Songbirds and the revised avian brain nomenclature

Abstract

It has become increasingly clear that the standard nomenclature for many telencephalic and related brainstem structures of the avian brain is based on flawed once-held assumptions of homology to mammalian brain structures, greatly hindering functional comparisons between avian and mammalian brains. This has become especially problematic for those researchers studying the neurobiology of birdsong, the largest single group within the avian neuroscience community. To deal with the many communication problems this has caused among researchers specializing in different vertebrate classes, the Avian Brain Nomenclature Forum, held at Duke University from July 18-20, 2002, set out to develop a new terminology for the avian telencephalon and some allied brainstem cell groups. In one major step, the erroneous conception that the avian telencephalon consists mainly 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 new names to reflect their now-evident homologies. The telencephalic regions that were incorrectly named to reflect presumed homology to mammalian basal ganglia have been renamed as parts of the pallium. The prefixes used for the new names for the pallial subdivisions have retained most established abbreviations, in an effort to maintain continuity with the pre-existing nomenclature. Here we present a brief synopsis of the inaccuracies in the old nomenclature, a summary of the nomenclature changes, and details of changes for specific songbird vocal and auditory nuclei. We believe this new terminology will promote more accurate understanding of the broader neurobiological implications of song control mechanisms and facilitate the productive exchange of information between researchers studying avian and mammalian systems.

FIGURE 1

(A) Classical view of avian and mammalian brain relationships according to the historical nomenclature. Although past authors had differing opinions as to which brain regions are part of the pallium versus subpallium, the images are color-coded according to the meaning of the actual names given to these brain regions. White lines represent laminae, cell-sparse regions separating brain subdivisions. Large white areas in the human cerebrum are the fibers bundles making up the white matter. Dashed lines divide regions that differ by cytoarchitecture. The abbreviations PA and LPO designate regions as defined by Karten and Hodos, while the spelled-out term paleostriatum augmentatum designates this entire area as defined by Ariëns-Kappers, Huber and Crosby. (B) Modern view of avian and mammalian brain relationships according to the new nomenclature. In birds, the lateral ventricle is located in the dorsal part of the pallium, whereas in mammals much of the ventricle is located near the border of the pallium with the subpallium. Abbreviations, classical view: Ac=accumbens; Ap=posterior archistriatum; B=nucleus basalis; Cd=caudate nucleus; CDL=dorsal lateral corticoid area; E=ectostriatum; GP=globus pallidus (i=internal segment, e=external segment); HA=hyperstriatum accessorium; HIS=hyperstriatum intercalatum superior; HD=hyperstriatum dorsale; HV=hyperstriatum ventrale; L2=field L2, LPO=lobus parolfactorius, OB=olfactory bulb; PA=paleostriatum augmentatum; Pt=putamen; Tn=nucleus taeniae. Abbreviations, modern view where different from panel A: E=entopallium; B=basorostralis; HA=hyperpallium apicale; HI=hyperpallium intercalatum; HD=hyperpallium densocellulare; Hp=hippocampus; LSt=lateral striatum; MSt=medial striatum; PoA=posterior pallial amygdala; TnA=nucleus taeniae of the amygdala; SpA=subpallial amygdala. (Figure adapted from Jarvis and colleagues.40)

FIGURE 2

Vocal and auditory pathways of the songbird brain within the context of the new avian brain nomenclature. Only the most prominent and/or most studied projections are indicated. For the vocal pathways (A), black arrows show connections of the components (dark grey) of the posterior vocal pathway, white arrows show connections of the components (white) of the anterior forebrain pathway, and dashed lines connections between the two pathways. For the auditory pathway (B), most of the hindbrain connectivity is extrapolated from non-songbird species. For clarity, only the lateral part of the anterior vocal pathway is shown, and the connection from Uva to HVC and reciprocal connections in the pallial auditory areas are not indicated. Note that the NCM and CMM are shown for schematic purposes, as they actually lie in a sagittal plane medial to that depicted, and the pathway from NCM to CMM is not depicted. Abbreviations: Av=avalanche; CLM=caudal lateral mesopallium; CMM=caudal medial mesopallium; CN=cochlear nucleus; CSt=caudal striatum; DM=dorsal medial nucleus; DLM=dorsal lateral nucleus of the medial thalamus; E, entopallium; B=basorostralis; HVC (no formal name other than HVC); LLD=lateral lemniscus, dorsal nucleus; LLI=lateral lemniscus, intermediate nucleus; LLV=lateral lemniscus, ventral nucleus; MLd=dorsal lateral nucleus of the mesencephalon; LMAN=lateral magnocellular nucleus of the anterior nidopallium; Area X=Area X of the medial striatum; MO=oval nucleus of the mesopallium; NCM= caudal medial nidopallium; NIf= nucleus interface of the nidopallium; nXIIts=nucleus XII, tracheosyringeal part; Ov=ovoidalis; PAm=paraambiguus; RAm=retroambiguus; RA=robust nucleus of the arcopallium; SO=superior olive; Uva=nucleus uvaeformis. (Figure adapted from Jarvis and colleagues.40)