The following is a short summary of the historical and current issues
of avian brain anatomical nomenclature. It is written by Erich Jarvis,
with editing input from Toru Shimuzu, Scott Husband, Harvey Karten, Loretta
Medina, Anton Reiner, Luis Puelles, Wayne Kuenzel, George Striedter, Martin
Wild, and Andres Csillag. The links in the text for the figures open a
Tetropod (4-limb) Vertebrate Relationship: The current accepted evolutionary relationship among tetrapod vertebrates is that amphibians evolved from a fish-like (osteichthyes) ancestor in the Devonian period around 400 million years ago (mya); these ancestral amphibians later gave rise to ancestral amniote-reptiles around 340 mya; and these ancestral reptiles gave rise to mammals about 300 mya, and then to birds about 200 mya (Fig. 1). Thus, mammals and sauropsids (birds and reptiles) are sister groups that inherited their brains from a reptilian ancestor. Although these lineage relationships were not as well characterized when nomenclature for the avian brain was devised, the close relationship between reptiles, birds, and mammals was known.
Historical Hypothesis: (This section refers to Figure 2; Click here for Fig. 2) The 100-year old avian terminology, which is still in use today, stated that the 6-9 major subdivisions of the avian telencephalon correspond to different components of the mammalian basal ganglia (Fig. 2). This concept originated in the early 1900s (Edinger et al 1903; Edinger 1908; Elliot-Smith 1910; Elliot-Smith 1919; Johnston 1923), culminating in the definitive document by Ariens-Kappers et al (1936; summarized in Striedter, 1997). Here it was argued that the avian spinal cord, midbrain, and thalamus were highly homologous to those of mammals, but that nearly all of the avian telencephalon corresponded only to mammalian basal ganglia (Fig. 2, purple regions). Thus, the Nissl defined avian telencephalic subdivisions were given names postfixed with a word that defines the mammalian basal ganglia, the striatum: i.e. avian paleostriatum, archistriatum, neostriatum, ectostriatum, and hyperstriatum (Fig. 2). At that time, the major components of the mammalian striatum were thought to be the caudate, putamen, globus pallidus, claustrum, and amygdala (Karten, 1969). Striatum meant a brain region with fibers passing through it, giving it a striatal appearance. The caudate, and sometimes the putamen, was called the neostriatum (new striatum). The globus pallidus was called the paleostriatum (ancient striatum). The amygdala was called archistriatum (original or first striatum). Some, such as Edinger, had considered the head of the caudate to be a separate structure from the rest of the caudate, and called it the lobus parolfactorius. Nearly all of the avian telencephalic subdivisions were based upon these names.
The avian paleostriatum primitivum was given this name because it was thought to be the homologue of a primitive globus pallidus. The avian paleostriatum augmentatum was named because it was thought to be an expansion (augmentation) of the primitive globus pallidus. The avian neostriatum was named because it was thought to be the homologue of the primate caudate, which was thought to be new striatum. Primate caudate and putamen were thought to be separate structures at that time. Avian archistriatum was named because it was thought to be the homologue of the mammalian amygdala. Avian ectostriatum was named because it is a region outside the named paleostriatum. Avian hyperstriatum was named because it was above the named avian neostriatum. Hyperstriatum was further divided into 4 regions: hyperstriatum ventrale (above striatum, ventral region); hyperstriatum dorsale (above striatum, dorsal region), hyperstriatum intercalatus or intercalatum (above striatum, interculated region) and hyperstriatum accessorium (above striatum, additional region). The hyperstriatum accessorium was considered the primitive striatal version of the mammalian cortex (Fig. 2, green regions), whereas the hyperstriatum ventrale and sometimes the hyperstriatum dorsale were considered expansions of the striatum. Avian nucleus basalis was named because it was thought to be homologous to mammalian basal nucleus of Meynert. However, there is not clear consensus if this was the reason why, as basal nucleus of Meynert sits ventral to the globus pallidus in mammals, whereas avian nucleus basalis sits dorsal to the then thought globus pallidus homologue, paleostriatum augmentatum; in the very first sections of the frontal plane, however, avian basalis can appear a little ventral to paleostriatum, or lobus parolfactorius. Avian lobus parolfactorius was named from Edinger's term for the region he considered to be in front of the caudate (Edinger et al 1903) as a brain lobule expanded from the olfactory tuberculum.
There were 3 main reasons that early comparative neuroanatomists named the avian telencephalic structures after the then named mammalian striatal structures: 1) the majority of the avian telencephalon is partly positioned below the lateral ventricle, and in most mammals, the so called striatal regions is partly positioned below the lateral ventricle (Fig. 2, purple regions); 2) both the avian telencephalon and the mammalian striatal regions consist of large conglomerates of cells instead of layers as in the mammalian cortex; and 3) comparative neuroanatomists at the time considered birds to be primarily instinctual animals and mammals to be more behaviorally advanced "up the evolutionary ladder." Following this "ladder" type of evolutionary thinking, Ariens-Kappers et al (1936) and others viewed the brain as having evolved in stages with new telencephalic masses being laid down one on top of the other during evolutionary time, comparable to sediment layers of the Grand Canyon. Ancient vertebrates, such as teleost fish, were thought to have only a paleostriatum primitivum. There then thought to be sequential evolutionary advances, with the addition of the paleostriatum augmentatum first, then the archistriatum, and then the neostriatum. With the appearance of reptiles, they believed there appeared a rudimentary hyperstriatum. With the appearance of birds, the hyperstriatum was thought to have become highly expanded. Then mammals, evolved a new way to do things, the latest advancement, a cortex above the striatum. Using these distinctions as arguments, it was asserted that the layered cortex was the ultimate of brain organization and the cause of more intelligent behavior in mammals, particularly in humans, whose cortex is highly expanded and who are at the top of the evolutionary ladder (Herrick 1956). The basal ganglia were thought to control primitive instinctual behaviors, supporting the association of presumed instinctual behaviors in birds and a corresponding telencephalon composed predominantly of striatum. This was the dominant view up until the mid-1960s.
The Changing Tide: (This section refers to Figure 3; Click here for Fig. 3) In the interim and even before the 1960s, the names and definitions of the mammalian brain structures were changing. The claustrum and the globus pallidus were no longer considered striatal structures. The name paleostriatum for the globus pallidus had fallen out of use. The claustrum is now known to be developmentally derive from primordial cortex. The name archistriatum for the amygdala had also fallen out of use, and the amygdala is now no longer considered part of the basal ganglia. Only the medial part of the amygdala is thought to be striatum-like in function (Swanson & Petrovich 1998) and this is still an issue of debate. The primate caudate and putamen are now known to really be one structure, not two, and together are now called the mammalian striatum. The term neostriatum is still commonly used, but for both caudate and putamen, or in place of striatum in other mammalian species. Other mammalian brain areas once not thought to be striatum are now included as part of the mammalian striatum: the mammalian nucleus accumbens, part of the basal forebrain below the caudate and putamen, continuous with cells below the anterior commissure, all now collectively called the ventral striatum, and the olfactory tubercule, a striatal structure below that (Heimer 2000).
For avian brain structures, in the 1960s, Juorio & Vogt (1967) found that, like the mammalian striatum, the avian paleostriatum augmentatum contains the highest levels of dopamine in the brain. Thereafter, Harvey Karten found that like the mammalian striatum, the avian paleostriatum augmentatum selectively expresses the highest levels of acetylcholinesterase in the telencephalon (Karten 1969). Using these expression profiles, both set of authors argued that only the avian paleostriatum primitivum corresponds to the globus pallidus whereas the paleostriatum augmentatum, and only this region, instead corresponds to the mammalian striatum (caudate/putamen) (Fig. 3, purple regions). Since then, studies examining expression of other genes/molecules (reviewed in Veenman 1997; also see Puelles et al 2000), neuronal connectivity (Bottjer & Johnson 1997; Durand et al 1997; Medina et al 1997; Marin et al 1998; Reiner et al 1998; Csillag 1999; Medina et al 1999), electrophysiological activity (Luo & Perkel 1999a,b; Hessler & Doupe 1999a,b), and gene activity (Jarvis et al 1998), have confirmed that the avian paleostriatum is homologous to the mammalian basal ganglia. It is also now known that birds do not solely exhibit instinctive behaviors. In fact some display complex and presumptive cognitive-like behaviors, i.e. vocal learning, not even found in many mammals, and these behaviors in birds involve both basal ganglia-like and pallial (above the basal ganglia) brain structures (Nottebohm 1972; Brenowitz 1997; Jarvis et al 1998). Nor is there widespread belief in the ascending ladder version of evolution, with humans at the pinnacle of the ladder. Co-evolution is the accepted norm. Recent data in mammals indicate several cortical-basal ganglia pathways may be cognitive pattern generators (Graybiel 1995; Graybiel 1997). For mammals we still are confounded with terms such as subhuman primates, where humans are equally subchimpanzee primates.
Cortex-Layered Hypothesis: (This section refers to Figure 3; Click here for Fig. 3) Based on comparative neuroanatomical connectivity of the avian and mammalian visual pathways, Karten (1969) further argued that the avian ectostriatum is similar to layer IV cells of the mammalian extrastriate visual cortex as both receive primary thalamic visual input (Fig. 3, orange regions). Part of the avian neostriatum is similar to mammalian cortical layers II/III as both receive input from the ectostriatum and layer IV, respectively, and the avian neostriatum, like layers II/III, projects to other cortical regions (Fig. 2C, green regions). Part of the avian archistriatum is similar to mammalian cortical layers V/VI as both receive input from the neostriatum and layers II/III respectively, and both project out of the telencephalon (Fig. 3, yellow regions; Zeier & Karten 1971). The avian auditory pathway follows a similar design (Fig. 3; Karten 1991; Wild et al 1993; Margoliash et al 1994; Mello et al 1998). In general, these pathways were argued to be similar to the mammalian lateral neocortex; the hyperstriatum accessorium and hyperstriatum dorsale were argued to be similar to the mammalian dorsal neocortex, where like the striate cortex, they receive direct projections from retino-recipient thalamic nuclei (Karten et al 1973). This "cortical hypothesis" has been supported and modified by the work of Reiner, Veenman, Shimizu, and others (Veenman et al 1995; Veenman 1997; Veenman et al 1997; Reiner et al 1998; Shimizu & Bowers 1999; Shimizu 2000), as well as by Karten (Karten & Shimizu 1989; Karten 1991; Karten 1997). It is the current dominant alternative hypothesis to the old avian brain hypotheses and its derived nomenclature.
Claustrum-Amygdala Hypothesis: (This section refers to Figure 4; Click here for Fig. 4) Using comparative developmental studies of the reptilian and mammalian brains, in the mid-1920s, Holmgren (1925) argued against the dominant basal ganglia hypothesis of the time. He concluded that the embryonic region called the dorsal ventricular ridge (DVR), which gives rise to most of the reptilian and avian telencephalon, develops from an evagination of the lateral wall of the neural tube at the same location that gives rise to the mammalian claustrum. Holmgren argued that the major subdivisions of the adult avian brain below the lateral ventricle are not striatal, but instead derivatives of this claustrum. Although later put to rest by Ari‘ns-Kappers et al (1936), the claustral hypothesis has been recently revitalized by Striedter (1997), who combined it with amygdala views (Ulinski 1983; Northcutt 1984; Bruce & Neary 1995; Striedter 1997; Rubenstein et al 1998; Puelles et al 1999). Striedter (1997) argued that Karten had correctly shown that the avian paleostriatum augmentatum corresponds to the mammalian striatum, but that the other dorsal avian brain subdivisions of the DVR (archistriatum, neostriatum, ectostriatum, and hyperstriatum ventrale) correspond to an expanded claustrum and amygdala. In the latest model of this hypothesis (Fig. 4) using developmental expression patterns of homeobox genes, Puelles et al (2000) argue that the avian neostriatum is homologous to the mammalian ventral claustrum, the avian hyperstriatum ventrale homologous to the mammalian dorsal claustrum, and avian archistriatum homologous to different parts of the mammalian amygdala. They further argue that the avian hyperstriatum dorsale and hyperstriatum accessorium are homologous to the mammalian neocortex. The latter conclusion has been supported by recent connectivity arguments (Medina & Reiner 2000). In StriedterŐs claustrum-amygdala hypothesis, the similar connectivity design between the avian archistriatum, neostriatum, and hyperstriatum ventrale with the mammalian cortex is argued to have evolved independently (Striedter 1997). One immediate consequence of this hypothesis is to determine the function and detailed connectivity of the mammalian claustrum, which has not been well studied.
The Current Dilemma: Nearly all neurobiologists who are aware of the various hypotheses agree that the current avian nomenclature (Fig. 2) is inaccurate. However, an alternative nomenclature with consensus from the avian scientific community has not been forthcoming. This is in part due to differences between various hypotheses. In the meantime, the current nomenclature leads to false comparisons. For example, Aldridge & Berridge (1998) have performed interesting studies on how the "mammalian neostriatum" controls syntax of grooming movement sequences in rodents. Yet, they make false comparisons with the High Vocal Center (HVC) thought by them to be in the songbird "basal ganglia", i.e. the "avian neostriatum". Although some investigators now include disclaimers in their publications that avian neostriatum is not the same as the mammalian neostriatum, that avian basalis is not the same as mammalian basalis, and that many avian brain regions suffixed with the word striatum are not really striatum, this is unsatisfactory way to bridge the gap between avian, reptilian, mammalian, and others neurobiologists. Indeed, without a useful, updated avian brain nomenclature, many scientists may not even approach the avian literature, or see any relevance in it as applied to their fields. A widespread resolution of these issues requires consensus decision making that most if not all neurobiologists will follow.
Why is a name important: It is dangerous to underestimate the power of names. Names identify an object and have meaning. In the case of the brain, this meaning usually indicates relative location, structure, function, and/or relationship. Name meanings make lasting impressions upon students and scientists. The names often set the level of difficulty or simplicity for learning brain anatomy. The more meaning given to a name, the easier it is to learn and integrate into the larger scheme of neuroscience as a scientific enterprise. Names facilitate or hamper scientific advance. In the present case of outdated avian nomenclature, they most certainly hamper it. Thus, the changes are not deemed as a desirable afterthought, but an absolute necessity.
A Solution: A group called the "ThinkTankers," consisting of Drs. Anton Reiner, Martin Wild, Luis Puelles, Loretta Medina, Georg Striedter, Andreas Csillag, and Wayne Kuenzel, formed in the late 1990's to address this issue. Through email communications amongst themselves and with other neurobiologists on a list server called "avi-eaters", a number of alternative nomenclatures were proposed. These included: naming all of the avian structures based on current proposed mammalian homologues/analogs; using transitional names until an agreement on homologues/analogs is reached; or naming them neutrally with respect to the mammalian brain; and even requesting mammalian neurobiologists to rename some mammalian brain structures. Although some resolutions were reached on the avian basal ganglia-like structures (subpallium) no resolution was in sight for remaining telencephalic regions (pallium). In order to reach a consensus, it was decided to hold a forum in July 2002 with the goal of deciding on new nomenclature. A 2-year discussion-, data-, and hypothesis-building period was deemed sufficient time for the body of scientists from various fields to come to a consensus. The goal of this proposal is to solicit assistance and funds from NIMH to facilitate and ensure that this important and historical forum is successfully carried through.
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