organization of the dorsocaudal neostriatal complex: a retrograde and anterograde tracing study in...

Organization of the DorsocaudalNeostriatal Complex: A Retrograde and

Anterograde Tracing Study in theDomestic Chick With Special Emphasis on

Pathways Relevant to Imprinting

MARTIN METZGER,* SHUCUI JIANG, AND KATHARINA BRAUN

Department of Neuromorphology, Federal Institute for Neurobiology,39118 Magdeburg, Germany

ABSTRACTIn the forebrain of domestic chicks, a network of distinct regions is crucially involved in

auditory and visual filial imprinting. Among these areas, a distinct part of the dorsocaudalneostriatal complex (dNC complex), termed neostriatum dorsocaudale (Ndc), was recentlydiscovered by its enhanced metabolic activity during the presentation of auditory and visualimprinting stimuli. Since there is evidence that the dNC complex consists of several distinctfunctional subareas, we investigated the neural connections of different parts of the dNCcomplex by retro- and anterograde pathway tracing. Special emphasis was put on theconnections of the dNC complex with other imprinting relevant regions in the rostraltelencephalon, such as the mediorostral neostriatum/hyperstriatum ventrale (MNH) and theintermediate and medial part of the hyperstriatum ventrale (IMHV). By anterograde andmultiple retrograde pathway tracing, we found that the dNC complex may at least besubdivided into three major constituents. The most medial part of the dNC complex, termedneostriatum dorsale (Nd), is characterized by strong reciprocal connections with the neostria-tal part of the MNH and by its auditory related inputs, including those from the output layersL1 and L3 of field L, and the shell region of the thalamic n. ovoidalis. The Ndc, which occupiesthe central aspects of the dNC complex, is mainly characterized by reciprocal connections withthe ectostriatal belt (Ep) and the adjacent neostriatum (N). Furthermore, Nd and Ndc receivestrong thalamic input from the n. dorsolateralis posterior (DLP), both project to the IMHV,and both are reciprocally connected with the archistriatum intermedium (AI). The mostlateral aspect of the dNC complex, termed Ndl, is characterized by afferents from theneostriatum frontale, pars trigeminalis (NFT), and by the lack of a thalamic input. Resultsindicate that the dNC complex comprises distinct subregions, which are characterized by theirspecific afferents from parasensory areas of different sensory modalities. These differentsubregions may be integral components of a general pattern of sensory processing in the aviantelencephalon. The strong interconnections between Nd, Ndc, and MNH as well as IMHV mayconstitute essential parts of auditory and visual imprinting circuits. J. Comp. Neurol.395:380–404, 1998. r 1998 Wiley-Liss, Inc.

Indexing terms: sensory processing; parasensory cortex; auditory pathways; learning; confocal

laser scanning microscopy

Different brain areas are considered to play a pivotalrole in visual and auditory filial imprinting in domesticchicks (for reviews, see Horn, 1985, 1990, 1991; Scheich,1987; Bolhuis, 1991; Scheich et al., 1991; Bolhuis and VanKampen, 1992). Whereas the intermediate and medialpart of the hyperstriatum ventrale (IMHV) seems to beparticularly involved in visual imprinting paradigms (Horn,

Grant sponsor: Deutsche Volkswagenstiftung; Grant number: I/67 823;Grant sponsor: Land Sachsen-Anhalt; Grant number: 1797A/0084.

*Correspondence to: Dr. Martin Metzger, Department of Neuromorphol-ogy, Federal Institute for Neurobiology. POB 1860, 39008 Magdeburg,Germany. E-mail: [email protected]

Received 19 June 1997; Revised 23 January 1998; Accepted 28 January1998

THE JOURNAL OF COMPARATIVE NEUROLOGY 395:380–404 (1998)

r 1998 WILEY-LISS, INC.

1985, 1990, 1991), the mediorostral neostriatum/hyper-striatum ventrale (MNH) seems to be particularly in-volved in auditory imprinting (Maier and Scheich, 1983;Wallhausser and Scheich, 1987; Bock et al., 1996). Inaddition, recent 2-fluoro-deoxyglucose (2-FDG) experi-ments revealed a circumscribed subarea in the dorsocau-dal neostriatum, which in acoustically and visually im-printed chicks displays an increased metabolic activityevoked by the presentation of the acoustic or visualimprinting stimulus, respectively (Bock et al., 1997). Thissubarea was termed by us neostriatum dorsocaudale (Ndc;Scheich et al., 1991; Metzger et al., 1996; Bock et al., 1997)and we will refer to the dorsocaudal neostriatum as awhole, as dorsocaudal neostriatal complex (dNC complex).

Information on the connectivity of the dNC complex isstill rather limited. Some major telencephalic and subtel-encephalic inputs of the dNC complex, such as the tha-lamic input from the n. dorsolateralis (DLP) and themesencephalic input from the area ventralis (AVT) andsubstantia nigra (SN), have been described in chicks(Metzger et al., 1996) and pigeons (Waldmann and Gun-turkun, 1993; Leutgeb et al., 1996). In addition, scatteredtracing data from several avian species have indicatedthat parts of the dNC complex are reached by afferents ofdifferent sensory modalities, including auditory (Bonke etal., 1979a; Wild et al., 1993; Metzger et al., 1996), visual(Shimizu et al., 1995; Leutgeb et al., 1996), somatosensory(Wild, 1987b; Funke 1989b; Leutgeb et al., 1996), andtrigeminal inputs (Wild et al., 1985; Wild and Farabaugh,1996). These tracing data led us to the hypothesis that thedNC complex, which appears cytoarchitectonically homoge-neous (Rehkamper et al., 1985), might comprise severalfunctionally distinct subunits. Thus, our first aim was toanalyze the connectivity of the putative dNC subregions bymultiple retro- and anterograde pathway tracing in moredetail.

The second aim of our study was to provide a detailedanalysis of the interconnections of the dNC complex withthe MNH and IMHV. There is only rather limited informa-tion on the circuits that underlie the perceptual compo-nents of auditory (Bonke et al., 1979a; Wallhausser-

Franke, 1989; Metzger et al., 1996) and visual imprinting(Bradley et al., 1985; Csillag et al., 1994). The IMHV andin particular the MNH are fairly remote from peripheralsensory input, which raises the critical question, by whichpathways sensory information is conveyed to these areas(for discussion, see Horn, 1985; Scheich et al., 1991). Thereis evidence that parts of the dNC complex project to MNHand IMHV (Bonke et al., 1979a; Bradley et al., 1985;Metzger et al., 1996) and also to the archistriatum interme-dium (AI; Wild et al., 1985, 1993), which is considered asthe somatosensorimotor component of the archistriatum(Zeier and Karten, 1971). These connections together withthe findings of the present study raise the possibility thatthe dNC complex might be an important relay stationproviding sensory input to the MNH and IMHV. In addi-tion, the connections with the AI point to a possible role ofthe dNC complex as a sensori-motor interface (see Wild etal., 1985, 1993; Rehkamper and Zilles, 1991), which maybe involved in the development of the (motor)-behavioralresponses towards a learned stimulus or object duringfilial imprinting.

To clarify such a possible relay function of the dNCcomplex, special emphasis was put on intratelencephalicconnections of the dNC complex with 1) sensory struc-tures, 2) imprinting relevant forebrain regions, includingthe MNH and IMHV, and 3) the AI. Thus, injections ofretro- and antero-grade tracers into the dNC complex werecomplemented by injections of retrograde tracers into theAI and IMHV and anterograde tracers into the MNH.Efferent connections of the IMHV (Bradley et al., 1985;Csillag et al., 1994) and afferent connections of the MNH(Wallhausser-Franke, 1989; Metzger et al., 1996) havebeen described previously.

The third aim of this study was to provide a detailedinterpretation of our results in relation to mammalianbrain circuits. The dNC complex is by some authorsconsidered to be the avian equivalent of the mammalianprefrontal cortex (PFC; Divac and Mogensen, 1985; Divacet al., 1985; Reiner 1986; Waldmann and Gunturkun,1993; Wynne and Gunturkun, 1995). This view is based onresults from behavioral lesion experiments, which have

Abbreviations

AA archistriatum anteriorAId archistriatum intermedium, pars dorsalAIv archistriatum intermedium, pars ventralAp archistriatum posteriorAPH area parahippocampalisAVT area ventralis (Tsai)Bas nucleus basalisCDL area corticoidea dorsolateralisDLA nucleus dorsolateralis anterior thalamiDLP nucleus dorsolateralis posterior thalamiDMA nucleus dorsomedialis anterior thalamiDMP nucleus dorsomedialis posterior thalamiE ectostriatumEp periectostriatal beltFA tractus fronto-archistriaticusFL field LHA hyperstriatum accessoriumHD hyperstriatum dorsaleHIS hyperstriatum intercalatumHp hippocampusHV hyperstriatum ventraleIMHV intermediate and medial part of the hyperstriatum ventraleL1 field L1L2 field L2L3 field L3

LAD lamina archistriatalis dorsalisLMD lamina medullaris dorsalisLPO lobus parolfactoriusLHy lateral hypothalamic areaMNH mediorostral neostriatum/hyperstriatum ventraleN neostriatumNC neostriatum caudaleNd neostriatum dorsalNdc neostriatum dorsocaudaleNdl neostriatum dorsolateraleNFT neostriatum frontal, pars trigeminalisNI neostriatum intermediumNI/NC transition zone of the medial neostriatum intermedium and

caudaleOV nucleus ovoidalisPA paleostriatum augmentatumPP paleostriatum primitivumROT nucleus rotundusSM nucleus septalis medialisSN substantia nigraSPO nucleus semilunaris paraovoidalisSRt nucleus subrotundusTn nucleus taeniaeTPO area temporo-parieto-occipitalisVL ventriculus lateralis

ORGANIZATION OF THE AVIAN NEOSTRIATUM CAUDALE 381

indicated a selective involvement of the dNC complex inthe performance of delayed alternation tasks (Mogensenand Divac, 1982, 1993) and spatial cognitive tasks, such ashoming in pigeons (Gagliardo and Divac, 1993; see alsoBingman et al., 1995), as well as on the immunocytochemi-cally demonstrated, rich dopaminergic innervation of thedNC complex (Waldmann and Gunturkun, 1993; Moons etal., 1994; Wynne and Gunturkun, 1995; Metzger et al.,1996). However, this view appears to be premature underhodological aspects (for discussion, see Metzger et al.,1996; Veenman et al., 1997). Thus, the connectivity pat-terns of the dNC complex were compared with mammalianbrain circuits.

MATERIALS AND METHODS

Similar to our previous tracing study (Metzger et al.,1996), this report is based on 4-day-old domestic chicks(White Leghorn; n 5 43, see Table 1) of either sex.Fertilized eggs were obtained from a local supplier (Horst-mann, Nienburg, Germany) and incubated in our labora-tory at 37.560.3°C. Chicks were socially reared in smallgroups at a light/dark cycle of 12/12 hours at 3062°C.Commercial food and water were available ad lib. Allexperimental protocols were conducted within NIH guide-lines for animal research and were approved by a reviewcommittee of the State of Saxony-Anhalt, Germany.

Anterograde tracing experiments

Biocytin injections. Ten 4-day-old chicks were usedin this part of the study. For the application of tracers,birds were deeply anaesthetized with an intramuscularinjection of Equithesin (0.01 ml/g b. wt.) and placed in astereotaxic apparatus. The skin over the skull was incisedand small openings in the skull at the level of the MNH ordNC complex were drilled with a dental burr. Multipleunilateral injections of biocytin (Sigma, Deisenhofen, Ger-many, 5% in Tris-HCL buffer 0.05 M, pH 7.6) were placedeither into the MNH (n54) or into different parts of thedNC complex (n56). In all cases, an equal amount of 1.2 µlbiocytin was injected in 100 nl steps at four adjacent sites

with a Nanoliter injector system (World Precision Instru-ments, Sarasota, FL). The pipette tip (OD 15–30 µm) wasleft in position for about 10 minutes before each with-drawal to reduce leakage of the tracer along the pipettetract. After a survival period of 22–26 hours, birds wereinjected with an overdose of a 20% Hypnodil (Janssen,Neuss, Germany) solution in 0.1 M phosphate-bufferedsaline (PBS, pH 7.4) and perfused via the left ventriclewith 50 ml of Tyrode’s solution (pH 7.0) containing 1%Liquemin (Roche, Grenzach-Whylen, Germany) followedby 500 ml fixative containing 4% paraformaldehyde and0.75% glutaraldehyde in PBS (pH 7.3). The brains wereremoved from the skull, postfixed overnight in 2% parafor-maldehyde, sectioned in the coronal plane on a Vibratome(section thickness 5 40 µm), and collected in PBS. Sectionswere preincubated in 1% sodium borohydride in PBS for 10minutes at room temperature to reduce background stain-ing. Sections were washed 33 in PBS and then the biocytinwas localized according to the protocol of Smith (1992). Inbrief, sections were incubated overnight at 4°C in anExtravidin peroxidase complex (Sigma, Deisenhofen, Ger-many) diluted 1/200 in PBS containing 0.3% Triton X-100.The bound complex was visualized by incubation for 10–12minutes in a solution of 0.025% diaminobenzidine (DAB)and 0.006% H2O2 in Tris-HCL buffer (0.05 M, pH 7.6).

Electron microscopy

Sections processed for electron microscopy were treatedas described above, except that Triton X-100 was omittedduring the incubation with the Extravidin peroxidasecomplex (Sigma). Following the visualization of biocytin,sections were rinsed in 0.1 M phosphate buffer (PB, pH7.4), postfixed by immersion in phosphate-buffered 1%osmium tetroxide, dehydrated in a graded series of alco-hols and propylene oxide, stained with 2% uranyl acetatein 90% alcohol, and flat-embedded in Spurr’s resin (TedPella, Inc., Redding, CA) between two overhead transpar-encies. Selected areas from the dNC and MNH wereexcised with a fine scalpel and glued onto precured Eponblocks. Series of ultrathin sections were cut on an ultrami-crotome (MT 7; RMC, Inc., Tucson, AZ) and examined in aZeiss (CEM 902A) electron microscope. Electron micro-graphs were made with a MultiScan CCD camera (Gatan,Inc., Pleasanton, CA) and printed on a Pictrography 3000printer (Fuji, Tokyo, Japan).

Retrograde tracing experiments

This part of the study was based on 33 4-day-old chicks.The procedure for anaesthesia and delivery of tracers wasthe same as described above in the anterograde tracingprotocol. Chicks received either single, unilateral injec-tions (n 5 11) of Fluoro-Gold (FG; Fluorochrome, Inc.,Englewood, CO, 2% aqueous solution) Diamidino Yellow(DY; Illing, Grob-Umstadt, Germany, 2% aqueous solu-tion), or Fast Blue (FB; Illing, Grob-Umstadt, Germany,2% aqueous solution), or multiple, unilateral injections(n 5 16) at different levels along the medial to lateral axisof the dNC-complex (Fig. 1). In the case of multipleinjections, chicks received either three injections (n 5 8),by using combinations of the fluorescent tracers FG/FB/DYtogether in one animal, or two injections (n 5 8), by usingthe tracer combinations green and red latex FluoSpheres(gFS/rFS; 10% solids, Molecular Probes, Eugene, OR) orFG/FB. In six cases, unilateral injections were placed intothe archistriatum intermedium (AI) and IMHV by using

TABLE 1. Experimental Parameters1

Numberof animals Injection site

Tracer

Left side Right side

2 MNH BC2 MNH BC2 Nd BC2 Nd BC2 Ndc BC2 Nd FB1 Nd FG3 Ndc FB2 Ndl DY1 Ndl FB2 Ndl FG2 Nd/Ndc FG/FB2 Nd/Ndc FG/FB2 Nd/Ndc gFS/rFS2 Nd/Ndc rFS/gFS2 AI/IMHV gFS/rFS1 AI/IMHV gFS/rFS2 AI/IMHV DY/FB1 AI/IMHV FB/DY2 Nd/Ndc/Ndl FB/FG/DY2 Nd/Ndc/Ndl FG/FB/DY2 Nd/Ndc/Ndl DY/FB/FG2 Nd/Ndc/Ndl FB/FG/DY

1BC, Biocytin; DY, Diamidino Yellow; FB, Fast Blue; FG, Fluoro-Gold; gFS, green latexFluoSpheres; rFS, red latex FluoSpheres; for other abbreviations, see list.

382 M. METZGER ET AL.

the tracer combinations gFS/rFS or DY/FB. In the case ofinjections into IMHV, tracer-filled pipettes were advancedat an angle of 5° from the vertical towards the midline. Forall tracers amounts of 0.05 µl (multiple injections) or 0.2 µl(single injections) were injected in four steps of 12.5 or 50nl, respectively. After survival for 5–7 days, birds wereperfused as described above, except that glutaraldehydewas omitted. Brains were stored in 30% sucrose in PBSuntil equilibration and coronal sections (40 µm) were madewith a Cryostate (Microm, Walldorf, Germany). Sectionswere mounted on gelatine-coated slides, air dried, andcoverslipped with Fluoromount (Serva, Heidelberg, Ger-many). Every third section through the injection sites andother selected areas were stained with cresyl violet for theevaluation of the spatial extent of the injection areas andboundaries of labeled structures.

Charting and histological analysis

Selected latex FluoSpheres labeled sections were ana-lysed by using a confocal laser scanning microscope (CLSM;Leica TCS4D, Leica, Bensheim, Germany). Sections werescanned at different magnifications in either a 512 I 512 ora 1,024 I 1,024 pixel format as reported in detail previ-

ously (Metzger et al., 1996). Some sections were scannedwith the 3D-Multi-Image-Stack-Acquisition-Software (3D-MISA; Zuschratter et al., 1996). This software allowsimage acquisition of large coherent regions in combinationwith high resolution of the single images. Image process-ing was carried out with the Adobe Photoshop program(Version 3.0; Adobe Systems, Inc., Mountain View, CA).Finally, color prints of CLSM-images were printed on aPictrography 3000 printer (Fuji, Tokyo, Japan). Otherphotomicrographs were taken on a Olympus Vanox micro-scope. All transverse sections that are displayed in photo-micrographs are illustrated with medial to the right forease of comparisons. Reconstruction drawings of the sec-tions were made from enlarged photomicrographs or byusing a microscope specimen projector apparatus.

RESULTS

Nomenclature

Unless otherwise stated, the nomenclature used through-out this report is adopted from the comprehensive atlas ofthe 2-week-old chicken brain (Kuenzel and Masson, 1988).With regard to the avian dNC complex, the terms pos-terodorsolateral neostriatum (PDLNS; Divac and Mo-gensen, 1985) and neostriatum caudolaterale (Ncl; Wald-mann and Gunturkun, 1993) have been adopted in thepigeon for a crescent-shaped area, which is delineated by avery dense dopaminergic innervation. In domestic chicks,the neostriatum caudale (NC) seems to be more homoge-neously innervated by dopaminergic fibers and no sucharea can be distinguished (Moons et al., 1994; Metzger etal., 1996). Thus, we refer to the most medial aspects of thedNC complex as neostriatum dorsale (Nd; according toBonke et al., 1979a; Wild et al., 1993) and to the centralaspects as Ndc (according to Metzger et al., 1996; Bock etal., 1997). In addition, we termed the most lateral aspectsof this complex neostriatum dorsolaterale (Ndl, see Fig. 1).We refer to the mediorostral neostriatum (N) and a narrowstripe of the overlying hyperstriatum ventrale (HV) asMNH and to the intermediate and medial part of the HV asIMHV. The borders of Ndc (see Fig. 3), MNH (see Fig. 4),and IMHV cannot directly be determined in Nissl-stainedsections. However, the borders of Ndc (see Bock et al.,1997), MNH (see Maier and Scheich, 1983; Wallhausserand Scheich, 1987), and IMHV (see Horn et al., 1979) canbe functionally unambiguously defined by their highlyreproducible stimulus evoked activation in acousticallyand/or visually imprinted chicks. Nissl-stained sectionscan then be superimposed over 2-Fluoro-deoxyglucose oruracil autoradiographs.

Anterograde tracing experiments

General results. Biocytin injections into the dNC com-plex were targeted to the medial (area Nd, Fig. 2) orcentral (area Ndc, Fig. 3) aspects of the dNC complex.Cases with spread of tracer into the caudal HV or into fieldL, which both can be identified in Nissl-stained sections(see Heil and Scheich, 1985; Wild et al., 1993), were notfurther analyzed. Injections of biocytin into the MNH (seeFigs. 4, 6A,B) generally involved the mediorostral neostria-tum (N) and parts of the overlying hyperstriatum ventrale(HV). Cases with obvious spread of tracer into the dorsallyadjacent Wulst or ventrally adjacent LPO were excludedfrom examination. The injection sites in the MNH anddNC complex were characterized by a central core of

Fig. 1. Schematic drawing of coronal sections of the dorsocaudalneostriatal complex (dNc complex) at four consecutive levels of rostro-caudal sequence. The black areas indicate the approximate extent anddistribution of multiple injections of retrograde tracers into theneostriatum dorsolaterale (Ndl), the neostriatum dorsocaudale (Ndc),and neostriatum dorsale (Nd) in one case coded dNC 8. The correspond-ing distribution of retrogradely labeled neurons in this case is shownin Figure 10. The striped areas indicate the approximate distributionand extent of injections in four other cases, which also received threeinjections of different retrograde tracers into the dNC complex,respectively. Note that the black and striped areas do not only indicatethe central core of injections but also the area in which tracer uptakemay have occurred. For abbreviations, see list.


retrogradely labeled neurons. Individual retrogradely la-beled neurons were also found at some distance (200–400 µm)from the injection site. Unless otherwise mentioned, thelabeling at greater distance from the injection sites wasexclusively anterograde. Anterograde labeling was strictlyconfined to the ipsilateral telencephalon.

Injections of biocytin into the Nd or Ndc revealed 1) atopographically ordered output of these regions to rostralaspects of the N, and 2) a system of projections that werealmost common to Nd and Ndc, including projections to thebasal ganglia, HV, IMHV, and AI.

Injections into dNC. Four out of six injections into thedNC complex were confined to area Nd, whereas twoinjections were placed more laterally into Ndc. Injectionscentered in Nd consistently resulted in a dense plexus offibers in the mediorostral neostriatum (N, Fig. 5A) includ-ing the neostriatal part of the MNH. Within the N, thedensity of labeled fibers slightly increased from rostral tocaudal with highest densities in the neostriatum interme-dium (NI, Fig. 5B). Very few scattered anterogradelylabeled fibers became obvious in the hyperstriatum acces-sorium (HA). Occasionally, few labeled fibers were found in

the hyperstriatum intercalatum supremum (HIS) andhyperstriatum dorsale (HD). In addition, labeled fiberswere consistently found in the HV and IMHV. Moderateanterograde labeling was detected in parts of the basalganglia complex. Labeled fibers became typically conspicu-ous in caudomedial parts of the lobus parolfactorius (LPO)and in the paleostriatum augmentatum (PA). In the caudaltelencephalon, few labeled fibers were observed to leavethe Nd laterally towards the Ndc. Numerous labeled fiberscoursed from the injection site in the Nd ventrolaterallytowards the AI. Within the AI, the majority of labeledfibers terminated in ventromedial aspects of the archistria-tum intermedium, pars ventralis (AIv, Fig. 5C). In addi-tion, some scattered labeled fibers could be observed in thearchistriatum intermedium, pars dorsalis (AId).

The two injections into Ndc resulted in only few labeledfibers in the MNH. Instead, numerous labeled fibers weredetected in more lateral aspects of the N (Fig. 5E) and NI.Additionally labeled fibers were found in the ectostriatalbelt (Ep, Fig. 5D), but were not seen in the core of theectostriatum (E). Sparse labeling could be detected in theWulst, where labeled fibers were mainly confined to HA.

Fig. 2. A-C: Schematic drawings from selected levels of coronalsections through the chick forebrain depicting the labeling after aninjection of biocytin into the neostriatum dorsale (Nd; indicated byblack area in C), in one case coded biocytin VIII. Fine lines representbiocytin labeled fibers and terminals. The hatched area in C indicatesthe approximate extent of area Nd as revealed by retro- and antero-grade tracing studies (see Bonke et al., 1979a; Wild et al., 1993;Metzger et al., 1996). For abbreviations, see list.

Fig. 3. A-C: Schematic drawings from selected levels of coronalsections through the chick forebrain depicting the labeling after aninjection of biocytin into the neostriatum dorsocaudale (Ndc; indicatedby black area in C),in one case coded biocytin VII. Fine lines representbiocytin labeled fibers and terminals. The hatched area in C indicatesthe extent of area Ndc as seen by 2-fluoro-deoxyglucose uptake studies(see Bock et al., 1997). For abbreviations, see list.


More caudally, scattered labeled fibers were found in theHV and IMHV (Fig. 5F). In the basal ganglia, the patternof anterograde labeling was similar to that described forinjections into Nd. In the caudal telencephalon, a broadfiber bundle coursed from the injection site in the Ndcventrally towards the AI. Whereas, the pattern of antero-grade labeling in the AId was similar to that described forinjections into Nd, the labeling in the AIv was mainlyfound in the dorsolateral parts of this structure.

Injections into MNH. After injections centered intothe MNH, anterograde intratelencephalic labeling waspresent in rostral parts of the visual Wulst including theHA, HIS, and HD. Some fibers were observed to leave theMNH ventrally towards medial portions of the LPO. Themajority of labeled fibers, however, were observed to leavethe MNH region as broad fiber bundles, which coursedthrough the N, HV and IMHV (Fig. 6C) towards medialaspects of the dNC complex. Most of these fibers termi-nated in a dense ‘‘V’’-shaped plexus ventral to the ventricu-lus lateralis in the mediodorsal aspects of the dNC com-plex (Fig. 6D). This area has been termed neostriatumdorsal (Nd) by Bonke et al. (1979a). The remainder offibers entering the dNC complex traveled from Nd either

strictly laterally through the subventricular zone towardsthe Ndc (Fig. 6E), or ventrolaterally towards the AI. In theAI, there was a distinct termination field in the AId (Fig.6F). Additionally, few labeled fibers were observed in thearea corticoidea dorsolateralis (CDL).

Electron microscopy

In order to clarify, whether biocytin-labeled axonalprocesses in the Nd and Ndc arising from the MNH and,vice versa, axon terminals in the MNH arising from the Ndand Ndc form functional synaptic contacts in their targetregions, these were also examined at the ultrastructurallevel. In general, the electron-dense DAB reaction productwas floccular and associated with the internal surface ofplasma membranes of myelinated and unmyelinated axons.In all examined areas, most biocytin-labeled axon termi-nals were apposed to pronounced postsynaptic thicken-ings, and synaptic specializations were therefore classifiedas asymmetrical synapses (Fig. 7A,B). Few labeled termi-nals formed symmetric synapses. In the Nd and Ndc, mostlabeled terminals formed synaptic contacts with dendriticspines (axospinous synapses, Fig. 7A,B) and containedround vesicles. Less frequently, we observed asymmetricor symmetric (Fig. 7C,D) synapses on dendritic shafts(axodendritic synapses) and least frequently we founddistinct synaptic specializations between biocytin-labeledaxons and cell somata (axosomatic synapses). Most ofthese axodendritic and axosomatic synapses were symmet-ric (Fig. 7C,D) and the biocytin-labeled axon terminalsoften contained pleomorphic vesicles. Some very largelongitudinally sectioned labeled axons and varicosities inthe Nd and Ndc gave no indication of synaptic contacts.

In the MNH, the pattern of labeled axons and axonterminals was generally similar to that in Nd and Ndcwith regard to synaptic specializations. However, lessasymmetric axospinous synapses and more longitudinallysectioned axons and varicosities without synaptic special-izations became obvious than in Nd and Ndc.

Retrograde tracing experiments

General results. Although the histological appear-ance of fluorescent tracer injection sites differed slightlyfor the different retrograde tracers that were used (seeMetzger et al., 1996), there were no obvious differences inthe general pattern of retrograde labeling obtained withthe five different retrograde tracers.Accordingly, the follow-ing description applies to all birds, regardless of theapplied tracer. Unless otherwise mentioned, retrogradelabeling was confined to the ipsilateral side of the brain.

Injections of retrograde tracers into the different parts ofthe dNC complex revealed 1) a topographically orderedsystem of projections from the belt regions of primarysensory areas and some other forebrain regions to thedifferent components of the dNC complex; and 2) a systemof projections that were almost common to all componentsof the dNC complex, including projections from the AI,thalamic projections from the n. dorsolateralis posterior(DLP) and mesencephalic projections from the substantianigra (SN) and area ventralis (AVT).

Single retrograde tracing experiments

Nd injections. Injections into Nd resulted in a distinctpattern of retrograde labeling in the avian auditory cortexanalogue field L (Bonke et al., 1979b). Whereas the inputlayer (L2) was almost devoid of labeled cells, the adjacent

Fig. 4. A-C: Schematic drawings from selected levels of coronalsections through the chick forebrain depicting the labeling after aninjection of biocytin into the mediorostral neostriatum/hyperstrriatumventrale (MNH; indicated by black area in A), in one case codedbiocytin X. Fine lines represent biocytin labeled fibers and terminals.The hatched area in A indicates the extent of the MNH as seen by2-fluoro-deoxyglucose uptake studies (see Maier and Scheich, 1983;Wallhausser and Scheich, 1987). For abbreviations, see list.


Fig. 5. A–C: Darkfield photomicrographs of anterogradely labeledfibers in the rostromedial neostriatum (N, A), neostriatum interme-dium (NI, B), and archistriatum intermedium, pars ventrale (AIv, C)after an injection of biocytin into the Nd. Note the paucity of labelingin the nucleus taeniae (Tn) in C. D–F: Darkfield photomicrographs ofanterogradely labeled fibers in the periectostriatal belt (Ep, D),

neostriatum (N) and paleostriatum augmentatum (PA, E), and inter-mediate and medial part of the hyperstriatum ventrale (IMHV, F)after an injection of biocytin into the neostriatum dorsocaudale (Ndc).Note the absence of labeling in the ectostriatal core (E) in D and E. VL,ventriculus lateralis. Scale bars 5 100 µm in A,B,F, 150 µm in C,D,E.


Fig. 6. Photomicrograph (A) and schematic representation (B)showing a biocytin injection centered on the neostriatal part (N) of themediorostral neostriatum/hyperstriatum ventrale (MNH). Darkfieldphotomicrographs (C-F) of anterogradely labeled fibers resulting fromthe injection depicted in A. C: Fascicles of labeled fibers passing

through the intermediate and medial part of the hyperstriatumventrale (IMHV). D–F: Termination fields in the neostriatum dorsale(Nd; D), neostriatum dorsocaudale (Ndc; E), and archistriatum inter-medium, pars dorsale (AId, F). For abbreviations, see list. Scale bars 5100 µm.


layers L3 and in particular L1 were heavily labeled (Fig.8A). Very strong labeling was also consistently present inthe rostromedial neostriatum (N), including the neostria-tal part of the MNH. Within the N, a pronounced rostral tocaudal gradient became obvious with highest densities ofretrogradely labeled neurons found in caudal aspects ofthe neostriatal part of the MNH. Retrograde labeling wasalso present in the transition zone of the medial neostria-tum intermedium and caudalis (NI/NC) dorsal to thelamina medullaris dorsalis (LMD, Fig. 8B,C). Further-more, Nd injections resulted in weak retrograde labelingin the Wulst. Labeled neurons in the Wulst were mainlyfound evenly distributed in the rostral hyperstriatumaccessorium (HA, Fig. 8D). Less frequently, we observedretrogradely labeled neurons along the border of thehyperstriatum dorsale (HD) and hyperstriatum ventrale(HV). A cluster of labeled neurons became typically con-spicuous in the hyperstriatum laterale (HL) near thevallecula telencephali (Va).

In the AI, we detected in two of three cases a distinctcluster of labeled neurons bilaterally in the ventromedialpart of the AIv, whereas a small FB injection placed at the

ventral border of the Nd only produced very few scatteredretrogradely labeled cells in the ipsi- and contra-lateralAIv. In the thalamus, retrogradely labeled neurons oc-curred frequently in rostral parts of the DLP and in theshell region of the n. ovoidalis (Ov, Fig. 8E,F). According toDurand et al. (1992), this shell region consists of the n.semilunaris paraovoidalis (SPO) and a thin layer of neu-rons which surround the core of the Ov. In addition, veryfew labeled neurons could be observed in n. subrotundus(SRt). In the mesencephalon, retrograde labeling wasprimarily found in the ventral part of the AVT. A fewlabeled neurons were seen in the central and dorsolateralparts of the SN, the substantia grisea centralis (GCt) andmore caudally in the locus coeruleus (LoC) and the n.subcoeruleus (SCv). Very few labeled neurons were pre-sent in homotopic areas of the contralateral mesencepha-lon.

Ndc injections. Injections into the Ndc resulted instrong retrograde labeling in the belt regions of the E,where two distinct populations of labeled neurons could bedistinguished. One cell group was situated dorsal to the Ein the periectostriatal belt (Ep, Fig. 9A,B) and the other

Fig. 7. Electron micrographs illustrating biocytin-labeled axonterminals in the mediorostral neostriatum/hyperstriatum ventrale(MNH) resulting from a biocytin injection into neostriatum dorsale(Nd; A,C) and biocytin-labeled axon terminals in the Nd resulting froma biocytin injection into MNH (B,D). A: Biocytin-labeled axon terminal(At) in the MNH forming an asymmetric synaptic contact (arrow) witha spine (Sp). B: Biocytin-labeled axon terminal (At) and axons (a) in

the Nd. The labeled axon terminal is forming an asymmetric synapticcontact (arrow) with a spine (Sp). Den, dendritic shaft. C: Longitudi-nally sectioned biocytin-labeled varicosity (Var) in the MNH forming asymmetric synaptic contact (arrowheads) with a dendritic shaft (Den).D: Biocytin-labeled axon terminal (At) in the Nd forming a symmetricsynaptic contact (arrowheads) with a dendritic shaft (Den). Scalebars 5 0.4 µm.


Fig. 8. Photomicrographs showing retrograde labeling after injec-tions of different retrograde tracers into neostriatum dorsale (Nd).A: Fast Blue (FB)-labeled neurons in layer 1 and 3 (L1, L3) of field L.Note that retrograde labeling is almost absent in layer 2 (L2) andcompletely absent in the hyperstriatum ventrale (HV). B: DiamidinoYellow (DY)-labeled neurons in the transition zone of the of the medialneostriatum intermedium and neostriatum caudale (NI/NC) and layer3 (L3) of field L. Arrowheads point to the lamina medullaris dorsalis(LMD). PA, paleostriatum augmentatum. C: Schematic representa-

tion of the labeled area in A (indicated by box). D: FB-labeled neuronsin the hyperstriatum accessorium (HA). E: FG-labeled cluster ofneurons (indicated by arrowheads) in the shell region of the n.ovoidalis (OV). Note that retrograde labeling in the n. semilunarisparaovoidalis (SPO) and n. subrotundus (SRt) is mostly due to an FBinjection into the Ndc of the same hemisphere. F: Nissl-stainedtransverse section adjacent to the section shown in E. For abbrevia-tions, see list. Scale bars 5 100 µm.

cell group was located immediately medial to the E inadjacent parts of the neostriatum (Fig. 9C). In contrast,the central core of the ectostriatum (E) was always devoidof retrograde labeling. Only few scattered labeled neuronsbecame obvious in the MNH. In the caudal telencephalon,labeled neurons were present in a neostriatal area overly-ing the laminae archistriatalis dorsalis (LAD) and LMD.Moderate retrograde labeling became obvious in mostsubdivisions of the Wulst, including rostral parts of theHA, HD, and HL. The HIS and the intercalated nucleus ofthe hyperstriatum accessorium (IHA, according to Shimizuet al., 1995) were not labeled. Retrogradely labeled neu-rons were also consistently found in the rostral HV.

In the AI, retrogradely labeled neurons were found intwo of three cases bilaterally in clusters in the AIv. Inanother case, we only detected ipsilateral labeling in theAIv. Thalamic and mesencephalic inputs to the Ndc havebeen previously described in detail (Metzger et al., 1996).

Ndl injections. Injections into Ndl typically involvedthe most lateral aspects of the dNC complex. In one casethere was spread of tracer into the cortex piriformis (CPi).Ndl injections resulted in a large number of retrogradelylabeled neurons in a rostroventral part of the N at theborder of the n. basalis (Bas, Fig. 9D). This area has beentermed neostriatum frontale, pars trigeminalis (NFT) byWild et al. (1985). Aside from the NFT, retrograde labelingin the telencephalon was mostly confined to weak labelingin rostral parts of the Hd and a distinct cluster of labeledneurons at the lateral rim of the N (Fig. 9E,F). This clusterwas situated dorsal to the tractus fronto-archistriaticus(FA) and extended in rostrocaudal direction in size up tothe level where the archistriatum anterior (AA) appears incresyl violet stained sections. In addition, few retrogradelylabeled neurons were found in the area tempero-parieto-occipitalis (TPO) and in an area dorsal to the laminaarchistriatalis dorsalis (LAD).

In three of five cases, a cluster of labeled neurons wasobserved bilaterally in the most ventrolateral aspects ofthe AIv. Two injections, which were confined to the mostcaudal aspects of Ndl, only produced some scatteredlabeled neurons in the ipsi- and contra-lateral AIv. Exceptof very few labeled neurons in the lateral hypothalamicarea (LHy), no retrograde labeling could be detected in thethalamus. In the mesencephalon, Ndl injections resultedin a similar pattern as described above for injections intoNd. Retrogradely labeled neurons were found in AVT, SN,GCt, LoC, and SCv.

Multiple retrograde tracing experiments

Multiple injections into the dNC complex. Multipleinjections of different retrograde tracers into the dNCcomplex generally confirmed the results of single injec-tions. Additionally, these multiple injections were a valu-able tool to reveal and specify distinct topographic pat-terns for some projection systems. Although injection sitesin the dNC were generally very restricted, due to the factthat in the case of multiple injections a smaller amount oftracers was delivered than in cases with single injections,in some cases there was a weak overlap of the nearbyinjection sites in the dNC complex. The following descrip-tion for multiple injections therefore mainly refers to thosecases in which no obvious overlap of the injection sites wasobserved (n 5 5 in cases with three injections, and n 5 5 incases with two injections).

A pronounced mediolateral topography became obviousfor the projections from rostral parts of the N to the dNCcomplex. In general, the most medial injections into thedNC complex resulted in retrograde labeling in medialparts of the N. In this way, injections, which were strictlyconfined to Nd, the medial part of the dNC complex,preferentially labeled neurons in the most medial parts ofthe N, including the neostriatal part of the MNH. Injec-tions into Ndc, the central part of the dNC complex,predominantly marked neurons in the Ep and adjacentparts of the N, whereas labeling in the MNH was onlyweak or absent (Figs. 10A, 11A). Following injections intoNdl, the most lateral part of the dNC complex, labelingwas confined to lateral aspects of the N, including the NFT,the TPO and a distinct area, which was situated dorsal tothe FA. Depending on the overlap of the injection sites inNd and Ndc, there was a small transition zone in therostrocentral N in which retrogradely labeled neurons,either labeled by injections into Nd or Ndc, were foundadjacent to each other.

A pronounced mediolateral topography also becameobvious for afferents, arising from a ventrocaudal zone ofthe N, which expands from medial to lateral along theLMD and LAD. Whereas injections into Nd mainly lead tolabeling in the most medial aspects of this zone, includingthe NI/NC transition zone, injections into Ndc predomi-nantly labeled the central, and injections into Ndl the mostlateral parts of this zone (Fig. 10D).

In the AIv, we detected in eight of the ten cases with noobvious overlap of the injection sites distinct clusters ofretrogradely labeled neurons. Labeled neurons in theseclusters projected either to Ndl, Ndc, or Nd (Fig. 12A).However, the size and in particular the rostral-caudalextent of these clusters varied considerably among indi-vidual cases. These clusters were typically also found inhomotopic areas of the contralateral AIv. As judged by theeye, the number of labeled neurons in the ipsilateral AIvonly slightly surpassed that in the contralateral AIv.

In the thalamus, neurons which were double-labeled byinjections into Nd and Ndc were numerous in rostral partsof the DLP (Fig. 11B). As estimated by counting cells inselected sections, up to 36% of labeled neurons in the DLPwere double-labeled by these injections. Those double-labeled neurons were found all over rostral DLP and noobvious topography of DLP projections was detectable. Adistinct topographical organization of thalamic afferentsto the dNC became obvious in the shell region of the n.ovoidalis (Ov). Whereas injections into Ndc first of allresulted in labeled neurons in the ventromedial portions ofthe Ov shell including the SPO and, in addition, in theventrally adjacent SRt, injections into Nd predominantlylabeled neurons in the dorsal and lateral portions of the Ovshell (Fig. 11C).

In the mesencephalic nuclei AVT and SN (Fig. 12B),neurons projecting to Nd, Ndc, and Ndl were commonlyonly single-labeled and often found adjacent to each other.Double-labeled neurons could only rarely be observed. Inthe SCv, double-labeled neurons were a little more com-mon and even a few triple-labeled neurons could bedetected.

Injections into the AI and IMHV. To reconfirm theresults from anterograde tracing experiments, six chicksreceived injections of different retrograde tracers into theAI and IMHV of one hemisphere (see Table 1). In fivecases, injections into AI were confined to this structure and


Fig. 9. Photomicrographs and a schematic representation showingretrograde labeling after injections of different retrograde tracers intoneostriatum dorsocaudale (Ndc; A-C) and neostriatum dorsolaterale(Ndl; D-F). A: Confocal laser scanning image of green FluoSpheres(gFS)-labeled neurons in the periectostriatal belt (Ep). Note thatlabeling is absent in the ectostriatal core (E). B: Schematic representa-tion providing overview of the labeled areas shown in A (small box) andC (large box). C: Retrogradely labeled neurons in the Ep and adjacent

neostriatum (N) after an FB injection into Ndc. D: Retrogradelylabeled neurons in the neostriatum frontale, pars trigeminalis (NFT)after an DY injection into Ndl. Note the absence of labeled neurons inthe n. basalis (Bas). E,F: Cluster of retrogradely labeled neurons at arostral (E) and caudal (F) level of the lateral neostriatum (N),resulting from an FG injection into Ndl. FA, tractus fronto-archistriati-cus. Scale bars 5 100 µm.

involved the dorsal (AId) as well as the ventral (AIv) partof the AI. In one animal, there was additionally minimalspread of tracer into the cortex piriformis. Among otherintratelencephalic inputs, which will not be described indetail, injections into AI resulted in strong retrogradelabeling throughout an extensive region of the NC, includ-ing the Nd (Fig. 12C), Ndc (Fig. 12D), and medial parts ofthe Ndl. Moderate labeling became obvious in the neostria-tal and hyperstriatal part of the MNH (Fig. 12E). Further-more, AI injections resulted in distinct labeling in thehippocampus (Hp; Fig 12F).

Fig. 11. Confocal laser scanning images of retrogradely labeledneurons resulting from an injection of green FluoSpheres (gFS) intothe neostriatum dorsocaudale (Ndc) and red FluoSpheres (rFS) intothe neostriatum dorsale (Nd) of the same hemisphere. A: Retrogradelabeling in the rostral neostriatum (N). B: Retrograde labeling in thenucleus dorsolateraleralis posterior thalami (DLP). Arrows point todouble-labeled neurons. C: Retrograde labeling in the shell region ofthe nucleus ovoidalis (OV), the nucleus semilunaris paraovoidalis(SPO), and nucleus subrotundus (SRt). Scale bars 5 50 µm.

Fig. 10. Schematic representation of the distribution of retro-gradely labeled neurons in chick brain coded dorsocaudale neostriatalcomplex (dNC) 8 at six consecutive levels of rostrocaudal sequence.This case received a triple injection of different retrograde tracers atdifferent levels along the medial to lateral axis of the dNC complex inone hemisphere. Diamidino Yellow (DY) was injected into neostriatumdorsolateral (Ndl) (resulting retrograde labeling indicated by stars),Fluoro-Gold (FG) into neostriatum dorsocaudale (Ndc; resulting retro-

grade labeling indicated by dots) and Fast Blue (FB) into neostriatumdorsale (Nd; resulting retrograde labeling indicated by triangles). Theblack areas in E indicate the different injection-sites, which are alsoshown in more detail in Figure 1. Filled squares indicate retrogradelylabeled neurons which are double-labeled by the injections into Nd andNdc. Each symbol represents several labeled cells, the number ofsymbols is roughly proportional to the number of labeled cells. Forabbreviations, see list.


Figure 11

Injections into IMHV (Fig. 13A,B) were mostly re-stricted to the caudomedial part of the hyperstriatumventrale with minimal spread of tracer into the N in one ofthe cases. Injections of retrograde tracers centered onIMHV resulted in moderate retrograde labeling through-out the rostral dNC complex, including rostral parts of theNd and Ndc. In contrast, the most caudal regions of thedNC complex were not labeled. In the Ndc, and to a minordegree also in Nd, many neurons were double-labeled byinjections into AI and IMHV (Fig. 12C,D). Weak labelingbecame obvious in HA. In the MNH, retrogradely labeledneurons were detected in the neostriatal and to a minordegree also in the hyperstriatal part (Figs. 12E, 13C). Onlya few neurons in the MNH were double-labeled by injec-tions into AI and IMHV. Strong labeling became evidentalong the entire rostral to caudal axis of the Hp (Fig. 12F),as well as in the area parahippocampalis (APH, Fig. 13D)and the area corticoidea dorsolateralis (CDL). Within theHp, labeled neurons were mainly confined to the dorsolat-eral subdivision (as defined by Szekely and Krebs, 1996).In the Hp, only very few neurons were double-labeled byinjections into AI and IMHV. A distinct population ofneurons was consistently labeled in lateral aspects of thePA (Fig. 13E). In the thalamus, few labeled neurons werepresent bilaterally in the n. dorsolateralis anterior (DLA)and unilaterally in the n. dorsointermedius posterior(DIP). The n. dorsomedialis anterior (DMA) and posterior(DMP) were only labeled by the injection with spread oftracer into the N. In the mesencephalon, very few labeledneurons became evident in the AVT and SN.

DISCUSSION

The results of the present study further elucidate theorganization of the avian dNC complex and are summa-rized schematically in Figure 14. We found that the dNCcomplex may at least be subdivided into three distinctsubareas (Nd, Ndc, and Ndl), which are mainly character-ized by topographically ordered projections from the beltregions of primary sensory areas. Our results indicate thatthe Nd and Ndc are interconnected with the MNH andIMHV and may be critically involved in auditory andvisual imprinting. In our discussion, therefore, we relatethe afferent and efferent connections of this complex to thethree subdivisions and we speculate about the role of someof these pathways for imprinting-like learning processes.In addition, our results will be discussed with respect tothe comparative neuroanatomy of telencephalic parasen-sory association areas in birds and mammals and to ageneral pattern of sensory processing in the avian telen-cephalon.

Specific connections of the threesubdivisions of the dNC complex

Nd-connections. Previous tracing studies in chicksand pigeons indicate that Nd, which was first described byBonke et al. (1979a) in the guinea fowl, may be character-ized by auditory inputs from L1 and L3 of field L (Bonke etal., 1979a; Wild et al., 1993), reciprocal connections withthe mediorostral N, including the neostriatal part of theMNH (Metzger et al., 1996), as well as efferent projectionsto the AIv (Wild et al., 1993). The distribution of retro-gradely labeled neurons following injections into MNH(Metzger et al., 1996; see their Fig. 5A) and AIv (Wild et al.,1993; see their Fig. 11E) outlines the Nd as V-shaped area

with the narrow part extending from the subventricularzone into the neostriatum. The present results from antero-grade tracing experiments reconfirm this observation,illustrating that the bulk of fibers that originate from theMNH terminates in a V-shaped plexus in Nd. Further-more, the demonstration of functional synaptic contacts inthe Nd after biocytin injections into MNH and, vice versa,in the MNH after biocytin injections into Nd, reconfirmsour observations from a retrograde tracing study (Metzgeret al., 1996) that indicated strong reciprocal connectionsbetween these areas. In contrast to Bonke et al. (1979a),who described a prominent projection from the caudal andintermediate parts (IMHV) of the HV to Nd, we failed todemonstrate retrogradely labeled neurons in these areasfollowing injections into Nd. This might indicate that sucha IMHV-Nd connection may not be monosynaptic (see alsoWild et al., 1993). Concerning the field L projections to Nd,our results are in keeping with a previous study in thepigeon (Wild et al., 1993). As mentioned by these authors,these projections mainly arise from L1 and L3 but not fromL2. Additional presumptive auditory projections to Ndarise from the shell region of the Ov. As described in ringdoves (Durand et al., 1992) and pigeons (Wild et al., 1993),we consistently found retrogradely labeled neurons in thisstructure following injections into Nd. These rich auditoryrelated inputs from L1, L3, and the Ov shell indicate thatNd may function first of all as a higher order associationarea of the auditory system. However, Nd injections alsoresulted in heavy retrograde labeling in the NI/NC transi-tion zone at the ventrolateral borders of field L. This areais beside the rostral HAconsidered as the major somatosen-sory body representation area in the avian telencephalon(Delius and Benetto, 1972; Wild, 1987b; Funke, 1989a),indicating that Nd may also be reached by somatosensoryinformation.

Our data from retro- and anterograde tracing experi-ments reconfirm a projection from Nd to the AI, which hasbeen previously described in the pigeon by Wild et al.(1993). However, in contrast to these authors, who de-scribed well-ordered termination fields in AIv and AId, weobserved a more scattered pattern of anterogradely la-beled fibers in these areas. The efferent projections of Ndto the AI suggest that these projections might provide animportant link between auditory structures and extratel-encephalic efferents (see Wild et al., 1993), since the AIgives rise to descending projections to the brainstem (Zeierand Karten 1971).

Ndc-connections. The Ndc has been discovered as afunctionally defined subregion of the dNC complex by itsstimulus induced metabolic activation in acoustically as

Fig. 12. Confocal laser scanning images of retrogradely labeledneurons in the archistriatum intermedium, pars ventral (Aiv; A) andsubstantia nigra (SN; B) resulting from a injection of green Fluo-Spheres (gFS) into the neostriatum dorsocaudal (Ndc) and red Fluo-Spheres (rFS) into the neostriatum dorsal (Nd). Confocal laser scan-ning images (C–F) of retrogradely labeled neurons resulting from ainjection of gFS into the archistriatum intermedium (AI) and rFS intothe intermediate and medial part of the hyperstriatum ventral(IMHV). C: Retrograde labeling in the Nd and area parahippocampalis(APH). D: Retrograde labeling in the Ndc and APH. E: Retrogradelabeling in the neostriatal (N) and hyperstriatal (HV) of the medioros-tral neostriatum/hyperstriatum ventral (MNH). F: Retrograde label-ing in the hippocampus (Hp). Arrows point to double-labeled neurons.Scale bars 5 100 µm in A, 25 µm in B, 50 µm in C.


Figure 12

well as visually imprinted chicks (Bock et al., 1997). Thepresent data indicate that the Ndc, in terms of its neuronalconnections, is mainly characterized by its strong recipro-cal connections with the Ep and adjacent parts of the N.Projections from the Ep and adjacent N to wide parts of thecaudolateral neostriatum have been described in the pi-geon (Ritchie 1979; Leutgeb et al., 1996). The lack ofretrogradely labeled cells in the ectostriatal core, foundhere after injections into Ndc, clearly reconfirms Ritchie’s(1979) conclusion that these projections exclusively arisefrom the Ep and the adjacent N. Furthermore, the resultsof the present study reconfirm that there is, as previouslydescribed in pigeons (Ritchie and Cohen 1977; Ritchie,1979), a topographical organization of Ep projections to thecaudal neostriatum, since we found the cells of origin of theprojection upon Ndc mainly located in a distinct cluster inthe dorsomedial Ep. The heavily labeled area in theneostriatum, medially adjacent to the E, overlaps with adistinct termination field of fibers arising from the DLP inthe pigeon (Kitt and Brauth, 1982; Gamlin and Cohen,1986). These projections have been implicated as part of asecond visual pathway from the optic tectum to thetelencephalon, since they seem to arise from the tectorecipi-ent caudal part of the DLP (Gamlin and Cohen, 1986).

The E is the major target of the ascending fibers of thetectofugal visual pathway (Karten and Revzin, 1966;Karten and Hodos, 1970; Benowitz and Karten, 1976;Watanabe et al., 1985; for reviews, see Gunturkun, 1991;Shimizu and Karten, 1993), whereas its output is mainlyrestricted to the Ep (Ritchie, 1979). Thus, the projectionsfrom the Ep may provide a major visual input to the Ndc.An involvement of the Ndc in the processing of learnedvisual information is also indicated by recent 2-FDGstudies in the domestic chick, which revealed in visuallyimprinted chicks a significantly enhanced stimulus evokedmetabolic activation of the Ndc (Bock et al., 1997). Further-more, we revealed a considerable input from parts of thevisual Wulst to the Ndc. This is in full agreement withresults derived from retrograde and anterograde tracingexperiments in pigeons, depicting an area comparable toNdc as a major target of projections from the Wulst(Shimizu et al., 1995; Leutgeb et al., 1996). The presentretrograde tracing data indicate that these projectionsmainly arise from the rostral HA. Although the knowledgeabout the exact extent of somatosensory regions within theWulst is far from complete (Wild, 1987b), parts of therostral HA have been implicated to be a somatosensorybody representation area (Delius and Benetto, 1972; Wild,1987b; Funke, 1989a). Thus, beside a visual component,also somatosensory information might be conveyed to theNdc via the Wulst. Furthermore, since learned acousticstimuli induce metabolic activation in the Ndc (Bock et al.,1997) of acoustically imprinted chicks and since we foundminor (presumptive auditory) projections from the Nd tothe Ndc, there may exist a convergence of inputs fromthree different sensory modalities (i.e., visual, auditory,and somatosensory) within Ndc. Thus, Ndc may functionas a polymodal higher-order association area (see Metzgeret al., 1996; Bock et al., 1997).

Ndl-connections. Injections that were confined to themost lateral aspects of the dNC complex resulted in strongretrograde labeling in a part of the rostral N, which hasbeen termed neostriatum frontale, pars trigeminalis (NFT,Wild et al., 1985). This is almost in complete agreementwith previous tracing studies in pigeons (Wild et al., 1985)

and zebra finches (Wild and Farabaugh, 1996), depicting alateral part of the dNC complex as a major recipient ofafferents from the NFT. In contrast to the results of Wild etal. (1985), we found retrogradely labeled neurons mainlyconfined to the rostroventral aspects of the NFT, but notdirectly dorsal to the n. basalis (Bas; compare their Fig. 6).Since the NFT receives strong projections from the adja-cent Bas (Wild et al., 1985; Veenman and Gottschaldt,1986; Dubbeldam and Visser, 1987), the primary sensorystructure of the trigeminal system, the Ndl may functionas a higher-order association area of the trigeminal sys-tem. This view is also supported by the paucity of otherinputs to the Ndl.

Common connections of the dNC complex. Asidefrom the specific connections of the Nd, Ndc, and Ndldiscussed above, we identified some connections, which arecommon for the dNC complex. These include reciprocalconnections with the AIv, efferent projections to the basalganglia, a thalamic input from the DLP, and a mesence-phalic input from the AVT and SN.

As a basic pattern of the archistriatal input of the dNCcomplex, we identified distinct clusters of neurons in theventromedial parts of the AIv projecting either to Nd, Ndc,or Ndl. This indicates a highly ordered topographicalorganization of AIv projections onto the dNC complex.Although the knowledge of the functional neuroanatomy ofthe avian archistriatum is far from complete (for reviewssee Dubbeldam, 1991; Butler and Hodos, 1996), tracingand immunohistochemical studies in the pigeon (Zeier andKarten, 1971; Wynne and Gunturkun, 1995) indicate thatthe archistriatum may be subdivided into several subre-gions, part of which including the archistriatum mediale,archistriatum posterior, and nucleus taeniae (Tn), appearto be homologous to the mammalian amygdala (Zeier andKarten, 1971; Lowndes and Davies, 1994; Butler andHodos, 1996). The present results indicate that in particu-lar the intermediate parts of the archistriatum are recipro-cally connected with the dNC complex. These intermediateregions appear to be mainly associated with the somatosen-sorimotor system and give rise to long descending projec-tions to the brain stem and rostral spinal cord (Zeier andKarten, 1971). This might indicate that the dNC complexmay be an important interface between sensory structuresand extratelencephalic efferents (see Wild et al., 1985,1993). We identified the AI as the only telencephalicstructure that projects bilaterally onto the dNC complex,suggesting that the AI might be an important source ofinterhemispheric information transfer. Although, we foundlabeled neurons at the border of the AIv and Tn, we failedto reconfirm a projection from the Tn proper onto Ndc,which has been recently described in a retrograde tracingstudy in the pigeon (Leutgeb et al., 1996). Whether thisdiscrepancy reflects an important species difference shouldbe clarified by complementary anterograde tracer injec-tions into Tn.

Biocytin injections into Nd and Ndc consistently re-sulted in moderate anterograde labeling in parts of thebasal ganglia. This clearly reconfirms observations inpigeons which indicate that the dNC complex is a majorsource of a ‘‘corticostriatal’’ projection system in birds(Veenman et al., 1995).

Concerning the thalamic input from the DLP, results arein keeping with previous retrograde tracing studies in thechick (Metzger et al., 1996) and pigeon (Funke, 1989b;Waldmann and Gunturkun 1993; Leutgeb et al., 1996),


Fig. 13. Photomicrograph (A) and schematic representation (B) ofa Fast Blue (FB) injection into the intermediate and medial part of thehyperstriatum ventrale (IMHV). C: Retrograde labeling in the neostria-tum (N) and hyperstriatum (HV) resulting from an Diamidino Yellow(DY) injection into the IMHV. D: Retrograde labeling in the area

parahippocampalis (APH) and hippocampus (Hp) resulting from anFB injection into the IMHV. E: Retrograde labeling in the paleostria-tum augmentatum (PA) resulting from an FB injection into the IMHV.NI, neostriatum intermedium; for other abbreviations, see list. Scalebars 5 100 µm.


which demonstrated widespread connections of the DLPonto large parts of the NC. Interestingly, in the presentstudy, DLP neurons were not labeled by injections whichwere confined to Ndl, whereas injections into Nd and Ndcresulted in heavy retrograde labeling in the DLP. The lackof a thalamic input onto Ndl, which has been implicated tobe first of all a higher-order association area of thetrigeminal system (see previous section), may be due to thefact that the principal nucleus of the trigeminal complex(PrV) projects directly to the Bas without an interveningthalamic relay (for reviews, see Dubbeldam, 1991; Butlerand Hodos, 1996). The great number of DLP neurons,which were double-labeled by injections into Nd and Ndc,indicates that the axons of DLP neurons are highlycollateralized within the dNC complex. So far there are noother studies on branching of thalamocortical cells inbirds. In mammals, it has been emphasized that branchedthalamic neurons are directed upon areas which arefunctionally connected (Spreaficio et al., 1981; Bullier etal., 1984; Minchiacchi et al., 1986). This might also be truefor the branched DLP connections upon Nd and Ndc andrenders an additional pathway, by which these areas areinterconnected. The DLP has been proposed to represent apolysensory relay nucleus that integrates somatosensory,visual, and auditory information (Korzeniewska, 1987;

Korzeniewska and Gunturkun, 1990), which might indi-cate that the Nd and Ndc, aside from their specific sensoryintratelencephalic afferents, may be reached by polymodalinformation via the thalamus.

As another prominent input system common to theentire dNC complex, we identified afferents from themesencephalic nuclei AVT and SN. This finding is in linewith results derived from retrograde tracing experimentsin pigeons (Waldmann and Gunturkun, 1993), describingmesencephalic projections from the AVT and SN to acaudolateral field within the dNC complex. In the domesticchick (Metzger et al., 1996), we demonstrated that thedopaminergic input to the Ndc arises mainly from the AVTand to a minor degree from the SN, which is very similar tothe mesolimbocortical dopamine (DA) system in mammals(for review, see Bjorklund and Lindvall, 1984). The presentresults from multiple retrograde tracer injections into thedNC complex suggests that only a small proportion ofneurons in the AVT and SN are collateralized and projectdivergently to different subareas in the dNC complex. Thisis in keeping with the situation in mammals where only asmall proportion of neurons in the ventral tegmental area(VTA) and SN seem to give rise to collateral projections tothe neocortex (for reviews, see Oades and Halliday, 1987;Fallon and Loughlin, 1995).

Fig. 14. Schematic diagram summarizes some of the pathways andthe general pattern of sensory processing defined in the present study.The belt regions (red) of primary sensory areas (light blue) sendprojections (red arrows) to distinct areas (light brown) of the dorsocau-dal neostriatal complex (dNC) complex. From there, information isconveyed (green arrows) either to the archistriatum intermedium (AI)or mediorostral neostriatum/hyperstriatum ventrale (MNH; green)

and intermediate and medial part of the hyperstriatum ventrale(IMHV; green). The MNH and IMHV project to the AId (blue arrows).Black arrows indicate other major pathways defined in the presentstudy. Note that minor reciprocal connections between the MNH andNdc are not included here. The dashed blue arrow from the IMHV tothe archistriatum intermedium, pars dorsale (Aid) indicates a projec-tion defined by Csillag et al. (1994). For abbreviations, see list.


Immunohistochemical studies have indicated that thedNC complex belongs to the most densely DA-innervatedforebrain regions in birds (Waldmann and Gunturkun,1993; Moons et al., 1994; Reiner et al., 1994; Wynne andGunturkun, 1995; Metzger et al., 1996). At the ultrastruc-tural level, dopaminergic axon terminals in the Ndc wereoften observed in close proximity to unstained axon termi-nals, sometimes even forming distinct axoaxonic contacts(Metzger et al., 1996). This might indicate that DA termi-nals in the dNc complex play, as in mammalian neocortex(see Smiley et al., 1992, 1994; Smiley and Goldman-Rakic,1993), an important role in the modulation of other inputsystems.

Implications for a general pattern of sensoryprocessing in the avian telencephalon

Results from many previous tracing studies (see text)indicate the existence of a general pattern of sensoryprocessing in the avian telencephalon (see Veenman et al.,1995). The basic pattern of information flow appears asfollows: Sensory information from subtelencephalic struc-tures is conveyed to the primary sensory areas (e.g., L2 forthe auditory system, the ectostriatal core for the visualsystem, and the n. basalis for the trigeminal system) andthence to their surrounding belt regions (e.g., L1 and L3for the auditory system, Ep for the visual system, and NFTfor the trigeminal system).

The main findings of this study are summarized inFigure 14. Results indicate that the three major subre-gions of the dNC complex are reached by specific afferentsfrom the belt regions of different sensory modalities. Thus,we postulate that, as a third step of a general pattern ofsensory processing in the avian telencephalon, the beltregions of primary sensory areas convey their projectionsto distinct regions in the dNC complex (e.g., Nd for theauditory system, Ndc for the visual system, and Ndl for thetrigeminal system). Furthermore, our results indicate thatas a fourth step, serving sensory-motor integration, infor-mation from the dNC complex might either be directlyconveyed to the archistriatum intermedium (see also Wildet al., 1985, 1993) and/or via the imprinting relevantregions MNH and/or IMHV. The latter possibility is sug-gested by the presence of direct projections from the dNCcomplex to the MNH and IMHV and by direct projectionsfrom the MNH (present study) and IMHV (Csillag et al.,1994) to the archistriatum. Evidence for a parallel process-ing of the dNC output is also derived from the presence ofneurons in the Nd and Ndc that project divergently to AIand IMHV. As a fifth step, information from the AI may betransferred to the striatum (Zeier and Karten, 1971; Bonsand Oliver, 1986; Szekely et al., 1994; Veenman et al.,1995) and/or subtelencephalic structures (Zeier and Karten,1971; Wild and Arends, 1987; Wild et al., 1993; Wild, 1994).

Comparisons with auditory and song controlpathways in oscine songbirds

In all avian species, Field L2a and L2b are the majortargets of auditory projections from the core of the tha-lamic n. ovoidalis (OV; Kelley and Nottebohm, 1979; Bonkeet al., 1979a; Brauth et al., 1987, 1994; Wild et al., 1993;Vates et al., 1996). In addition, there are minor projectionsfrom Ov to fields L1 and L3 in the guinea fowl (Bonke et al.,1979a) and oscine songbirds (Vates et al., 1996). L2a andL2b then relay information to fields L1 and L3 in theguinea fowl (Bonke et al., 1979a) and oscine songbirds

(Vates et al., 1996). In pigeons (Wild et al., 1993) as well asoscine songbirds (Kelley and Nottebohm, 1979; Vates etal., 1996) L1 and L3 thence project to neostriatal areas inthe dorsocaudal telencephalon, which have been termedneostriatum dorsale (Nd) in gallinaceous birds (Bonke etal., 1979a; Metzger et al., 1996) and pigeons (Wild et al.,1993), and hyperstriatum ventrale, pars caudalis (HVc;Nottebohm et al., 1976) in oscine songbirds. The HVc hasbeen recently redesignated as ‘‘higher vocal center,’’ sinceit actually lies within the neostriatum (Nottebohm, 1987).Furthermore, it has been demonstrated that not HVc itselfbut the shelf area surrounding it is the major target offibers arising from L1 and L3 (Kelley and Nottebohm,1979; Fortune and Margoliash 1995; Vates et al., 1996).Similar to Nd (Wild et al., 1993), HVc thence projects to thearchistriatum (Nottebohm et al., 1982; Fortune and Margo-liash 1995; Vates et al., 1996). Based on these correspond-ing pathways it has been proposed that the shelf area ofthe HVc may be considered equivalent to the Nd (Bonke etal., 1979a; Scheich et al., 1991; Wild et al., 1993; Fortuneand Margoliash 1995; Vates et al., 1996). The presentresults give further evidence for this view, by demonstrat-ing that Nd in the domestic chick is, like in pigeons,characterized by afferents from L1 and L3 and efferentconnections to the AI.

Furthermore, our data also indicate a possible correspon-dence of the neostriatal part of the MNH and the medialpart of the magnocellular nucleus of the anterior neostria-tum (mMAN) in oscine songbirds. MAN, which was ini-tially identified as a unified zone (Arnold et al., 1976), maybe subdivided into a medial (mMAN) and lateral (lMAN)portion (Bottjer et al., 1989; Vates et al., 1997). Beside aquite similar location in the mediorostral neostriatum, themediorostral neostriatum in chicks (Wallhausser-Franke,1989; Metzger et al., 1996) and mMAN in oscine songbirds(Vates et al., 1997) share common major afferents from thethalamic n. dorsomedialis posterior (DMP; see also Wild,1987a) as well as an efferent projection to Nd (Metzger etal., 1996; present study) or HVc, respectively (Nottebohmet al., 1982; Bottjer et al., 1989; Vates et al., 1997). Ofparticular interest may be our recent observation that, asin oscine songbirds (Vates et al., 1997), only the mostmedial parts of the neostriatum project to Nd or HVc,respectively, and receive afferents from the DMP (unpub-lished observations). Furthermore, acoustically evokedresponses can be recorded in the MNH (Bredenkotter andBraun, 1997) and mMAN (Vates et al., 1997). However,there are also obvious discrepancies concerning the connec-tions of MNH and mMAN. For example, unlike in oscinesongbirds (Vates et al., 1997), in domestic chicks, DMPprojections onto the MNH are strictly unilateral (Metzgeret al., 1996) and there is a reciprocal connection betweenthe MNH and Nd (present data). Thus, more anatomicaldata are needed to clarify a possible correspondence ofMNH and mMAN. In summary, the present data indicatethat although domestic chicks lack discrete song controlnuclei, some of the pathways that underlie song learningin oscine songbirds may be phylogenetically old and al-ready be present in gallinaceous birds where they mightplay a role in filial imprinting.

Role of the dNC complex inimprinting-like learning paradigms

The present results indicate that the Nd and to a minordegree the Ndc are reciprocally connected with the MNH.


In addition, both Nd and Ndc project to the IMHV. Avariety of area specific morphological, physiological, andmetabolic changes has been observed in the MNH ofdomestic chicks, following auditory filial imprinting (forreviews, see Scheich, 1987; Scheich et al., 1991), and in theIMHV following visual imprinting (for reviews, see Horn,1985, 1991). Based on these observations it has beenpostulated that the MNH is crucially involved in auditoryand the IMHV in visual filial imprinting. In addition, theIMHV has been demonstrated to play a pivotal role inaversive learning paradigms such as passive avoidancetraining in the domestic chick (for reviews, see Rose 1991;Stewart 1991). Previous tracing studies in domestic chickshave indicated that the MNH (Wallhausser-Franke, 1989;Scheich et al., 1991; Metzger et al., 1996) as well as theIMHV (Bradley et al., 1985) are fairly remote from periph-eral sensory input. These observations clearly raise thecritical question by which pathways auditory and visualinformation are conveyed to MNH and IMHV. Althoughthe MNH and the IMHV are not considered as primaryauditory areas, neurons in these structures are responsiveto auditory stimuli (Scheich, 1987; Brown and Horn, 1994;Nicol et al., 1995; Bredenkotter and Braun, 1997). Inaddition, it has been demonstrated that some populationsof neurons in the MNH increase their responsivenesstowards learned, behaviorally relevant auditory stimuli(Bredenkotter and Braun, 1997). The present resultsindicate that both MNH and IMHV are reached by affer-ents from the Nd, which in turn is a major target of theoutput layers L1 and L3 of field L, the avian equivalent ofthe primary auditory cortex (see also Bonke et al., 1979a,b;Wild et al., 1993). Thus, Nd is likely to represent the majorrelay station by which auditory information is conveyed toMNH and IMHV. A similar relay function for the transferof visual information may be fulfilled by the Ndc, which isa major target of the belt regions of the visual ectostria-tum. Neurons in the IMHV have been demonstrated to beresponsive to visual stimuli and there is a learning relatedincrease in visual responsiveness after visual imprinting(Bradford and McCabe, 1994; Brown and Horn, 1994; Nicolet al., 1995). The present results reconfirm an input fromthe HA to IMHV, which has been previously described inthe domestic chick by Bradley et al. (1985). However, weonly detected few labeled neurons in the HA followinginjections of retrograde tracers into IMHV and we failed toreconfirm a projection from the optic tectum to the IMHV,which was described by Bradley et al. (1985). Thus, thehere demonstrated input from the Ndc onto IMHV may beanother important route which transmits visual informa-tion to IMHV. Moreover, since a combination of visual andauditory stimuli has been found to enhance visual imprint-ing in the domestic chick (Van Kampen and Bolhuis, 1993),the convergent projections from Nd (auditory) and Ndc(visual) onto IMHV might provide the anatomical sub-strate to convey auditory and visual information. Anotherinterface function of the dNc complex is suggested by theefferent connections between Nd, Ndc and the AI. Theseconnections point to a role of this region as a sensori-motorinterface, which may be involved in the development of the(motor)-behavioral responses towards a learned stimulusor object.

Under the assumption that the Ndc represents a polysen-sory associative brain region, visual as well as acousticfeatures of imprinting objects should be integrated in thisregion. This view is supported by the observation that in

imprinted chicks the Ndc is highly activated during presen-tation of either acoustic or visual stimuli (Bock et al.,1997). A direct involvement of the Ndc in filial imprintingis also indicated by the fact that chicks, which receivedbilateral Ndc injections of the competitive NMDA antago-nist DL-2-amino-5-phosphono valeric acid (APV) duringthe imprinting experiments, showed a dose-dependentdecrease of imprinting success compared to vehicle-injected controls (Bock et al., 1997). A similar effect hasbeen shown after APV-injections into the MNH (Bock etal., 1996) and IMHV (McCabe et al., 1992), giving furtherevidence that glutamatergic mechanisms are involved infilial imprinting (see also McCabe and Horn, 1988; Wang etal., 1994; Gruss and Braun, 1996).

Comparisons to mammals

In mammals, thalamocortical connections are importantcriteria for the delineation and definition of cortical areas(Rose and Woolsey, 1948; Divac et al., 1978; Uylings andVan Eden, 1990; Butler and Hodos, 1996). The presentresults, together with data from previous tracing studiesin chicks (Metzger et al., 1996) and pigeons (Waldmannand Gunturkun, 1993; Leutgeb et al., 1996), indicate thatthe main thalamic input to Nd and Ndc arises from theDLP. Based on electrophysiological and tracing data, it hasbeen proposed that the avian DLP might be equivalent tothe posterior thalamic complex (Po) of mammals (Korze-niewska, 1987; Wild, 1987b; Korzeniewska and Gun-turkun 1990; Waldmann and Gunturkun, 1993). In the Pocomplex (Poggio and Mountcastle, 1960; Curry, 1972;Chalupa and Fish, 1978; for review, see Jones, 1985), aswell as in the DLP (Korzeniewska 1987; Korzeniewska andGunturkun 1990), a great percentage of neurons aresensitive to stimuli of different sensory modalities. Further-more, the Po complex (Berkley, 1980; Berkley et al., 1986;Hicks et al., 1986) and DLP (Arends et al., 1984; Gamlinand Cohen, 1986; Wild, 1989; Korzeniewska and Gun-turkun 1990) share common afferents from the dorsalcolumn nuclei and the reticular formation. The corticaloutput of the mammalian Po complex is mainly directed tothe primary sensory cortex (SI; Nothias et al., 1988; Fabriand Burton, 1991; Krubitzer and Kaas, 1992; Lu and Lin,1993) and to more caudally situated regions in the parieto-temporal association cortex, which are located between SIand the primary auditory and visual cortices (Vaudano etal., 1991; Krubitzer and Kaas, 1992; Di et al., 1994). Thetelencephalic output of the DLP is widespread (for discus-sion, see Metzger et al., 1996). Nevertheless, some of thetelencephalic connections of the DLP show fundamentalsimilarities to those of the Po. For instance, DLP projectsto the medial neostriatum intermedium and caudale (NI/NC), which is considered as a major somatosensory bodyarea in the telencephalon (Wild, 1987b; Funke 1989a,b).With regard to the here-described DLP projections to theNd and Ndc (see also, Waldmann and Gunturkun 1993;Metzger et al., 1996), we postulate that these projectionsmight be equivalent to the Po projections onto the parieto-temporal association cortex in mammals. Mainly based onstudies in monkeys, these parietotemporal areas havebeen referred as parasensory association cortex (Pandyaand Seltzer, 1982; Pandya and Yeterian, 1985). Theseauthors further distinguish between first and second orderparasensory association areas, which are characterized asfollows: First-order association areas are located immedi-ately adjacent to the primary sensory cortices from which


they receive direct input. In the avian telencephalon, thesecriteria are fulfilled by the belt regions of primary sensoryareas, which are located immediately adjacent to theprimary sensory areas from which they receive majorinput (for reviews, see Dubbeldam, 1991; Rehkamper andZilles, 1991; Veenman et al., 1995). Thus, these beltregions might be functionally equivalent to first orderparasensory areas in the mammalian neocortex. Second-order association areas in the mammalian neocortex re-ceive only indirect cortical sensory input via the first orderassociation areas (Pandya and Seltzer, 1982). Our resultsindicate that this criteria is fulfilled by the Nd, Ndc, andNdl, since their major telencephalic inputs arise, respec-tively, from the belt regions of primary auditory, visual,and trigeminal areas. Together with the above-discussedpossible correspondence of the mammalian Po complexand the avian DLP, these findings suggest that at least Ndand Ndc might be equivalent to second order parasensoryassociation areas in the mammalian parietotemporal neo-cortex and provide new doubts on the view that parts of thedNc complex should be considered equivalent to the mam-malian prefrontal cortex (for discussion, see also Metzgeret al., 1996; Veenman et al., 1997). With regard to Ndl, wefailed to demonstrate a direct input from the DLP, whereasit is also characterized by its strong input from the NFT,the belt region of the trigeminal system.

Also in terms of its output, the dNC complex mightsubserve a similar relay function as the mammalianparietotemporal neocortex. The association areas in themammalian parietotemporal neocortex provide an anatomi-cal link between primary sensory areas and limbic as wellas prefrontal brain regions (for review, see Pandya andSeltzer, 1982; Creutzfeldt, 1995). Comparably, large partsof the dNC complex project to the archistriatum as well asto higher associative forebrain regions such as the MNHand IMHV. Parts of the avian archistriatum have beenimplicated to be equivalent to the mammalian amygdala(Zeier and Karten, 1971) and both MNH (Metzger et al.,1996) and IMHV (Horn, 1985) have been discussed asavian equivalents of the prefrontal cortex. In addition,electrophysiological and neuroanatomical studies in theparietotemporal neocortex of monkeys (for reviews. seePandya and Yeterian, 1985; Van Essen et al., 1990; Felle-man and Van Essen, 1991) and rodents (Vaudano et al.,1991; Di et al., 1994; Barth et al., 1995) have indicated thatthis part of neocortex consists of a mosaic of uni- andpoly-modal association areas. The present results provideat least anatomical evidence that this may also be true forthe avian dNC complex, since there is convergence of inputfrom at least two different sensory modalities in the Ndand Ndc, whereas Ndl may be exclusively reached bytrigeminal input.

Taking all these considerations and the proposed modelfor a general pattern of sensory processing in the aviantelencephalon into account, our study indicates that thereare substantial similarities between the avian and mam-malian telencephalon in the cascade of relays from the beltregions of primary sensory areas to higher associativeareas. These observations support the view that largeparts of the avian telencephalon including the Wulst anddorsal ventricular ridge (DVR) may be considered akin tomammalian neocortex (see Karten 1969, 1991; Nauta andKarten, 1970; Dubbeldam, 1991; Rehkamper and Zilles,1991; Shimizu and Karten, 1991; Butler, 1994; Veenman etal., 1995; Metzger et al., 1996; Schnabel et al., 1997).

ACKNOWLEDGMENTS

We are grateful to Prof. Hans-Joachim Bischof forcritical comments on the manuscript. We thank Dr. W.Zuschratter for advice concerning confocal-laser-scanningmicroscopy and U. Kreher and P. Kremz for excellentphotographic assistance.

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