AVIAN BRAIN NOMENCLATURE FORUM
18-20 JULY, 2002 - DURHAM (NC, USA)
PROPOSAL FOR NEW NOMENCLATURE - July 2, 2002
This proposal is a revised version of a previous one done in collaboration with Luis Puelles, to which I have incorporated some suggestions done by some avietaers (to whom I am very grateful). I thank long and productive discussions on the development and evolution of the brain, and on a possible new avian brain nomenclature maintained during several years with Luis Puelles. I also thank discussions and input on a possible new avian brain nomenclature from George Paxinos and Salvador MartÌÐnez, as well as comments and criticisms to previous versions of this proposal provided by Georg Striedter, David Perkel, Christoph Redies, Harvey Karten, Erich Jarvis, Tony Reiner, Laura Bruce, Wayne Kuenzel, Gregory F. Ball, Andras Csillag and all participants of the avi-eater list. Finally, I would like to add that -in a similar spirit to that clarified by Georg Striedter, David Perkel, Tony Reiner, Andras Csillag and all other participants at the Forum- I will go to this meeting with an open mind, prepared to debate the different issues, and happy to support any other proposal or part of it that seems appropiate.
1. OLD NAMES VERSUS NEW NAMES.
The names currently employed for the avian telencephalon were first applied when knowledge on the non-mammalian brain and techniques for studying the brain were both very poor and limited (Huber and Crosby, 1929; AriÌÇns-Kappers, Huber and Crosby, 1936). The inherited names that we commonly employ for the avian brain are represented in the most popular avian brain atlases (on the pigeon brain: Karten and Hodos, 1967; on the chicken brain, Kuenzel and Masson,1988; see also Dubbeldam, 1998). These names have been very useful and have provided a basic framework for studies of the avian brain during many decades. During the last three decades, our knowledge on the development and on the anatomical and functional organization of the avian brain has considerably increased. As a consequence, our current understanding of the basic organization of the avian brain is clearly better. In particular, the data collected during the last three decades have radically changed our conception of the telencephalon, considered in the distant past to be mostly striatal-like, to our modern view of the avian telencephalon consisting of large pallial as well as subpallial divisions. This irreversible development brings us closer to present concepts on the mammalian telencephalon, and makes us uncomfortable with a number of inherited names with the suffix -striatum and implying a striatal homology (for example, neostriatum, hyperstriatum) applied to structures that we now know are pallial (and, therefore, non-striatal). In addition, the weird-sounding names of many avian telencephalic structures (for example, paleostriatum augmentatum) have made the avian brain studies inaccessible to non-avian neuroscientists, or the data from avian brain studies have been erroneously interpreted by non-avian neuroscientists. All of this has inspired the present willingness among avian neuroscientists for changing the names of the avian telencephalon.
What should the new names be like? Should they be homology-based or independent from any homology? In order to make the nomenclature change less traumatic, should we keep the initials (or abbreviations) of the old names and try to find new names having the same initials but different meaning? As long discussed by many authors through the avi-eaters list and dinner meetings during the past years, all of these options have advantages and disadvantages, which we will not enter to explain here again. In our own search of good and useful names and abbreviations, we applied the following general rules:
1) In cases of structures of evident homology with mammalian counterparts, accepted by a vast majority (at least 90-95% of avian neuroscientists), the new names should be homology-based (example: pallium versus subpallium; parts of the basal ganglia in the subpallium; see below). In these cases, the new names should facilitate the direct understanding of the structure to both avian and non-avian neuroscientists. This essential advantage should overcome the radical change in both names and abbreviations (for example, from paleostriatum augmentatum or PA to lateral striatum or LSt).
2) In cases of structures with partly unknown or controversial homology relationships (for example, many pallial subdivisions), the new names should reflect topological position, which provides cues on invariant location relative to neighbouring structures in different avian species (for example, from neostriatum or N to epistriatal pallium or E).
In these cases, the names and abbreviations should change as little as possible, and should respect the particular adjectives given to specific areas or nuclei described inside the major territories (for example, no change for Field L and High Vocal Center; minor changes in some cases, like passing from oval nucleus of the anterior neostriatum or NAo to oval nucleus of the anterior epistriatal pallium or EAo).
The reasons that support each specific change are explained below, and the changes can be found in an accompanying Table at the end.
2. CONSIDERATIONS ON THE TELENCEPHALON.
The telencephalon is a paired structure classically described as the rostralmost or rostrodorsal part of the forebrain in all vertebrates, directly related to paired olfactory evaginations (olfactory bulbs), from which each telencephalic hemisphere receives direct olfactory input. In addition to the olfactory input, in all vertebrates the telencephalon receives other types of sensory, multimodal or modulatory information from the brainstem (mainly the thalamus and hindbrain), and contains centers for sensorimotor, limbic and emotional proccessing, subserving as well memory formation. The brainstem input, as well as the relative size and functional importance of the telencephalon, dramatically increase in amniotes (mammals, birds and reptiles). The telencephalon appears as a pair of evaginated vesicles in most vertebrates, although they are everted in some fish groups (Actinopterygians).
There is general agreement that the telencephalon is, as a brain part, homologous across all gnathostomes, due to its conserved topology, independently of the various forms, sizes, histological organizations, connections and functions that present in different animal groups (Holmgrem, 1922, 1925; Kuhlenbeck, 1973; Northcutt, 1995; Striedter, 1997; Nieuwenhuys, 1998). Further supporting this, some basic traits are common in the telencephalon of all vertebrates, including agnathans.
3. MAJOR HISTOGENETIC DIVISIONS OF THE TELENCEPHALON.
A large amount of data supports that the telencephalon in all vertebrates has two major histogenetic divisions: the pallium and the subpallium. The existence of these two divisions is based on developmental, molecular, and connectivity data explained below. If we consider the telencephalon isolated from the rest of the brain, the pallium is located at the top of the telencephalic vesicle, covering the subpallium, which is located in the apparent “base” of the hemisphere (basal or ventral telencephalon). However, this classic view of the pallium as dorsal and subpallium as ventral is contradicted by data from fate map experiments in tetrapods (for example, Cobos et al., 2001a), and generates difficulties and much confussion when we consider the telencephalon as an integral part of the forebrain. The pallial and subpallial divisions are specified very early in development and are soon revealed by evolutionarily conserved expression of different sets of developmental regulatory genes (or master genes). As a consequence of their different master gene expression, these divisions develop into distinct histogenetic territories showing different architecture, cell types, connections and function. The pallium typically expresses members of the T-brain, Emx and Pax homeobox gene families during development, and mainly produces glutamatergic neurons involved in excitatory connections. The subpallium typically expresses some Dlx and Nkx homeobox genes during development and gives rise mainly to GABAergic neurons involved in inhibitory circuitries and projections. A third radial histogenetic area (called by developmental neurobiologists the anterior entopeduncular area; see Puelles et al., 2000; MarÌÐn and Rubenstein, 2001) is described at the transition between subpallial and preoptic regions in all vertebrates (in the telencephalic stalk or telencephalon impar), based on the expression of the gene Sonic hedgehog (Shh) on top of the other subpallial markers. This general area seems related to the basal forebrain cholinergic cell groups. Some groups of large cholinergic neurons partially invade the rest of the subpallium, and many subpallial GABAergic cells invade tangentially the whole pallium, where they become inserted as inhibitory interneurons of various types (the latter process seems to operate in mammals, birds - Cobos et al., 2001b- and possibly in other vertebrates as well).
These basic developmental traits characterize the pallium or the subpallium/entopeduncular area in fishes (Murakami et al., 2001; Hauptmann et al., 2002; Wullimann and Rink, 2002), amphibians (MarÌÐn et al., 1998; Smith-FernÌÁndez et al., 1998; Brox et al., 2002), reptiles (Reiner et al., 1984; 1998; Reiner, 1991; 1993; Medina and Reiner, 1995; Smith-FernÌÁndez et al., 1998; Fowler et al., 1999), birds (Veenman and Reiner, 1994; 1996; Veenman et al., 1995; Medina and Reiner 1995; 2000; Reiner et al., 1984;1998; Puelles et al., 2000), and mammals (Reiner et al., 1984;1998; Puelles et al., 2000; MarÌÐn and Rubenstein, 2001). Both the pallium and subpallium as such are considered homologous across all vertebrates or, at least, all gnathostomes.
Based on these traits, the pallium in birds includes the currently named hippocampal complex (hippocampus and parahippocampal area), the whole hyperstriatum, the neostriatum, the olfactory pallial areas (cortex piriformis) and the majority of the archistriatum. On the other hand, the avian subpallium/entopeduncular area consists of the lobus parolfactorius, the paleostriatum augmentatum, the paleostriatum primitivum, the majority of the septum and several basal forebrain groups that include the large cholinergic cells and the stria terminalis nuclear complex (part of it erroneously named nucleus accumbens in the past; see below). It is not definitively clear at present whether a small part of the archistriatum is also subpallial (Puelles et al., 2000; Jarvis and Mello, 2000; Redies et al., 2001; see recent discussion in the avieater list). In any case, the archistriatal complex is in a topological position and shows connections and neurochemical features that strongly support that it is homologous as a field to part of the amygdala of mammals (Zeier and Karten, 1971; Striedter, 1997; Puelles et al., 2000). This is based on the following facts: (1) the archistriatum is located in the caudal and lateroventral part of the telencephalon, showing a topological position and developmental origin identical to that of the amygdala (Striedter, 1997; Puelles et al., 2000); note that this is a very important condition for homology; (2) Like the mammalian amygdala, the avian archistriatum receives inputs from other parts of the pallium, including the hippocampal complex and some associative pallial areas (like NCL), and from some multimodal dorsal thalamic nuclei (Wild et al., 1993; Veenman et al., 1995; KrÌ¦ner and GÌ¹ntÌ¹rkÌ¹n, 1999); (3) Like the mammalian amygdala, the avian archistriatum projects to the striatum and bed nucleus of the stria terminalis, as well as to the hypothalamus and several brainstem areas through the so-called occipitomesencephalic tract (Zeier and Karten, 1971; Nottebohm et al., 1976; Wild, 1993; Wild et al., 1993; Veenman et al., 1995; Davies et al., 1997; Dubbeldam et al., 1997; KrÌ¦ner and GÌ¹ntÌ¹rkÌ¹n, 1999); (4) Like the mammalian amygdala, the avian archistriatum is involved in memory, sensorimotor and viscerolimbic functions (Cohen, 1975; Ramirez and Delius, 1979; Knudsen et al., 1995; Knudsen and Knudsen, 1996; Lowndes and Davies, 1995). The amygdala in mammals is known to have pallial and subpallial components (Swanson and Petrovich, 1998; Puelles et al., 2000). Since we cannot be sure at this moment whether the avian archistriatum is completely pallial or whether it contains a small subpallial part, I preferred not to include this territory within the pallium/subpallium divisions, but to treat it as a separate telencephalic structure which I propose to call the amygdaloid complex. Note that amygdaloid is the same as amygdala-like (term suggested by some avieaters), and that this term applied to the archistriatum does not exclude the possibility of adding other neighbouring telencephalic structures to the amygdaloid complex (for example, NCL: see discussion in Redies et al., 2001, page 280, first column, third paragraph; another example, nucleus taeniae: Thompson et al., 1998; Cheng et al., 1999). The concept of mammalian amygdala, including the extended amygdala, seems elastic enough to be able to encompass any eventual advances in comparative analysis with the avian counterpart. Against opinions to the contrary, I believe that the concept of amygdala will continue to be used in neuroscience.
Several avian neuroscientists prefer to use a neutral term to rename the avian archistriatum because either they are not convinced by the evidence for the homology of the whole archistriatum with the mammalian amygdala, or they say that the archistriatum is comparable to only part of the mammalian amygdala, or they consider that there are too many things unknown about what other structures of the avian telencephalon may be part of the avian amygdala. To resolve this, Striedter and Perkel have proposed to call the avian archistriatum as Region A, a term that has two advantages: it is neutral and helps to retain the abbreviations. However, I prefer to keep the proposal of amygdaloid complex because, in my opinion, the evidence that support the homology of the whole archistriatum (as a histogenetic field) to part of the amygdala is strong and solid (reasons and references in the previous paragraph). In my opinion, the term “amygdaloid” makes reference to the fact that the adult derivatives in mammal and bird of this histogenetic telencephalic territory are not completely identical. As noted above, this term also leaves open the possibility of adding more parts of the avian telencephalon to the complex.
3A) THE PALLIUM (P).
As noted above, the avian pallium includes the hippocampal complex (hippocampus and parahippocampal area), the hyperstriatum, the neostriatum, the olfactory pallial areas (cortex piriformis) and the majority of the archistriatum. Excluding the archistriatum from this section, the rest of the avian pallium can be divided into four major anatomical and functional subdivisions (Karten, 1991; Butler, 1994; Striedter, 1997; Medina and Reiner, 2000; Puelles et al., 2000), which from medial to lateroventral are:
a) the hippocampal complex, in the medial part of the pallium, which includes the hippocampus (Hp) and the parahippocampal area (APH). This territory expands dorsolaterally at caudal levels, as the Wulst disappears, accompanying the expansion of the lateral telencephalic ventricle (Casini et al., 1986; Bingman et al., 1987; Shimizu and Karten, 1990; Erichsen et al., 1991; Krebs et al., 1991; Sherry et al., 1992; SzekÌ©ly, 1999; Atoji et al., 2002). A recent study of the chicken telencephalon suggests that the main part of the area corticoidea dorsolateralis (CDL, located above the lateral ventricle) represents a caudolateral extension of the APH and belongs to the hippocampal complex (Redies et al., 2001).
b) the Wulst (German term that means bulge), in the dorsomedial part of the pallium, which includes the hyperstriatum accessorium (HA), the hyperstriatum intercalatus superior (HIS) and the hyperstriatum dorsale (HD) (Karten et al., 1973; Bagnoli and Burkhalter, 1983; Miceli and RepÌ©rant, 1983; 1985; Reiner and Karten, 1983; Shimizu and Karten, 1990; GÌ¹ntÌ¹rkÌ¹n, 1991; Medina and Reiner, 2000). It is located between the medially situated hippocampal complex and more lateral pallial regions. A shallow superficial groove, called vallecula, demarcates the lateral boundary of the Wulst. In some birds (like the owl), the Wulst expands dorsolaterally to cover most of the dorsal telencephalic surface (Karten et al., 1973). The Wulst is no longer present at caudal telencephalic levels, where the parahippocampal area (including the area corticoidea dorsolateralis or CDL) and the lateral telencephalic ventricle expand laterally, and the vallecula is no longer observed.
c) the hyperstriatum ventrale (HV), in the intermediate part of the pallium, between the Wulst and the Neostriatum (RehkÌÛmper et al., 1984; Reiner et al., 1989; Csillag et al., 1994; Brauth et al., 1994; Striedter, 1994).
d) the neostriatum (N), in the ventral part of the pallium, just above the striatum (Karten and Hodos, 1970; RehkÌÛmper et al., 1985; Arends and Zeigler, 1986; Dubbeldam and Visser, 1987; Wild, 1987; 1992; 1994; Wild et al., 1985;1993; Brauth et al., 1994; Striedter, 1994; Metzger et al., 1998; KrÌ¦ner and GÌ¹ntÌ¹rkÌ¹n, 1999). The neostriatum includes the specialized ectostriatum, nucleus basalis and field L areas.
Both the HV and N form the avian dorsal ventricular ridge (DVR), and show olfactory-recipient areas adjacent to the surface (cortex piriformis or CPi; Reiner and Karten, 1985).
The division of the avian pallium in at least these four territories is also supported by molecular and developmental data (KÌÛllÌ©n, 1962; Smith-FernÌÁndez et al., 1998; Puelles et al., 2000; Redies et al., 2001).
To name these four pallial divisions without using potentially controversial homology postulates (in comparison with mammalian pallial divisions), I propose to either keep some of the known names (for example, hippocampus or Wulst), or - when needed- to substitute the names containing the suffix -striatum by names having a combination of the terms pallium plus a topological term (for example, intermediate pallium to refer to the hyperstriatum ventrale) (see Table). For some pallial subdivisions in which topological terms may lead to apparent confusion (for example, in the Wulst), we can change to a partially numeric terminology (see below and Table):
a) hippocampal complex (abbreviated H), including Hp, APH and CDL. NO CHANGE. As an alternative, the CDL could be renamed as caudolateral APH (APHcl), and the name restricted to this specific part of the hippocampal complex, as defined in Redies et al. (2000).
b) Wulst pallium, abbreviated W. For the suddivisions of the Wulst, Luis Puelles and I previously proposed to use topological position: HA changes to medial Wulst (WM); HIS changes to intercalated Wulst (WI); HD changes to lateral Wulst (WL); the part of the Wulst called lateral hyperstriatum (HL) located near the pial surface (superficial to HD; Shimizu and Karten, 1990) may be called the superficial lateral Wulst (WLs). (to understand the topological (not simply topographic) position of Wulst subdivisions, see Medina and Reiner, 2000). However, the major problem with this is that many avieaters would prefer to use the topographic terms based on how we see these Wulst subdivisions in frontal or sagittal sections, particularly in birds with a large Wulst (like owls): using topographic criteria, the HA may be seen just as dorsal, and the HD as ventral. However, we strongly disliked these topographic terms because they involve wrong topological position for entities that extend from the ventricle to the pial surface and, as explained above, topology is a very important criterion for understanding the brain basic units and for comparisons among vertebrates (see also Kuhlenbeck, 1973; Nieuwenhuys, 1998). As an alternative, Wayne Kuenzel have suggested using numeric names for Wulst subdivisions, and I support this proposal: HA can change to W1; HIS can change to W2; HD can change to W3 (see Table). Other possibility is to keep the adjectives accessory and intercalated for the HA and HIS parts of the Wulst (abbreviated WA and WI), respectively, and to use the term paraintercalated Wulst (abbreviated WPI) to refer to the HD of the current nomenclature. In this way we keep some of the subdivision adjectives and remove the misleading term “dorsal”. Nevertheless, we still prefer the topological terms applied to Wulst subdivisions because, in our opinion, they would help non-avian neuroscientists to understand better the position of these areas, and this may contribute to a more extended consideration of avian brain research. In the abbreviations, we prefer to keep W first, as a reference to the common denominator of all subdivisions and to have all parts together alphabetically (in abbreviation lists). MODERATE CHANGES. The term Wulst seems to have a good acceptance among many avieaters. However, Helmut Wicht noted that this is an ugly term in comtemporary German. As an alternative, we could use the term dorsal or dorsomedial pallium.
c) HV can change to intermediate pallium, abbreviated I. The term makes reference to its topological position within the pallium. The well-known dorsal and ventral subdivisions of HV will change to dorsal intermediate pallium (ID) and ventral intermediate pallium (IV), respectively. The nuclei described in the frontal/anterior part of the HV in chicken and budgerigar (HVn, HVo, lAHV; Brauth et al., 1994; Durand et al., 1997; Jarvis and Mello, 2000; Redies et al., 2001) can be called the nucleus of the intermediate pallium (In), or the oval and lateral nuclei of the anterior intermediate pallium (Ino, Inl) (see Table for other examples). As for the Wulst, in the abbreviations we prefer to keep I first, as a reference for the common denominator of all subdivisions of the intermediate pallium and to evade alphabetical chaos. CHANGES EASY TO REMEMBER. As proposed by Striedter and Perkel, and suggested to us by Redies, a possible alternative name for HV could be to use “Region HV” of the pallium (or HV pallium), with the advantage of keeping abbreviations. This name, however, will not help mammalian and other non-avian scientists.
d) N can change to epistriatal pallium, simply abbreviated E. This term (which is not used that consistently in the classic literature -Edinger, Elliot Smith, etc‰¥Ïsee Striedter,1997) makes reference to the topological position in the pallial region just above the striatum. Note that “epi” means “above”. The different subdivisions of N (frontal-NF, intermediate-NI, caudal-NC, lateral-NL, etc.) can easily be changed to EF, EI, EC, EL, etc.. Similarly, the caudolateral neostriatum (NCL), can be changed directly to epistriatal caudolateral pallium (ECL). Some of the specific sensory nuclei or areas of the N can either retain their name (for example, ectostriatum, field L, nucleus interfacialis, etc.), or change slightly (nucleus basalis may change to nucleus basalis trigemini, abbreviated BT, as suggested by Harvey Karten, to avoid confusion with mammalian or avian basal magnocellular nucleus, which is located in the subpallium and contains cholinergic neurons). Other specific areas or nuclei of N, like those related to hearing and vocal circuitries in budgerigars and oscine songbirds (MAN, NAo, NLc, etc.; Brauth et al., 1994; Striedter, 1994; Jarvis and Mello, 2000), can easily change name by substituting N for E (example, MAE, EAo, ELc, etc.; see Table for other examples). Similarly, the recently described neostriatal island field of chicken (NIF; Redies et al., 2001) can easily change to epistriatal island field (EIF; this general term could include both the ectostriatal and neostriatal island fields described at intermediate and more caudal N levels in chick, Redies et al., 2001). The new name and abbreviation (EIF) would avoid current confusion of this area with the interfacial nucleus (Nif) of songbirds, which -as proposed above- can keep both name and abbreviation. Other centers, such as the High Vocal Center (HVC) of songbirds, as well as the shelf and the para-HVC (Nottebohm et al., 1976; Wild, 1994; Fortune and Margoliash, 1995; Vates et al., 1996; Foster and Bottjer, 1998; Mello et al., 1998) can retain their name and abbreviation. CHANGES EASY TO REMEMBER or NO CHANGES. As proposed by Striedter and Perkel, and suggested to us by Redies, a possible alternative name for N could be Region N of the pallium (or N pallium), with the advantage of keeping abbreviations. This name, however, will not help mammalian and other non-avian scientists. On the hand, one of the problems with using the terms epistriatum (meaning above the striatum) or ectostriatum (meaning outside the striatum) is that not many avieaters are familiarized with Latin terms, and do not know the exact meaning of “epi” or “ecto” (this problem was also pointed out by Onur GÌ¹ntÌ¹rkÌ¹n, Laura Bruce, Tony Reiner and others). Thus, some people with not enough knolowledge on Latin terms may erroneously think that the epistriatum or the ectostriatum are parts of the striatum. To avoid this problem, an alternative name for epistriatal pallium could be ventral pallium (note that this term is currently employed in some publications in the avian brain by Puelles, Redies, Medina and collaborators; the term ventral pallium has also been suggested as an alternative by Georg Striedter and David Perkel, as well as by Wayne Kuenzel).
The cortex piriformis located at the surface of HV and N (now called I and E) can retain its classic name and abbreviation (CPi). NO CHANGE
3B) THE SUBPALLIUM/ENTOPEDUNCULAR AREA (SP/AEP).
As noted above, the subpallium/entopeduncular area includes the lobus parolfactorius (LPO), the paleostriatum augmentatum (PA), the paleostriatum primitivum (PP), the majority of the septum and several basal forebrain groups that include the large cholinergic cells and the stria terminalis nuclear complex (part of it erroneously named nucleus accumbens in the past). Developmental, topological, neurochemical, connectivity and functional data strongly support that, lateral to the ventricle, the avian subpallium contains the basal ganglia homologs (Karten and Dubbeldam, 1973; Kitt and Brauth, 1981; Brauth et al., 1983; Reiner et al., 1984; 1998; Medina and Reiner, 1995; 1997; Medina et al., 1997). On the medial side of the ventricle, the subpallium contains most of the septum.
The major two subdivisions of the basal ganglia are the striatum and the pallidum. The striatum typically shows a rich innervation by dopaminergic fibers and high acetylcholinesterase activity, whereas the pallidum is poor for both. The cell types and connections of the striatal and pallidal neurons are also distinct in morphology, neuropeptide content and connections (Reiner et al., 1984; 1998; Medina and Reiner, 1995). Developmental and molecular data have indicated that the striatum and the pallidum each represent complete radial histogenetic domains of the subpallium that are present in the subpallium both on the lateral side (basal ganglia) as well as on the medial side (septum) of the ventricle (Puelles et al., 2000; Cobos et al., 2001a; Marin and Rubenstein, 2001; Redies et al., 2001). In the basal ganglia, the striatal and pallidal domains are directly comparable to mammalian derivatives of the lateral and medial ganglionic eminences (LGE, MGE), respectively. For the avian basal ganglia, I basically agree with the homology-based proposal for name changes of Reiner/Csillag.
In conclusion, I propose the following subpallial terms:
* The paleostriatum augmentatum (PA) changes to lateral striatum (STl). This is based on the relative position of PA with respect to LPO (which is also striatum). - AGREES WITH REINER/CSILLAG.
* The lobus parolfactorius (LPO) changes to medial striatum (STm). The rostromedial part of LPO includes the nucleus accumbens (Acc), defined because of its relative position within the striatum and because of its strong dopaminergic innervation by axons arising in the A10 dopaminergic cell group (see Reiner et al., 1994). However, at present a clear distinction between the Acc area and the remaining medial striatum is not possible. A specific cell group is found in the LPO of songbirds (Area X) and budgerigars (magnocellular nucleus of LPO or LPOm) (Jarvis and Mello, 2000; Farries and Perkel, 2002). The majority of the cell types found in songbird Area X resemble those of a typical striatum in physiological and possibly neurotransmitter features (Farries and Perkel, 2002). In addition, Area X also contains a cell type that resembles a typical pallidal cell in its projections to the thalamus and its physiological features (Bottjer et al., 1989; Farries and Perkel, 2002). However, both Area X and its counterpart in budgerigar (LPOm) appear to be located in the medial striatum, and we propose to call them just Area X or magnocellular nucleus of the medial striatum, respectively. The latter could be abbreviated STmc.
In developing chicken, the caudoventral part of LPO appears directly related to the Nkx2.1 expressing neuroepithelium (a pallidal marker), and is therefore included in the pallidal radial histogenetic domain (see Figs. 7f-g and 8c-d in Puelles et al., 2000; see also Redies et al., 2001; Cobos et al., 2001a). In chicken and pigeon, the caudoventral part of LPO has cells showing mixed striatal and pallidal features during development and in the adult (Sun and Reiner, 2000; see discussion in Redies et al., 2001, page 281). The mixed features of its cell population might be due to tangential immigration of neurons originated in the adjacent striatal area. In a previous version of this proposal, Luis Puelles and I suggested to call this caudoventral part of LPO the medial pallidum, abbreviated PAm. However, some avieaters have expressed concern about the use of this term in the adult, and about the uncertainty of the exact boundary between the pallidal and striatal parts of LPO in the adult. We will continue studying this area to try to resolve this question. For now, I do not propose any different term for this part of LPO until this issue is completely solved (thus, I propose to call the whole LPO as medial striatum). - AGREES WITH REINER/CSILLAG AND WITH ESTABLISHED DEFINITION OF ACCUMBENS IN MAMMALS.
* The paleostriatum primitivum (PP) changes to dorsal pallidum (PAd). This term is cell type and hodology-based (reasons explained in Reiner et al., 1984; 1998; Reiner and Carraway, 1987; Medina and Reiner, 1995; 1997; Medina et al., 1997). The only concern is that it is not clear that the avian dorsal pallidum has the same relative topological position with regard to the ventral pallidum as defined for the mammalian counterparts (Heimer et al., 1995). However, both the mammalian and avian dorsal pallidal neurons are born in the same histogenetic territory of the subpallium (expressing the homeobox gene Nkx2.1), but these neurons undergo a relatively long migration proccess in birds, to end located far away from the ventricle (Puelles et al., 2000).- AGREES WITH REINER/CSILLAG.
* The intrapeduncular nucleus (INP) - NO CHANGE.
* The nucleus accumbens (Acc) of Karten and Hodos (1967) does not correspond to the accumbens defined above as a part of the STm (in correspondence with the mammalian counterpart); this area may be named bed nucleus of the stria terminalis, lateral part (BSTl), based on the reasons summarized by Aste et al. (1998; see also Berk, 1987). AGREES WITH REINER/CSILLAG and is a homology-based term, only in the sense of being comparable to part of the mammalian BST complex.
* septal nuclei (SL, SM, etc.). As noted above, they are located in the septal part of the subpallium (same topological position of mammalian septum). The terms lateral septal nucleus and medial septal nucleus currently used in birds (Karten and Hodos, 1967) just refers to the relative position within the septum. Available hodological data (input from the hippocampal complex and output to the hypothalamus; for example Krayniak and Siegel, 1978; Atoji et al., 2002) suggest homology with comparable nuclei of the mammalian septum - NO CHANGE.
In addition, we propose:
* A population of GABAergic neurons found interstitial to the medial forebrain bundle (FPM, or, better, MFB) may be named ventral pallidum (PAv). - AGREES WITH REINER/CSILLAG and is a cell type and hodology based term (Reiner and Carraway, 1987; Veenman and Reiner, 1994; Medina and Reiner, 1997; Reiner et al., 1998). In addition, in both mammals and birds the neurons of the ventral pallidum are related to the same pallidal (Nkx2.1 expressing) histogenetic territories of their respective subpalliums (Puelles et al., 2000).
* The cell population located around the anterior commissure at the subpallio-preoptic transition corresponds to the bed nucleus of the stria terminalis, medial part (BSTm), as proposed by Aste et al. (1998; see also Berk, 1987; Jurkevich et al., 1999). This is a homology based term in the sense of being comparable to part of the mammalian BST complex.
* The population of large cholinergic neurons of the basal telencephalon partly invading the lateral and medial forebrain bundles, and the dorsal and ventral pallidal parts (Medina and Reiner, 1994), is a cell group that appears comparable to the large cholinergic cells included in the substantia innominata and the nucleus basalis of Meynert of mammals (Medina and Reiner, 1994). Therefore, we suggest calling this avian cell group the basal telencephalic magnocellular cell population (BM).
* We also suggest, as proposed in Medina and Reiner (1994), introducing the term nucleus of the diagonal band (DB) to refer to groups of large cholinergic neurons located in the area of the fasciculus diagonalis Brocae (in the septal and basal forebrain), and surrounding the septomesencephalic tract (the latter renamed here the pallio-mesencephalic tract; see below).
3C) THE AMYGDALOID COMPLEX (A).
As noted above, this is proposed to refer to the largely pallial archistriatal complex. Also as noted above, the neutral term Region A has been proposed by Striedter and Perkel to refer to this area (see above, pages 4-5). However, whatever disadvantages may accompany the concept of “amygdaloid complex”, I prefer this term because it seems most helpful for bridging the confusions when we extrapolate data from birds to mammals (see other reasons above). The different subdivisions described in the archistriatum can be easily changed as explained below, and retain their abbreviations (see Table):
* anterior archistriatum (AA) changes to anterior amygdaloid area (AA).
* intermediate archistriatum (Ai) changes to intermediate amygdaloid area (Ai). This affects the dorsal and ventral parts described in Ai, Aid and Aiv (Zeier and Karten, 1971; Wild et al., 1993; Redies et al., 2001), which changes to dorsointermediate and ventrointermediate amygdaloid areas. See Table for other examples.
* the nucleus robustus of the intermediate archistriatum of songbirds (RA, Nottebohm et al., 1976; Vicario, 1991; Wild, 1993; 1994) may change to nucleus robustus of the amygdaloid complex (RA). See Table for other examples of specific archistriatal nuclei of songbirds and budgerigar.
* medial archistriatum (Am) changes to medial amygdaloid area (Am).
* posterior archistriatum (Ap) changes to posterior amygdaloid area (Ap).
* nucleus taeniae (Tn) is included in the complex and does not need changing.
MINOR CHANGES, EASY TO REMEMBER.
4. CHANGES OF NAMES OF INTRATELENCEPHALIC BOUNDARIES.
As a consequence of the changes of pallial and subpallial names, some of the intratelencephalic boundaries need a change, specially those distinct as glial palisades or “laminae” at the border between pallial subdivisions. We propose the following:
* lamina medullaris dorsalis (LMD), at the border between striatum and epistriatal pallium, can remain the same or be simply called the pallial-subpallial boundary (psb), just like in other vertebrates. This would underline the primary telencephalic divisions. Although LMD is traditionally dear to us avi-eaters, it conveys no meaning to mammalian neuroscientists, while they know what is the pallio-subpallial boundary in mammals.
* lamina hyperstriatica (LH), at the border between the epistriatal pallium and the intermediate pallium, can be called inferior pallial lamina (ipl) or (in Latin) lamina pallialis inferior (lpi).
* lamina frontalis superior (LFS), at the border between the intermediate pallium and the Wulst, can be called superior pallial lamina (spl) or lamina pallialis superior (lps).
* lamina frontalis suprema (LFM), at the border between the lateral and intercalated subdivisions of the Wulst, can be called supreme pallial lamina (mpl) or lamina pallialis suprema (lpm).
* lamina archistriatalis dorsalis (LAD) can be called dorsal amygdaloid lamina (dal; or retain as abbreviation lad).
We note that there are advantages and disadvantages in having these names in Latin versus English versions, since the abbreviations of the English terms represent more change relative to previous abbreviations. There is also a problem with the “superior” and “supreme” laminae, since both come up with an “s” for abbreviation. The solution offered in the Karten & Hodos atlas is to abbreviate “supreme” with “m”, but we doubt this is very helpful to the naÌøve user. One possible solution would be to depart even more from tradition and call the three pallial laminae placed over the pallio-subpallial boundary respectively “inferior”, “middle” and “superior” (ipl, mpl, spl), or even “ventral”, intermediate” and “dorsal” (vpl, ipl, dpl). Other options may be possible in this line of thought.
5. CHANGES TO FIBER TRACTS.
The name of some fiber tracts are also affected by the name changes in the telencephalon, and to be consistent we propose the following changes:
* tractus archistriatalis dorsalis (DA) can be changed to dorsal amygdaloid tract (DA).
* tractus frontoarchistriaticus (FA) can be changed to frontoamygdaloid tract (FA).
* tractus thalamostriaticus (TTS) can be changed to thalamoepistriatal tract (TE) or thalamopallial tract (TP).
Other fiber tracts involve wrong connections, and can be change to the following:
* tractus septomesencephalicus (TSM) may be changed to pallio-mesencephalic tract (PM), since it mainly connects the Wulst and the midbrain tectum (Reiner and Karten, 1983; Casini et al., 1992).
* tractus occipitomesencephalicus (OM) is known to contain amygdaloid (archistriatal) projections to the hypothalamus and brainstem and reach levels beyond the mesencephalon (for example, Zeier and Karten, 1971; Wild et al., 1993; Durand et al., 1997). A possible name for the avian OM could be ventral amygdalofugal tract (VA, hodology-based term).
6. CHANGES IN SPECIFIC AREAS OF BRAINSTEM DIRECTLY RELATED TO THE TELENCEPHALON.
Some particular areas of the brainstem that are connected with the telencephalon have inherited names that produce confusion because of the implied similarity to non-homologous areas of the mammalian brainstem. One example of this is the nucleus tegmenti pedunculo-pontinus pars compacta (TPc), located in the diencephalic-midbrain tegmentum (Puelles and Medina, 1994), which is known to contain a large population of dopaminergic neurons that project to the telencephalic striatum, and to be homologous to the substantia nigra pars compacta of other vertebrates (Reiner et al., 1984;1994; 1998; Kitt and Brauth, 1986a,b; Bailhache and Balthazar, 1993; Puelles and Medina, 1994; SzÌ©kely et al., 1994; Medina and Reiner,1995; Metzger et al., 1996). The name, however, wrongly suggests a homology with the tegmental pedunculopontine nucleus of mammals, located in rhombomere 1 and characterized by the presence of numerous cholinergic neurons, but no dopaminergic neurons. On the other hand, the avian true pedunculopontine nucleus homolog containing cholinergic neurons has been described in the rhombomere 1 tegmentum of pigeons (Medina and Reiner, 1994). To avoid this confusion we propose the following changes that agree with the proposal of REINER/CSILLAG:
* nucleus tegmenti pedunculo-pontinus pars compacta (TPc) changes to substantia nigra pars compacta (SNc, A9 dopaminergic cell group).
* the laterally adjacent GABAergic cell population previously called substantia nigra pars lateralis (SNL; Veenman and Reiner, 1994; Medina and Reiner, 1997) should be identified for clarity as the substantia nigra pars reticulata (SNr).
* The cell group named area ventralis of Tsai (AVT) in the Karten and Hodos' atlas, is known to be homologous to the mammalian ventral tegmental area (VTA, A10 dopaminergic cell group; Bailhache and Balthazar, 1993; Reiner et al., 1994; Puelles and Medina, 1994) and for clarity it should be named the same as in mammals. This proposal agrees with REINER/CSILLAG.
* the cell group identified in Karten and Hodos' 1967 atlas as LoC at rostral section levels (i.e., LoC at levels 2.75, 2.50, 2.25 of the pigeon brain atlas) actually corresponds to the midbrain A8 dopaminergic cell group. This is based in data obtained during the last decade indicating that although at these levels this area certainly contains catecholaminergic neurons, these neurons are not noradrenergic, but dopaminergic, and clearly coincide in relative topography and continuity with those of the SNc, or A9 group (Bailhache and Balthazar, 1993; Reiner et al., 1994).
* the cholinergic cell group located in the rhombomere 1 tegmentum, caudal to the SNc-A9 and A8 dopaminergic groups as seen in sagittal sections (it appears underneath the caudal SNc in frontal sections), can be properly named pedunculopontine tegmental nucleus (PPN), as proposed by Medina and Reiner (1994).
In addition, to complete the list of basal ganglia-related structures expected by mammalian neuroscientists, we propose:
* the avian anterior nucleus of the ansa lenticularis (ALa), a glutamatergic cell group that originates and is located in the same topological position as the mammalian subthalamic nucleus, and is reciprocally connected with the basal ganglia, should be renamed as the avian subthalamic nucleus (STN). All this evidence is presented in Jiao et al. (2000) (also Medina and Reiner, 1995; 1997; Reiner et al., 1998).
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We use the concept of homology basically as first employed by Owen in 1843 (the same structure in different animals under every variety of form and function). This emphasizes in our view evolutionarily conserved topological and developmental "sameness", that is, relative morphogenetic stability, as opposed to similarity in adult form or function. Similarity may or may not obtain among homologues, depending on the cases. For the brain of vertebrates (assumed to share a common Bauplan), the topological (relative) position and relevant causal molecular constellations mapped within the Bauplan are important primary features suggesting homology, even though there usually is significant variation in the detailed histogenesis of derived radial domains in the mantle zone (i.e., details of cell migration, layering, connectivity, etc). The particular cell populations that originate within the homologous fields can be compared secondarily for similarity, or for more detailed levels of homology (i.e., as characteristic cell types), by analyzing other features, such as differentiation markers, neurotransmitter content, connectivity, physiological properties, etc. (see Puelles and Medina, 2002, Brain Res. Bull. 57:243-255).