organization and efferent connections of the archistriatum of the mallard,anas platyrhynchos l.: an...

Organization and Efferent Connectionsof the Archistriatum of the Mallard,

Anas platyrhynchos L.: An Anterogradeand Retrograde Tracing Study

J.L. DUBBELDAM,* A.M. DEN BOER-VISSER, AND R.G. BOUT

Neurobehavioral Morphology, Institute of Evolutionary and Ecological Sciences,Leiden University, 2300 RA Leiden, The Netherlands

ABSTRACTThe intratelencephalic and descending connections of the archistriatum of the mallard

were studied using anterograde and retrograde tracers. Autoradiography after injections of[3H]-leucine served to visualize the intratelencephalic and extratelencephalic efferent connec-tions of the archistriatum. Horseradish peroxidase (HRP), HRP–wheatgerm agglutinin, andfluorescent tracers were used to identify the precise origin of the projections to the variousterminal fields found in the anterograde experiments. Four main regions can be recognized inthe archistriatum of the mallard: (1) the rostral or anterior part that is a source ofcontralateral intratelencephalic projections, in particular to the contralateral archistriatum;(2) the dorsal intermediate archistriatum that is the origin of a large descending fiber system,the occipitomesencephalic tract, with projections to dorsal thalamic nuclei, the medialspiriform nucleus, the intercollicular nucleus, the deep tectum, parts of the mesencephalicand bulbar reticular formation, and the subnuclei of the descending trigeminal tract. Thereare no direct projections to motor nuclei. This part corresponds to the somatic sensorimotorpart as defined by Zeier and Karten (1971, Brain Res. 31:313–326); it also contributes to theipsilateral intratelencephalic connections and, to a lesser degree, to contralateral intratelen-cephalic connections. (3) The ventral intermediate archistriatum is another region that is alsoa source of intratelencephalic projections, in particular of those to the lobus parolfactorius.The most lateral zone sends fibers to the septal area. (4) The caudoventral intermediate andposterior archistriatum is another region that is a source of the projections to the hypothala-mus and thus corresponds to the amygdaloid part of the archistriatum as defined by Zeier andKarten; it also contributes a modest component to the occipitomesencephalic tract. Thedifferent cell populations are not spatially separated, which makes it impossible to recognizedistinct subnuclei within the four main regions of the archistriatum of the mallard. J. Comp.Neurol. 388:632–657, 1997. r 1997 Wiley-Liss, Inc.

Indexing terms: sensorimotor; amygdala; intratelencephalic circuits; extratelencephalic

projections

The archistriatum in birds is the source of a largeextratelencephalic fiber system, the occipitomesencephalictract. It is also a source of many intratelencephalic connec-tions. Many studies have examined the role of the archi-striatum in vocalization (e.g., Nottebohm, 1993; Striedter,1994) and feeding (e.g., Wild et al., 1985; Dubbeldam andVisser, 1987) and in behavioral changes after lesions (e.g.,Phillips, 1964; Phillips and Youngren, 1971; Ramirez andDelius, 1979; many studies are summarized in Tombol andDavies, 1994). Based on the pattern of afferent and effer-ent connections of the archistriatum in the pigeon (Zeierand Karten (1971, 1973), four main regions can be recog-nized: anterior (Aa), intermediate (Ai), medial (Am), and

caudal or posterior (Ap). It is common use to subdivide thearchistriatum into a sensorimotor area (Aa 1 Ai) and alimbic/amygdaloid area (Am 1 Ap). An even finer subdivi-sion has been proposed (Zeier and Karten, 1971, 1973), buta Golgi study of the archistriatum has revealed a uniformdistribution of cell types throughout the archistriatum of

Grant sponsor: Leiden University; Grant number: EEW/6.94.9.*Correspondence to: Dr. J.L. Dubbeldam, Institute of Evolutionary and

Ecological Sciences, Leiden University, POB 9516, 2300 RA Leiden, TheNetherlands. E-mail: [email protected]

Received 6 May 1996; Revised 20 June 1997; Accepted 29 June 1997

THE JOURNAL OF COMPARATIVE NEUROLOGY 388:632–657 (1997)

r 1997 WILEY-LISS, INC.

the chicken (Tombol and Davies, 1994). New data on theintrinsic organization of the telencephalon (review inDubbeldam, 1991) and the availability of new anterogradeand retrograde tracing techniques permit a more precisedetermination of the sources of archistriatal afferents andthe targets of its efferents.

In the present study, the efferent connections of thearchistriatum in the mallard are analyzed by using acombination of anterograde and retrograde tracing meth-ods. In particular, we analyzed which parts of the archi-striatum are part of the sensorimotor circuit controllingthe activity of the motor centers of the jaw, tongue, andneck muscles. More generally, our aim was to determinewhether the detailed subdivisions as proposed for thepigeon could be found in the mallard. Experiments usinganterograde tracers serve mainly to establish the overallpattern of archistriatal projections. The retrograde tracerexperiments enabled us to assess the existence of specificsubnuclei within the archistriatum of the mallard.

MATERIALS AND METHODS

The experimental animal was the mallard, Anas platy-rhynchos L. Only adult drakes were used. The animalswere obtained from a commercial supplier and kept in thelaboratory with food and water available ad libitum. Allinjections and lesions were made stereotactically by using

the atlases of Zweers (1971: brainstem) and of Bol andDubbeldam (unpublished: telencephalon). The experi-ments were performed under loco-equithesin anesthesia.

Anterograde tracing experiments:Autoradiography

Quantities of 0.1–0.5 µl [3H]-leucine (10–20 µC/µl) wereinjected in various regions of the archistriatum. After 7days, the animals were perfused under deep anesthesiawith 10% formaldehyde solution. The brains were embed-ded in gelatin and cut on a freezing microtome into 24-µmsections. The sections were mounted on slides, defatted inxylene, and dipped in Ilford G5 emulsion. After exposuretimes of 4, 8, or 16 weeks at 4°C, parallel series weredeveloped and fixed. The sections were counterstainedwith Cresyl Fast Violet (Certistain) and examined withbrightfield and darkfield illumination.

Serial sections stained with the Fink-Heimer method afterdamaging small parts of the archistriatum were availablefrom a previous study (Arends and Dubbeldam, 1982). Weused these sections to verify trajectories of the fiber systems.

Retrograde experiments

Two sets of experiments were undertaken. In one set,the animals received an injection of 0.2–0.4 µl of 25%horseradish peroxidase (HRP; Serva, Heidelberg, Germany)

Abbreviations

Nomenclature according to Breazile and Kuenzle, 1993 (NAA). When other terms are used, the NAA term appearswithin brackets.

A archistriatumAd/v archistriatum rostrale, pars dorsalis/ventralisAi archistriatum intermediumAm archistriatum medialeAn nucleus angularisAp archistriatum caudaleBas nucleus basalisCA commissura anterior [rostralis]CC canalis centraliscd subnucleus caudalis of TTDCPi cortex piriformisDA tractus dorso-archistriaticusDIP nucleus dorso-intermedius posterior [caudalis] thalamiDLP nucleus dorsolateralis posterior [caudalis] thalamiE ectostriatumFA tractus fronto-archistriaticusFLM fasciculus longitudinalis medialisFPL fasciculus lateralis prosencephaliFRL formatio reticularis lateralis mesencephaliFRM formatioreticularis medialis mesencephaliFV funiculus ventralisHA hyperstriatum accessoriumHD hyperstriatum dorsaleHIS hyperstriatum intercalatum supremumHV hyperstriatum ventraleHy hypothalamusIA area intertrigeminalis (Arends and Dubbeldam, 1982)ICo nucleus intercollicularisIM nucleus intermedius medullae oblongataeIMC nucleus magnocellularis isthmiINP nucleus intrapeduncularisip subnucleus interpolaris of TTDIPC nucleus parvocellularis isthmiLAD lamina archistriatalis dorsalisLFB lateral forebrain bundle (FPL)LH lamina hyperstriaticaLMD lamina medullaris dorsalisLoC locus [nucleus] ceruleus

LPO lobus parolfactoriusmV nucleus motorius nervi trigeminimVII nucleus motorius nervi facialisN neostriatumNf,d/l/m/v neostriatum, pars frontalis [rostralis] dorsalis/ lateralis/

medialis/ventralisNi,l neostriatum, pars intermedia lateralisNLM nucleus lentiformis mesencephaliNM neostriatum, pars medialisNV nervus trigeminusNVIII nervus vestibulocochlearisnLL nuclei lemnisci lateralisOI oliva inferior [complexus olivaris caudalis]Ov nucleus ovoidalisPA paleostriatum augmentatumPL nucleus lateralis pontisPP paleostriatum primitivumPPC nucleus principalis precommissuralisPrV nucleus sensorius principalis nervi trigeminiRGc nucleus reticularis gigantocellularisRot nucleus rotundusRPc,dl/vm nucleus reticularis parvocellularis, pars dorsolateralis/ven-

tromedialisRu nucleus ruberSG substantia gelatinosaSGC stratum griseum centraleSL nucleus septalis lateralisSpM nucleus spiriformis medialisSRot nucleus subrotundusSSp nucleus supraspinalis [n. hypoglossi]STr nucleus [subnucleus] subtrigeminalisTn nucleus teniaeTOM tractus occipitomesencephalicusTSM tractus septomesencephalicusTTD tractus descendens nervi trigeminiVeD nucleus vestibularis descendensVP paleostriatum ventrale

ORGANIZATION OF ARCHISTRIATUM IN MALLARD DUCK 633

in distilled water or of 0.03–0.2 µl of a mixture of 0.5% HRPconjugated to wheat germ agglutinine (WGA-HRP; Sigma,St. Louis, MO) and 10% HRP. In some experiments,

WGA-HRP was delivered iontophoretically by using analternating current of 2 or 5 µA for 20–30 minutes. After asurvival period of 3 days, the animals were perfused with

Fig. 1. Photographs of cresyl-stained sections through the rostral pole (A), intermediate zone (B), andcaudal pole (C) of the archistriatum showing the main subdivisions of this region. D: Section througharchistriatum stained for acetylcholine esterase (AChE) activity. Scale bars 5 1 mm. For legends inFigures 1–18, see list of abbreviations.

634 J.L. DUBBELDAM ET AL.

saline 1 0.2% heparine, followed by 2% paraformaldehyde 11.5% glutaraldehyde in 0.1 M phosphate buffer and by 20%sucrose in phosphate buffer. Serial transverse sectionswere cut on a freezing microtome, and parallel series wereprocessed with the diaminobenzidine-tetrahydrochloride

(Adams, 1981) and tetramethylbenzidine (Mesulam, 1982)procedures and counterstained with Cresyl Fast Violetand Neutral Red, respectively.

In the second set of experiments, fluorescent tracerswere used. The birds received injections of 0.3 µl 3% Fast

Figure 1 (Continued.)


Blue (FB) and of 0.3 µl 2% diamino-yellow dihydrochloride(DY) in distilled water in different regions of the brain.After a survival period of 3 to 10 days, the animals wereperfused successively with avian saline, 12% paraformal-dehyde in distilled water, and a 20% sucrose solution. The40-µm cross sections were cut on a freezing microtome.Sections were mounted on slides and examined under aLeitz fluorescent microscope equipped with a filter systemproviding light of 360 nm.

Nissl-stained serial sections were available as a refer-ence; these had previously been used to prepare a stereo-taxic atlas of the forebrain (Bol and Dubbeldam, unpub-lished). This atlas uses the same stereotactic plane as theatlas of the brainstem of the mallard (Zweers, 1971). Anumber of sections were stained for acetylcholinesterase(AChE) activity according to the method of Koelle asmodified by Tsuji (1974).

The nomenclature of the Nomina Anatomica Avium(Breazile and Kuenzel, 1993) is used in this study (seeAbbreviations). The protocols used in this study were

approved by the Animal Care and Use Committee ofLeiden University.

RESULTS

Anatomy of the archistriatum

The subdivisions of the archistriatum (Dubbeldam andVisser, 1987) are shown in Figures 1 and 2. In the rostralpole (archistriatum rostrale), a dorsal region (Ad), withlarge, round, or polygonal and rather lightly stained cells,and a ventral region (Av), with slightly smaller and darkercells, can be distinguished. The intermediate zone (archi-striatum intermedium; Ai) and the caudal pole (archistria-tum caudale, Ap) contain an homogeneous population ofpolygonous cells that are only slightly smaller than thoseof Ad (Fig. 1A,B). The most medial zone is characterized bythe presence of large and lightly stained cells scatteredbetween the converging fibers of the occipitomesence-phalic tract and rostral commissure (archistriatum me-

Fig. 2. Five sections from rostral (X 5 5.6) to caudal (X 5 2.4) showing the subdivisions of thearchistriatum in the mallard. The shaded areas indicate a region with high AChE activity in the neuropil(compare with Fig. 1D).


diale, Am; Figs. 1B, 2). Many fibers of the frontoarchistri-atic tract pass through the lateral part of archistriatum,giving it the appearance of a belt area, the lamina archi-striatalis dorsalis (LAD). The cells in LAD are elongateand rather darkly stained. The smallest cells are found inthe medioventral nucleus teniae (Tn). In the sectionsstained for AChE activity (unpublished observations), theventrolateral zone of archistriatum is positive (Figs. 1D,2). The archistriatum can be further subdivided based onthe pattern of afferent connections.

In all experiments using anterograde tracers, both in-tratelencephalic and extratelencephalic projections werefound. The two groups of efferent connections are de-scribed separately; each description is followed by a descrip-tion of retrograde experiments.

Intratelencephalic connections

Anterograde experiments. The following descriptionis based on experiments using autoradiography (n 5 4).Two representative cases are described.

Figure 3 shows the distribution of silver grains overdifferent parts of the forebrain after a [3H]-leucine injec-tion into the dorsal half of Ai. Labeled fibers in theipsilateral hemisphere can be followed through severalpathways. Fibers reach the lateral parts of the caudal andintermediate neostriatum, the lateral half of the dorsalneostriatum frontale (Nf; Dubbeldam and Visser, 1987),dorsal hyperstriatum ventrale (HV), dorsal hyperstriatum(HD), and hyperstriatum intercalatum supremum (HIS;Fig. 3E–I) through the dorsoarchistriatal tract (DA). Asecond group of fibers follows the lamina medullarisdorsalis coursing medially; the fibers then turn dorsallyand, passing through the neostriatum (N) and hyperstria-tum ventrale, project to HD and HIS (Fig. 3C–F). At morerostral levels, dispersed fibers can be seen passing throughneostriatum and HV, apparently without projections tothese regions. A third group of fibers penetrates thepaleostriatal complex, in particular the paleostriatumaugmentatum (PA) and n. intrapeduncularis (INP) and thelateral lobus parolfactorius (LPO). It is difficult to decidewhether these are just passing fibers or represent projec-tions to these areas. The high density of silver grainssuggests that they project to these areas (Fig. 5A). There isa dense silver precipitation over Ad (Fig. 3D,E). Fibers tothe contralateral hemisphere cross through the commis-sura anterior (Fig. 3E). Part of these fibers project to therostral Am, and other fibers pass rostral to the archistria-tum and penetrate the paleostriatal complex and DA. Theoverall pattern of silver grains is comparable to that in theipsilateral hemisphere, although less dense.

Figure 4 depicts the distribution of silver grains after a[3H]-injection into the Am. The pattern of intratelence-phalic connections differs considerably from the previouscase because the most prominent projection is to theventromedial LPO and the region ventral to the septum(Fig. 4D); this area may correspond to nucleus accumbens(see Discussion). Labeled fibers to this region were alsoobserved after an HRP-WGA injection deep ventrally intothe Ai. Only sparse silver deposits were found in theregions described in the first experiment. The other twoautoradiography experiments fit the pattern of the firstexperiment.

Fink-Heimer preparations after lesions in different partsof the archistriatum (Fig. 13) are not very helpful inrevealing details of the intratelencephalic projections. The

intratelencephalic fibers are rather small and widelyscattered, making it difficult to follow them to theirtargets. However, the general picture is not different fromthat of the autoradiographs.

Retrograde experiments. A large number of HRPinjections into the various presumptive terminal fields ofarchistriatal efferents established the precise origin ofthese fibers. The following description is mainly restrictedto the occurrence of cells in the archistriatum.

Neostriatum and hyperstriatum ventrale (n 5 10). HRP-injections were placed in various regions of N and HV.Such injections always labeled cells bilaterally in thearchistriatum. Figure 6 shows one case that is characteris-tic for all experiments. Ipsilaterally, cells are found mainlyin the dorsal Ai, in some cases extending into the lateralAp; occasionally, a few cells occurred in Ad. Contralater-ally, labeled cells are restricted to the dorsal Ai (Fig. 7B;after an injection into the lateral neostriatum, Fig. 8B). Inan additional double-labeling experiment, cells were foundagain in the dorsolateral Ai and Ap after injecting fluores-cent tracers into the Nf (from medial) and the medial HD 1HV (from dorsal), respectively. Only a few double-labeledcells were found. Two HRP injections into the intermediateN and in N 1 HV, respectively, included parts of thepaleostriatal complex; in these cases, cells were restrictedto the dorsal Ai.

His-HD-dorsal HV (n 5 2). The HRP injections labeledmany cells in Ad, including rostrodorsal Am, and in thelateral half of Ai and Ap. Injections restricted to HA (Fig.8A; n 5 2) did not label cells in the archistriatum; however,when such injections extend into HD (n 5 3), the samedistribution of labeled cells was found as in the first set ofexperiments.

Lobus parolfactorius (Fig. 9). The HRP injections (n 53) into the medial or central parts of LPO (with a horizon-tal approach from contralateral) predominantly labeledcells in the ventral parts of Ai and Am, in the larger part ofAp, and a few cells in Av. A more ventral injection centeredin the area ventral to the septum and the accumbensregion (Fig. 8C) labeled cells in the same regions, albeitmore medially. After an experiment with injections of DYand FB in His-HD-HV and in LPO, respectively, manylabeled cells were found in the Av, the dorsolateral andventral Ai, and in the Ap. This experiment combines thetargets of the previous two groups of experiments, result-ing in a similar distribution of labeled cells. In thisfluorescent tracer experiment, a small number of double-labeled cells was found (Fig. 10).

Archistriatum. The HRP injections into the archistria-tum or interrupting the commissura rostralis (anterior)labeled cells in the contralateral Ad.

Comments: Retrograde experiments. The ventral halfof the archistriatum (Av and ventral Ai) and Ap appear tobe the source of projections to LPO and regions medial toit. The dorsal Ai, in some experiments including thedorsolateral part of Ap, is the source of projections to thevarious parts of the neostriatum, HD, and His. Theanterograde experiments suggest that HV may containmainly passing fibers, although projections to its mostdorsal zone cannot be excluded. There are no indications ofa topological organization of these archistriatal efferents.The Ad is mainly a source of projections to the contralat-eral archistriatum. Table 1A summarizes the results ofboth anterograde and retrograde experiments.


Fig. 3. Series of sections showing the intratelencephalic distribution of silver deposits (black dots)after a [3H]-leucine injection into the intermediate archistriatum. Experiment As25.


Fig. 4. Intratelencephalic and hypothalamic distribution of silver deposits after a [3H]-leucineinjection into the medial part of archistriatum (Am). Experiment As23.


Extratelencephalic connections

Anterograde experiments. Figures 11 and 12 showthe trajectory and terminal fields of the occipitomesence-phalic tract (TOM) as visualized after a [3H]-leucineinjection into the intermediate archistriatum. This is the

same experiment illustrated in Figure 3. A comparablepattern of projections was seen in Fink-Heimer prepara-tions after damaging this part of the archistriatum. Thetrajectory of the occipitomesencephalic tract is comparableto that described in the pigeon (Zeier and Karten, 1971).

Fig. 5. Photographs of autoradiograms after [3H]-leucine injec-tions into the archistriatum. A: Distribution of labeling over PA andINP with fibers crossing PP (darkfield microscopy). B: Distribution oflabel in the dorsal nucleus motorius N.XII (n. intermedius); thisphotograph suggests mainly the presence of passing fibers (darkfield).

C: Photograph showing part of an injection site in the archistriatumand labeled TOM; note projections to medial reticular formation(arrows) and n. intercollicularis. D: TOM 1 dense projection to themedial spiriform nucleus. Scale bars 5 500 µm in A,D, 100 µm in B,800 µm in C.


Its fibers collect medially in the archistriatum into fas-cicles that form the beginning of the TOM. At the level ofthe anterior commissure, this tract takes a ventral andcaudal turn entering the thalamus (Figs. 4C, 11B). TheTOM is a distinct tract that can be followed down into therostral cervical cord. Along its entire course, fibers split off

to terminate in specific cell groups and in parts of thereticular formation. Terminals are found ventral to therotundal nucleus (n. subrotundus, Fig. 11B) and the prin-cipal precommissural nucleus (Fig. 11B,C), in the posteriordorsointermedial (DIP) and dorsolateral (DLP) nuclei ofthe dorsal thalamus (Fig. 11D), the intercollicular nucleus

Figure 5 (Continued.)


(Fig. 11C,D), and medial spiriform nucleus (Figs. 3D, 11D).Modest numbers of fibers enter the optic lobe to disperse instratum album and griseum centrale of the mesencephalictectum. Rather dense silver precipitation was found overthe medial reticular formation of the thalamus and mesen-cephalon (Fig. 11B–D). Fibers pass the lateral lemniscalnuclei medially, with a few fibers entering the lateral ponsnucleus (Figs. 11D, 12A). Other targets of the TOM are thelocus ceruleus (Fig. 12A) and subcerulean (Fig. 12A,B)nuclei.

At the level of the trigeminal and facial motor nuclei,TOM is a compact bundle passing the principal trigeminalsensory nucleus medially. A high density of silver grains isfound over the ipsilateral parvocellular reticular forma-tion but not over the motor nuclei (Fig. 12B,C). Fineterminal debris occurred over the intertrigeminal area.More caudally, the density of silver grains was high overthe dorsomedial zone of the parvocellular reticular forma-tion (RPc,dl) but more modest over the ventromedial zone(RPc,vm) and the subtrigeminal nucleus. Other targets are

the subnuclei oralis and interpolaris of the descendingtrigeminal tract. From the level of the fifth nerve, modestnumbers of labeled fibers were seen crossing the midlineto terminate in the contralateral subtrigeminal nucleus(Fig. 12E,F). The ipsilateral fibers were followed caudallyinto n. centralis medullae oblongatae, pars dorsalis (thecaudal continuation of RPc; Bout, 1987), and into the firsttwo segments of the cervical cord (Fig. 12H–K). Manyfibers crossed through the dorsal hypoglossal nucleus (n.intermedius), apparently without terminals in this nucleus(Fig. 4B).

In another experiment, the [3H]-leucine injection in-cluded the medial part of the archistriatum (Fig. 5). Thisinjection labeled the hypothalamic component of TOM.These fibers followed a more medial pathway and werefiner than those of the TOM proper. This componentprojected over the whole length of the hypothalamus, withthe densest projection passing to its caudal part.

Ten experiments using the Fink-Heimer technique aftersmall lesions of various parts of the archistriatum were

Fig. 6. Distribution of labeled cells in the ipsilateral (filled circles) and contralateral (open circles)archistriatum after an injection of horseradish peroxidase (HRP) into the HD-HV-Nf; black area (X 5 3.2)indicates injection site. Experiment HR248.


available (Fig. 13). The experiments were particularlyuseful to provide details about the source of descendingarchistriatal projections. In most cases, the lesions weremade from a lateral approach avoiding the overlying partsof the hemisphere. The overall picture resulting from theseexperiments support the autoradiographic data. Degenera-tion debris was found in the nucleus spiriformis medialis

(SpM) after lesions in the lateral half of the dorsal Ai (n 53; e.g., 5 in Fig. 13) but not after damaging the intermedi-ate or ventral parts of the Ai. This projection on SpM wasalso found after an Phaseolus-lectin injection into thedorsolateral Aa/Ai. Tectal projections were found specifi-cally after damaging the intermediate zone of Ai (n 5 3;e.g., 14 in Fig. 13). This intermediate region, the dorsal Aa

Fig. 7. Photographs of labeled cells in the archistriatum. A: Lowmagnification view shows distribution of cells after an injectionincluding SpM and lateral reticular formation of mesencephalon

(experiment HR 451). B: A small number of labeled cells in the medialAi after an injection into the contralateral lateral neostriatum (experi-ment HR428; also see Fig. 8B). Scale bars 5 200 µm in A, 100 µm in B.


(e.g., 11 in Fig. 13) and the most lateral zone of the dorsalAi (9 in Fig. 13) contributed little to the projections to themore caudal (bulbar) parts of the brainstem. Experiment11 confirmed the existence of a projection from the Ad tothe contralateral Ad (see section on IntratelencephalicConnections).

Retrograde experiments. The origin of the variousdescending archistriatal projections has been confirmed byinjections of HRP, HRP-WGA, and fluorescent tracers in aseries of terminal fields found after the anterograde experi-ments. The following observations are described fromcaudal to rostral; the description is limited to labeling inthe archistriatum.

Parvocellular reticular formation (two HRP-injectionsin n. centralis medullae oblongatae dorsalis (CMOD), fourin more rostral parts). The HRP injections in these areas

labeled cells mainly in the dorsal half of the intermediatearchistriatum, with occasional labeled cells in Aa (Figs. 14,15). There was a tendency for labeling in the dorsolateralhalf after injections into RPc,dl and for labeling in thedorsomedial half after injections into RPc,vm (Fig. 15).Labeled cells in the Ai were also found after HRP injectionsin segment 2 of the cervical cord (Zijlstra, 1992). In allexperiments, small numbers of labeled cells were found inthe contralateral Ai; these cells probably innervate thecontralateral n. subtrigeminalis. After injections with dif-ferent fluorescent tracers in the reticular formation at thelevel of the supraspinal (ventral hypoglossal) nucleus andof the trigeminal motor nuclei, respectively, fluorescentcells were found to mingle in the dorsal Ai, but nodouble-labeled cells were found (Tellegen and Dubbeldam,1996).

Fig. 8. Photographs showing three HRP–wheatgerm agglutinininjection sites in the telencephalon. A: Injection (from dorsal) into thelateral half of the right HA (experiment HR430); this injection labeledno cells in the archistriatum. B: Injection from lateral in the lateral

neostriatum (experiment HR428; compare with Fig. 7B). C: Injectionin subseptal region (from contralateral; experiment HR295); the re-sulting labeling is the same as in experiment III in Figure 9. Scalebar 5 200 µm.


Injections into CMOD and RPc always labeled modestnumbers of cells around the lateral forebrain bundle (Figs.14, 15). These cells have been identified as the bed nucleusof the lateral forebrain bundle (Arends and Dubbeldam,1982), but they may be part of the ventral paleostriatum(Dubbeldam and Visser, 1987).

Parabrachial region. Small HRP injections (n 5 3) intothe parabrachial region, just rostral to the principal sen-sory nucleus and motor cell groups of the trigeminal nerve(N.V) and lateral to TOM, labeled many cells in the ventralpart of the archistriatum intermedium and medial archi-striatum caudale but no cells in the dorsal Ai (Fig. 16). Twolarge injections in this region using fluorescent tracerscovered more medial parts including (part of) the n.ceruleus. These injections labeled many cells in the dorsalAi and, in one case, a modest number of cells in the ventralAi. We do not have specific injections in locus ceruleus andthe subcerulean nuclei, but HRP injections interruptingTOM rostral to these nuclei always result in the presenceof labeled cells in the Ai and Ap.

Tectum (n 5 3). Injections covering the tectal layerslabeled cells in the intermediate region of Ai (Fig. 16). Aninjection into the intercollicular nucleus, ventral to theSpM, labeled cells in the dorsal Am and ventral Ai and afew cells in an intermediate zone of Aa and Ai and in Ap.Labeled cells were found also in nucleus ovoidalis. Asecond injection in the intercollicular nucleus also touchedon SpM and interrupted part of the anterior commissure.In this case, labeled cells were found in the Ad in additionto modest numbers in the intermediate Ai and Ap.

N. spiriformis medialis. Two injections covering SpMand its direct surroundings labeled cells mainly in thedorsal Ai (Figs. 7A, 18). These injections also filled thefibers of the pedunculus cerebellaris rostralis (brachiumconjectivum). More medial injections always interruptedTOM, labeling many cells in the archistriatum. One injec-tion was restricted mainly to the medial mesencephalicreticular formation; labeled cells were found caudally inthe intermediate and ventral Ai.

Fig. 9. Distribution of labeled cells in the archistriatum after three injections (black areas) in differentparts of LPO. Open circle, labeled by injection I; filled circle, labeled by injection II; black triangle, labeledby injection III.


Hypothalamus (n 5 3). In one experiment, a massiveHRP injection covering a large part of the hypothalamuswas made. Labeled cells were found medially in theventral Ai and Ap (Fig. 17). A smaller injection into thesame region and an experiment using a fluorescent tracerconfirmed this pattern of labeling.

Comments. The anterograde experiments clearlyshowed the existence of the two components of the occipito-mesencephalic tract (Table 1). The routes of the descend-ing tracts and the pattern of projections to the brainstem,spinal cord, and hypothalamus in the mallard appears tobe similar to that described in the pigeon (Zeier andKarten, 1971). The dorsal half of Ai appears to be thesource of projections to the reticular formation of thebrainstem and the source of projections to the medialspiriform nucleus, a relay to the cerebellum (Kartenand Finger, 1976). Subnuclei projecting to specific parts ofthe reticular formation could not be recognized. Therewas a tendency for the medial Ai to project to more ventralparts and for the lateral Ai to project to more dorsal

parts of the reticular formation. However, there wasno strict segregation of the cell populations in Ai. Theintermediate Ai was the source of projections to the tectumand n. intercollicularis; the injections in the latter cellarea may interrupt fibers running to the tectum. Theventral Ai and Ap sent fibers to the hypothalamus but alsocontributed fibers to the TOM proper projecting to morerostral, i.e., mesencephalic, parts of the reticular forma-tion. No cells in these parts of the archistriatum werefound in retrograde experiments after injections aroundthe motor nuclei of nervus trigeminus or at more caudallevels.

The caudal part of the Am was continuous with themedial Ap; the rostrodorsal part contained labeled cellsonly after injections into the parvocellular reticular regionand thus appears to be part of Ai. Based on these experi-ments, the dorsal Ai can be considered the sensorimotorcomponent of the archistriatum, and the ventral Ai 1 Apincluding the (ventral) Am are the amygdaloid part. The

Fig. 10. Distribution of labeled cells after a diamino-yellow dihydrochloride injection in HA-HD-HV(open circle) and a Fast Blue injection in the central LPO (filled circle). A small number of double-labeledcells (plus sign) was observed. Experiment F30.


most rostral parts of archistriatum (Ad and Av) contrib-uted very few fibers to TOM.

DISCUSSION

Comments on techniques

In this study, autoradiography after injections of [3H]-leucine was used for anterograde tracing; this methodreveals a clear pattern of the distribution of the main fibersystems. The disadvantage of this method, however, is thedifficulty of distinguishing labeled fibers from terminals insome areas. For this reason, Fink-Heimer material wasused to verify the trajectory of the fibers, in particular ofthe descending system. The archistriatum is favorablypositioned for this procedure because it can be approachedlaterally, with little damage to surrounding structures. Inwell-stained Fink-Heimer preparations, small fascicles inthe brainstem can be followed to their terminal fields. Thecombined use of the two anterograde methods does providean overall picture of the distribution of the archistriatalefferents, which can be used to select sites for retrogradeinjections. These injections not only confirm the results ofthe anterograde experimen but also permit one to ascer-tain the origin of projections to specific targets. The use ofiontophoresis enables the delivery of small amounts oftracer in specific terminal fields. Figure 18 summarizesthe results of a number of retrograde experiments.

Alternatively, we could have used other anterogradetracers, making small injections in different parts of thearchistriatum. However, Phaseolus-agglutinin never pro-vided satisfactory results in the mallard. Recently, we usedBDA with good results. But with many retrograde experi-ments already completed, we decided not to apply it to thearchistriatum. Applying biotinylated dextran amine in thepresent experiment would have required the death of

many more animals without improving our data signifi-cantly.

Intratelencephalic connections

Thus far, no exhaustive study of intratelencephalicarchistriatal connections is available. The studies of Zeierand Karten (1971, 1973) are still the most importantsources for comparison. These authors transected theanterior commissure and analyzed the resulting pattern ofdegeneration by using the Fink-Heimer method. Retro-grade tracing methods that might have provided specificinformation about the origins of these projections werelargely unavailable at the time. Our data show that thearchistriatum is an important source of commissuralfibers. Like Zeier and Karten (1973), we found a medialand a lateral stream of labeled fibers in the contralateralhemisphere. The lateral stream (their pars temporalis)follows the dorsoarchistriatal tract to caudal parts of theneostriatum and hyperstriatum ventrale (a few fibers).More rostrally, fibers traverse the neostriatum and HV toreach a region in the Wulst that may correspond to the HISof the pigeon. The medial stream passes the lateral LPOand medial parts of the N and HV, again to reach HIS. Thetwo fiber systems contribute projections to parts of thelateral LPO and paleostriatal complex and to the dorsome-dial part of the rostral archistriatum. In addition, parts ofthe caudal neostriatum, hyperstriatum ventrale, and HISreceive afferents through these two pathways.

The pattern of ipsilateral projections in the mallard islargely similar to the contralateral one but generallyexhibits a higher density of the silver grains over thecorresponding areas. In contrast to Zeier and Karten(1973), we found no projection to n. basalis, but labeledfibers were sometimes seen following the lamina medul-laris dorsalis. The PA receives a dense projection alsorecognized in the pigeon (Veenman et al., 1995). A projec-tion to the medial intermediate HV, described in thechicken (Bradley et al., 1985), was not found in our mate-rial. In the pigeon, a well-delineated terminal field hasbeen reported rostrally in the intermediate HV after inter-ruption of the anterior commissure (Zeier and Karten,1973). The HRP injections restricted to hyperstriatumaccessorium do not label archistriatal cells. After a[3H]-leucine injection in the most medial part of thearchistriatum (A), ipsilateral projections to the ventrome-dial part of LPO and lateral septum were found. Ourretrograde experiments, however, indicate that this part ofA is a source of projections to LPO, whereas septalafferents appear to derive from the caudolateral zone.Projections to the commissural area, ventral to the sep-tum, have their origin in the ventral half of the rostralarchistriatum.

Our HRP experiments show that the dorsal anteriorarchistriatum (Ad) is a source of projections to the contra-lateral archistriatum, whereas the ventral anterior archi-striatum (Av) is a source of projections to the region dorsalto the commissura anterior (CA). The dorsal portions of theanterior and intermediate archistriatum send projectionsto the contralateral neostriatum and hyperstriatal re-gions. The dorsal and ventral Ai and the dorsal part of Apsend projections to the ipsilateral neostriatum and hyper-striatal regions. The ventral portions of Ai and Ap aresources of projections to LPO. The ventrolateral zones of Aiand Ap are sources of projections to the region ventral ofthe septum. This subseptal region appears to correspond

TABLE IA. Overview of Intratelencephalic Archistriatal Projections AsFound in This Study

Ad Av Ai(d) Ai(i) Ai(v) AM/AP AP(l)

N (r) a, l, r, f a1 (r)HV a, r a fHIS/HD r f a, r, f a f r, fLPO (r) r a, rPA/INP a, r aacc a*, l, r a, l, rA (cl) a, l, r a a

a: anterograde (autoradiography), a* (WGA-HRP); l: anterograde (Fink-Heimer prepa-ration); r: retrograde (HRP, HRP-WGA); (r): occasionally labeled cells; f: retrograde(fluorescent tracer); (d), (i), (l), (v): dorsal, intermediate, lateral, ventral part; 1[3H]-leucine injections extend into intermediate Ai. See text for numbers of experiments, andabbreviations.

TABLE IB. Overview of Descending Archistriatal Projections Found inThis Study

Ad Av Ai(d) Ai(i) Ai(v) AM/AP AP(l)

Hy r, f a, r, fDIP/DLP a a1

PPC a aSpM a, l, r aICo a, l, r a, (r) r (r)tectum a a, l, rFRM a, l aparabr. r, f rLoC a aRPc a, l, r, f aSTr a, l, r aCMOD a, l, r anTTD a, l a

1See Table IA for abbreviations.


to part of the nucleus accumbens in the pigeon (Karten andHodos, 1967) and thus may be part of the paleostriatalcomplex. Szekely et al. (1994) found labeled cells in Ap ofthe chicken after HRP injections into the nucleus accum-bens but not after injections into the lateral septum. Bonsand Oliver (1986) described a projection to LPO from theventral archistriatum and n. teniae in the quail. Theseobservations support our assumption that the subseptalarea corresponds to (part of) the nucleus accumbens.

However, there is a large overlap of the sources of thevarious projections in the mallard, and no well-delineatedsources of specific projections can be recognized (Fig. 18).

Descending projections

In their study on the extratelencephalic connections ofthe archistriatum in the pigeon, Zeier and Karten (1971)distinguished a TOM, i.e., the occipitomesencephalic tract,and a HOM, i.e., the hypothalamic branch of TOM. The

Fig. 11. Distribution of silver deposits in diencephalon and mesencephalon after a [3H]-leucineinjection into the intermediate archistriatum. Same experiment as depicted in Figure 3.


Fig. 12. Distribution of silver deposits in the caudal half of the brainstem; same experiment asdepicted in Figures 3 and 11.


HOM was assumed to have its origin in the Am and Ap;together, these formed the amygdaloid part of the archi-striatum. There is also electrophysiological evidence forthis connection (Schriber, 1978). These two fiber systemsalso can be recognized in the mallard. However, only arelatively small part of the archistriatum, mainly thedorsal half of Ai, is the source of TOM and thus representsthe ‘‘sensorimotor area.’’ The distribution of the efferents ofthe dorsal Ai is broadly comparable to that described in thepigeon (Zeier and Karten, 1971). The most prominentterminal fields are in the n. dorsointermedius and n.dorsolateralis posterior thalami, n. subrotundus, the me-dial spiriform nucleus, medial and lateral mesencephalicreticular formation, n. precommissuralis principalis, thedeep tectal layers, n. intercollicularis, locus ceruleus andsubcerulean nucleus, the area intertrigeminalis, parvocel-lular reticular formation (dense in the dorsolateral butlighter in the ventromedial zone) and its caudal continua-tion CMOD, the subtrigeminal nucleus (bilaterally), andthe subnuclei of tractus descendens nervi trigemini (TTD).No termination was found in the motor nuclei of the

trigeminal and facial nerves (Arends and Dubbeldam,1982). Perhaps a few terminals occur in n. intermedius,the dorsal motor nucleus of the hypoglossal nerve. In songbirds, pars tracheosyringealis of this motor center receivesa direct archistriatal projection that has its origin in aspecific region, nucleus robustus archistriatalis (Vicario,1991). This region is also the source of a projection to aspecific cell group (n. dorsomedialis) in nucleus intercol-licularis (Wild, 1993). Such a n. robustus has not beenrecognized in the mallard.

A ‘‘limbic’’ component appears to descend with the TOM,which is not entirely unexpected because amygdaloidprojections to the brainstem reticular formation also havebeen described in mammals (e.g., Hopkins, 1975). Theparabrachial region appears to be a terminal field of thiscomponent. In the rat, an indirect amygdaloid pathway tothe trigeminal motor nucleus passes through the pontinereticular formation (Takeuchi et al., 1988). In birds, too,this part of the reticular formation sends fibers to thetrigeminal motor nuclei; thus, a comparable situation mayexist between birds and mammals.

Fig. 13. Location of the various lesions in the archistriatum causing degeneration of the extratelence-phalic projections. Numbers indicate the experiments.


Contralateral projections were found only in the me-dulla oblongata, more specifically in the subtrigeminalnucleus. The numbers of labeled cells in the contralateralAi always were modest; their distribution was similar tothat in the ipsilateral archistriatum. Cells projecting tothe dorsolateral zone of RPc were found predominantly inthe lateral part of the dorsal Ai; cells projecting to themedioventral zone often occupy a more medial position,but the two groups are not strictly separated.

In Varanus exanthemicus, projections pass from the‘‘basal ganglion’’ to the reticular formation (ten Donkelaarand de Boer-van Huizen, 1981). These authors concludedthat the striatum can influence the motor apparatus ofbrainstem and spinal cord through direct and indirectprojections. No separate equivalent of the avian archistria-tum has been recognized in reptiles. It is tempting toassume that projections, corresponding to the archistriatalprojections in birds, are included in these projections fromthe reptilian striatum. Further, the TOM may be compa-rable to the bundle of Bagley (Zecha, 1962; also see Cohenand Karten, 1974). This corticotegmental tract projects to

the dorsolateral part of the reticular formation and adja-cent nuclei of TTD from the level of the facial nucleibackward (Haartsen and Verhaart, 1967). It has no directprojections to the motor trigeminal nuclei and nucleusambiguus. A few fibers may join the lateral funiculus, butprojections to the external cuneate nucleus are absent.Probably, the bundle of Bagley does not really extend intothe spinal cord (Haartsen and Verhaart, 1967). Therefore,TOM resembles this bundle in several respects and shouldnot be compared with the pyramidal tract proper.

Subdivisions of archistriatum

Several criteria are available to distinguish subdivisionsin the archistriatum. One possibility is to use cell size andpacking density as a criterion. In a previous study in themallard, Dubbeldam and Visser (1987) used this criterionand distinguished an anterior part with a dorsal and aventral subdivision (Ad andAv, respectively), an intermedi-ate part (Ai), a medial part (Am), and a posterior part (Ap).The lateral zone of the archistriatum (lateral belt) ischaracterized by the presence of frontoarchistriatic fibers

Fig. 14. Distribution of labeled cells in the archistriatum after an HRP injection in n. centralismedullae oblongatae dorsalis (CMOD; black area in insert). Experiment HR329.


(Dubbeldam and Visser, 1987). The nucleus teniae is theonly part containing relatively small cells. Grossly, thesesubdivisions correspond to those described in the pigeon(Zeier and Karten, 1971) and have been applied in manyother studies. However, using the Golgi technique, Tomboland Davies (1994) were unable to distinguish such cellregions in the chick. In our Nissl-stained material, mostarchistriatum cells are quite large and round or polygonal;cells in the lateral belt are slightly darker and elongate,whereas cells in Av are polygonal, slightly smaller, andmore darkly stained than in the other parts (Dubbeldamand Visser, 1987). Other regional differences seem to bedue to differences in density of fibers and fascicles ratherthan to differences in cell appearance, which is particu-larly true for Am.

Histochemistry may offer another criterion for subdivi-sions. In the mallard, AChE activity was found in theventrolateral region of Ai 1 Ap (unpublished observation;Figs. 1, 2); this region does not correspond with one of thesubdivisions described earlier. The pattern of AChE activ-

ity in the paleostriatal complex of the mallard is compa-rable to that described in the pigeon (Parent and Olivier,1970); in that study, the possible presence of AChE activityin the archistriatum was not mentioned. Veenman andReiner (1994; also Veenman et al., 1994) distinguished alateral and anterior somatomotor and a medial and caudalvisceromotor component in the archistriatum of the pi-geon. The medial visceral part contains less gamma-aminobutyric acid (GABA)-ergic fibers and terminals andless cells positive for glutamic acid decarboxylase than thelateral somatic part (Veenman and Reiner, 1994); there isalso a difference in the density of GABAA receptors be-tween these medial (low density) and lateral (high density)regions (Veenman et al., 1994). These observations sup-port the bipartition of the archistriatum proposed by Zeierand Karten. Bailhache and Balthazart (1993) describedthe presence of dopamine b-hydroxylase and tyrosinehydroxylase immunoreactive elements in the n. teniae ofthe quail; the dorsal Ai also contains elements immunore-

Fig. 15. Distribution of labeled cells in the archistriatum after HRP injections in the dorsolateral(open circles) and ventromedial (filled circles) RPc, respectively. Black areas in insets indicate injectionsites; lower panel, dorsolateral RPc; upper panel, ventromedial RPc. Experiments HR105 and HR344.


active to tyrosine hydroxylase. Such data are not availablefor the mallard.

An important criterion in the present study is thepattern of afferent and efferent connections of the variousparts of archistriatum. In the mallard, the frontal andlateral neostriatum sends projections to Ad and to thedorsal half of Ai (Dubbeldam and Visser, 1987). This regionmay also receive ‘‘visual’’ input from the ectostriatumthrough relays in the neostriatum intermedium (Dubbel-dam and Visser, 1987). A comparable pattern of projectionshas been described in the pigeon (Ritchie, 1979: visualinput; Wild et al., 1985: trigeminal input). Auditory inputfrom field L reaches the ventromedial nucleus of Ai via thedorsal neostriatum caudolateral to field L (pigeon: Wild etal., 1993); a comparable projection to the rostromedialarchistriatum may exist in the budgerigar (Brauth andMcHale, 1988) and barn owl (Knudsen et al., 1995). In the

pigeon, the ventromedial Ai is the origin of a pathway withterminals surrounding the ovoidalis complex, the nucleusmesencephalicus lateralis pars dorsalis, and the nuclei ofthe lateral lemniscus (Wild et al., 1993). Because differentspecies were examined, the equivalency of the subdivisionswithin the archistriatum are difficult to resolve.

In the mallard, the most lateral zone of the (dorsal) Ai inthe mallard receives afferents from the ventral paleostria-tum, Am and Ap from the medial neostriatum, and themedial zone of the ventral Ai and Ap from the caudalneostriatum. The Ad is the main recipient of fibers fromthe contralateral archistriatum (Dubbeldam and Visser,1987; present study). By comparing these observationswith data on the pigeon (Zeier and Karten, 1971, 1973),several parallels can be recognized. First, the anteriorarchistriatum receives afferents from the contralateralhemisphere (CA input) and input via DA and tractus

Fig. 16. Distribution of labeled cells in the archistriatum after HRP injections in the parabrachialregion (filled circles) and tectum mesencephali (open circles), respectively. Black areas in insets indicateinjections sites. Experiments HR115 and HR368.


frontoarchistriaticus, and Ai receives input via DA. Sec-ond, sources of the ipsilateral input are Nf, the lateral partof Ni, and area temporo-parieto-occipitalis (TPO; Ritchie,1979). According to Wild et al. (1985), the trigeminal inputfrom n. basalis in the pigeon reaches the archistriatumdirectly via Nf and indirectly via part of the caudalneostriatum. Probably, the second pathway is the same asthe route from n. basalis via Nf and lateral Ni described inthe mallard (Dubbeldam and Visser, 1987). In the pigeon,AP receives input from the medial telencephalic wall(Zeier and Karten, 1973). The same may be true for Am.Csillag et al. (1994) described a specific projection from themedial intermediate HV (IMHV), a region involved in filialimprinting, to the ventral Ai and Ap. Thus far, a compa-rable connection has not been found in the mallard.

The results of the present study show that Ad is primar-ily a source of contralateral telencephalic projections,whereas the dorsal portion of Ai is the main source of TOM.This fiber system receives a modest ‘‘amygdaloid’’ contribu-tion from Am and Ap. Further, Am and the ventral Ap arethe sources of the HOM. This picture is comparable to that

in the pigeon (Zeier and Karten, 1971, 1973). Our datasuggest that the Am in the mallard is not a separateregion. The ventromedial region is continuous with Ap andcould be part of it. Its slightly different appearance may bedue to the presence of the many fascicles converging intothe occipitomesencephalic tract and anterior commissure.The same is true for the more rostral dorsomedial area(Fig. 2) that seems to be a medial continuation of Ad andnot a separate region. The cells sending projections todifferent destinations form no distinct subnuclei withinthe archistriatum. Distinct subnuclei, however, may existin other species. The n. robustus in certain species of songbirds (Oscines; e.g. Nottebohm et al., 1982) is a well-knownexample. It can be questioned whether this cell group is anewly formed center or merely a concentration of cells thatoccur more dispersed throughout a larger region withinthe archistriatum of other species (Dubbeldam, 1993).Efferents from n. robustus reach the subnucleus dorsome-dialis of nucleus intercollicularis (with a role in therespiration), nucleus hypoglossus, pars syringotrachealis(vocalization), and other centers that are involved in

Fig. 17. Distribution of labeled cells in archistriatum after an HRP-injection covering about the wholehypothalamus. Black area in inset indicates injection site. Experiment HR125.


respiration (Vicario, 1993; Wild, 1993). At least some ofthese projections exist in other groups of birds. Anotherexample of such a specialized center may be the ‘‘gazecenter’’ described in the barn owl (Knudsen et al., 1995).Our data suggest that the situation found in the mallard,and possibly in the pigeon, represent the primitive condi-tion, whereas the occurrence of specialized subnuclei is aderived character.

Functional considerations

The distinction of a sensorimotor part and an amygda-loid part in the archistriatum is primarily based onanatomical grounds, but it is supported by behavioralevidence. The medial and caudal parts of the archistria-tum are involved with aspects of fear and aggression asbased on lesion studies (e.g., Phillips, 1964; Martin et al.,1979: mallard; Ramirez and Delius, 1979: pigeon) andconditioning experiments (e.g., Cohen, 1975: pigeon). Bilat-eral interruption of the TOM causes a rise of plasma

corticosteroid levels (e.g., Martin et al., 1979). In mam-mals, the amygdala has an important role in the expres-sion of (conditioned) fear (e.g., discussion in Davis et al.,1994). In chickens, the amygdaloid part of the archistria-tum forms part of the system for filial imprinting (Lowndeset al., 1994). In an evoked potential study, Phillips (1966)showed that there is no multisensory but only visual inputto this part of the archistriatum. The existence of thisvisual input is confirmed by anatomical data in the pigeon(Ritchie, 1979). In contrast to the visual projection to thesensorimotor part of the archistriatum (via the lateralneostriatum), the input to the amygdalar part follows amore medial pathway (via the medial neostriatum cau-dale; Ritchie, 1979).

The sensorimotor part is a source of trigemino- andvisuomotor systems projecting to premotor regions intectum and brainstem. Karten and Shimizu (1989) empha-sized the parallel organization of the avian rotundo-ectostriatal-neostriatal-archistriatal pathway and the

Fig. 18. Map of the results of a number of different experiments showing that no distinct subnuclei canbe recognized in the archistriatum of the mallard. A, contralateral archistriatum; B, parabrachial region;C, commissural area; H, hypothalamus; L, LPO; N, contralateral neostriatum and HV; R, RPc; S, septalarea; T, ipsilateral neostriatum, HV, HIS; V, ventral LPO, n. accumbens.


mammalian pulvinar-visual cortex pathway, both project-ing to the tectum mesencephali. The archistriatal gazefield of the barn owl with its projections to the tectum(Knudsen et al., 1995) may represent a special case of thispathway. Dubbeldam and den Boer-Visser (1994) de-scribed a comparable wiring diagram for the trigeminalpathway, with projections to premotor centers of jaw andneck muscles in the parvocellular reticular formation ofthe brainstem (also see Tellegen and Dubbeldam, 1994). Insong birds, the n. robustus archistriatalis projects tovocalization and respiration motor centers. In the budgeri-gar, the vocalization system receives its input from theauditory part of n. basalis and is the so-called centralnucleus of the anterior archistriatum, the source of projec-tions to these motor centers (Striedter, 1994). Even thoughdistinct differences exist between the vocalization sys-tems, suggesting an independent evolution in song birdsand budgerigars, clear parallels can also be recognized. Inview of the similarities in organization, not only of thevocalization pathways in these two groups but also of thevisuomotor and trigeminomotor pathways in other birds,we suggest that the various sensorimotor circuits withinthe telencephalic region derived from the dorsal ventricu-lar ridge possess a basically similar pattern of organiza-tion. Each of the circuits begins in a telencephalic end-station of an ascending sensory system and ends, afterseveral relays in parts of the neostriatum, in the sensorimo-tor part of the archistriatum. Other projections from theseneostriatal relays reach the paleostriatum and/or lobusparolfactorius (see review in Dubbeldam, 1991). The recog-nition of a general pattern may help us to understandbetter the specializations in the various species of birds.

ACKNOWLEDGMENTS

We thank Dr. K. Kardong (Washington State University,Pullman) for his comments on a previous draft of ourmanuscript and Mr. Martin Brittijn for preparing thedrawings.

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