory inputs directly from the torus semicircularis. The anterior tuberal and central posterior nuclei receive primarily auditory and mechanosensory, but also minor electrosensory, inputs. The efferent projections of the central posterior nucleus are presently unknown, but the lateral preglomerular and anterior tuberal nuclei project to nonoverlapping portions of the telencephalon. A cladistic analysis of these indirect torotelencephalic pathways reveals that 1) the pathway through the dorsal thalamus is probably a primitive character for gnathostomes, 2) a well-developed pathway through the posterior tuberculum is probably a derived character for actinopterygian fishes, 3) the pathway through nucleus electrosensorius is probably a derived character for catfishes and gymnotoid teleosts, and 4) auditory pathways through the hypothalamus probably evolved independently in catfishes and frogs.
Numerous scientists have sought a homologue of mammalian isocortex in sauropsids (reptiles and birds) and a homologue of sauropsid dorsal ventricular ridge in mammals. Although some of the proposed theories were enormously influential, alternative theories continued to coexist, primarily because the striking differences in pallial organization between adult mammals, sauropsids, and amphibians enabled different authors to enlist different subsets of similarity data in support of different hypotheses of putative homology. A phylogenetic analysis based on parsimony cannot discriminate between such alternative hypotheses of putative homology, because sauropsids and mammals are sister groups. One solution to this dilemma is to include embryological patterns of telencephalic organization in the comparative analysis. Because early developmental stages in different taxa tend to resemble each other more than the adults do, the embryological data may reveal intermediate patterns of organization that provide unambiguous support for a single hypothesis of putative homology. The validity of this putative homology may then be supported by means of a phylogenetic analysis based on parsimony. A comparative analysis of pallial organization that includes embryological data suggests the following set of homologies. The lateral cortex in reptiles is homologous to the piriform cortex in birds and mammals. The anterior dorsal ventricular ridge in reptiles is probably homologous to the neostriatum and ventral hyperstriatum in birds and to the endopiriform nucleus in mammals. The posterior dorsal ventricular ridge in reptiles is most likely homologous to the archistriatum in birds and to the pallial amygdala in mammals. The pallial thickening in reptiles is probably homologous to the dorsal and intercalated portions of the hyperstriatum in birds and to the claustrum proper in mammals. Finally, the dorsal cortex in reptiles is probably homologous to the accessory hyperstriatum and parahippocampal area in birds and to the isocortex in mammals. These hypotheses of homology imply relatively minor evolutionary changes in development but major changes in neuronal connections. Most significantly, they imply the independent elaboration of thalamic sensory projections to derivatives of the lateral and dorsal pallia in sauropsids and mammals, respectively. They also imply the independent evolution of lamination in the pallium of birds and mammals.
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