Rostral Wulst in passerine birds. I. Origin, course, and terminations of an avian pyramidal tract

Rostral Wulst in Passerine Birds.I. Origin, Course, and Terminations

of an Avian Pyramidal Tract

J.M. WILD* AND M.N. WILLIAMS

Department of Anatomy, School of Medicine and Health Science, University of Auckland,Auckland 92019, New Zealand

ABSTRACTAn avian ‘‘pyramidal tract’’ was defined in zebra finches and green finches by making

injections of neuronal tracers into the hyperstriatum accessorium (HA) of the rostral Wulst.Extratelencephalic projections of rostral HA traveled in the septomesencephalic tract (TSM)and gave rise to nuclear-specific terminal fields in the precerebellar medial spiriform nucleusof the posterior thalamus, the red nucleus in the mesencephalon, the medial pontine nucleusin the pons, and the subtrigeminal, external cuneate, cuneate, gracile, and inferior olivarynuclei in the medulla. Extensive but more diffuse terminal fields were also present in thestratum cellulare externum of the posterior hypothalamus, the central periaqueductal gray,the prerubral field, and the lateral and ventrolateral tegmentum of the pons and medulla.There was also a sparse projection to the dorsal thalamic nucleus intermedius ventralisanterior, which supplies the somatosensory input to the rostral Wulst, and distinct projectionsto the intercollicular region surrounding the central nucleus of the inferior colliculus, wherethey partly overlapped the projections of the dorsal column nuclei. Projections from HA to thecerebellum via the TSM are described separately. In the brainstem the ventral ramus of TSMwas situated ventral to the medial lemniscus at the base of the brain, entered the spinal cordin the inner margin of the lateral funiculus, predominantly ipsilaterally, and terminatedbilaterally but predominantly contralaterally in the medial part of the base of the dorsal hornof the upper six or seven cervical segments. After injections of tracers into putative targets,numerous retrogradely labeled cells were found in the rostral HA, predominantly ventrally.The results confirm the presence of a major descending fiber system in passerine birds thatresembles in its brainstem course and several of its terminations the pyramidal tract ofmammals. The reciprocal projections of HA with the hypothalamus suggest that rostral HAmay also incorporate neuronal components that in mammals would be considered parts ofprefrontal cortex. J. Comp. Neurol. 416:429–450, 2000. r 2000 Wiley-Liss, Inc.

Indexing terms: hyperstriatum accessorium; corticospinal tract; corticobulbar tract;

septomesencephalic tract; zebra finch

Although there is considerable variability in the origins,course, spinal extent and specific sites of termination ofthe pyramidal or corticospinal tract in different mamma-lian species, its ubiquitous presence is considered almost adefining characteristic of brain organization in the Class(Kuypers, 1981). Thus, nonmammalian vertebrates arenot generally thought to have a pyramidal tract, if for noother reason than that they do not have a laminatedneocortex from which such a tract could arise. In birds,however, a multilaminated elevation on the dorsum of thefrontal telencephalon, the Wulst, is often considered com-parable with parts of mammalian neocortex (e.g., Karten,1969; Nauta and Karten, 1970; Karten and Shimizu,1989).

On the basis of its differential afferents and efferentsand its differential response to sensory stimuli, the Wulsthas been divided into two main regions, a large visual partlocated more caudally and a smaller somatosensory partthat extends to the rostral pole of the brain (Revzin, 1969;

Grant sponsor: Whitehall Foundation, Inc.; Grant number: R94RO7;Grant sponsor: National Institutes of Health; Grant number: R01NS29467–07.

*Correspondence to: J.M. Wild, Department of Anatomy, School ofMedicine, University of Auckland, Auckland 92019, New Zealand.E-mail: [email protected]

Received 9 February 1999; Revised 22 September 1999; Accepted 22September 1999

THE JOURNAL OF COMPARATIVE NEUROLOGY 416:429–450 (2000)

r 2000 WILEY-LISS, INC.

Delius and Bennetto, 1972; Karten et al., 1973; Karten etal., 1978; Wild, 1987; Wild, 1997; Funke, 1989a; Funke,1989b). The most superficial lamina of the Wulst is knownas the hyperstriatum accessorium (HA), which lies moremedially at rostral levels and more dorsally at caudallevels. HA is bordered laterally or ventrally, respectively,by a narrower, small-cell lamina called the intercalatedhyperstriatum accessorium (IHA), which at rostral levelsof the Wulst receives most of the terminations of theprincipal somatosensory nucleus of the dorsal thalamus(Wild, 1987; Wild, 1997; Funke, 1989b). HA has long beenknown to be the origin of the so-called septomesencephalictract (TSM), which is the major outflow from dorsal

regions of the rostral telencephalon (early studies re-viewed in Ariens-Kappers et al., 1960; see also Reiner andKarten, 1983). The dorsal ramus of this tract, which hasbeen thought to originate largely from visual regions of theWulst, projects on the optic tectum and visual nuclei of thethalamus and pretectum (Karten et al., 1973; Bagnoli etal., 1980; Miceli et al., 1987; Gunturkun et al., 1993), butits basal or ventral ramus passes further caudally, appar-ently to a variable extent in different species (Wallenberg,1906; Adamo, 1967; Dubbeldam, 1976). In an owl, Karten(1971) briefly reported a long descending tract that origi-nated in the Wulst and entered the upper cervical spinalcord. Likewise in psittacines, Kalischer’s (1905) tractus

Abbreviations

A archistriatumAn nucleus angularisAVT area ventralis TsaiBas nucleus basalisBO bulbus olfactoriusCA commissura anteriorCb cerebellumCbd tractus cerebellaris dorsalisCC canalis centralisCO chiasma opticumCP commissura posteriorCu nucleus cuneatusCuE nucleus cuneatus externusCS nucleus centralis superior (Bechterev)DCN dorsal column nuclei (Nuclei gracilis et cuneatus)df dorsal funiculusdh dorsal hornDIVA nucleus dorsalis intermedius ventralis anteriorDLM nucleus dorsolateralis anterior thalami, pars medialisDMA nucleus dorsomedialis, pars anteriorDSD ducussatio supraoptica, pars dorsalisDSV decussatio supraoptica, pars ventralisE ectostriatumEx nucleus externus (of the intercollicular complex)FLM fasciculus longitudinalis medialisFPL fasciculus prosencephali lateralisGCt substantia grisea centralisGLv nucleus geniculatus lateralis, pars ventralisHA hyperstriatum accessoriumHb nucleus habenularisHD hyperstriatum dorsaleHIP tractus habenulo-interpeduncularisHIS hyperstriatum intercalatus superiorHL nucleus habenularis lateralisHV hyperstriatum ventraleICc central nucleus of the inferior colliculus (a.k.a. nucleus mes-

encephalicus lateralis, pars dorsalis (MLd)ICo nucleus intercollicularisIO nucleus isthmo-opticusIHA hyperstriatum accessorium, pars intercalatusImc nucleus isthmi, pars magnocellularisIpc nucleus isthmi, pars parvocellularisLa nucleus laminarisL2 primary thalamorecipient lamina of auditory telencephalonLFM lamina frontalis supremaLFS lamina frontalis superiorLH lamina hyperstriaticalMAN lateral magnocellular nucleus of the anterior neostriatumLMD lamina medullaris dorsalisLoC locus ceruleusLPO lobus parolfactoriuslPS nucleus interstitio-pretecto-subpretectalisMC nucleus magnocellularis cochlearisML lemiscus medialisMLd nucleus mesencephalicus lateralis, pars dorsalis (a.k.a. cen-

tral nucleus of the inferior colliculus (ICc)MV nucleus motorius nervi trigemininBOR nucleus of the basal optic rootNC neostriatum caudaleNF neostriatum frontale

NI neostriatum intermediumnIII nucleus oculomotoriusNIII nervus oculomotoriusnIV nucleus trochlearisNV nervus trigeminusNVI nervus abducensNVII nervus facialisNVIII nervus vestibularisOI nucleus olivaris inferiorOM tractus occipitomesencephalicusOv nucleus ovoidalisPA paleostriatum augmentatumPBvl nucleus parabrachialis, pars ventrolateralisPL nucleus pontis lateralisPM nucleus pontis medialisPP paleostriatum primitivumPPC nucleus principalis precommissuralisPrV nucleus sensorius principalis nervi trigeminiPT nucleus pretectalisPyr Tr pyramidal tractQF tractus quintofrontalisR nucleus rapheRAm nucleus retroambigualisRPgc nucleus reticularis pontis caudalis, pars gigantocellularisRt nucleus rotundusRu nucleus ruberS nucleus tractus solitariusSCE stratum cellulare externumSCv nucleus subcoeruleus ventralisSP nucleus subpretectalisSpL nucleus spiriformis lateralisSpM nucleus spiriformis medialisSpMv nucleus spiriformis medialis, pars ventralisSRt nucleus subrotundusSSp nucleus supraspinalisST nucleus subtrigeminalisT nucleus tangentialisTIO tractus isthmo-opticusTpC nucleus tegmenti pedunculo-pontinus, pars compactaTSM tractus septo-mesencephalicusTSMd tractus septo-mesencephalicus, pars dorsalisTSMv tractus septo-mesencephalicus, pars ventralisTTD nucleus et tractus nervi trigeminiUva nucleus uvaeformisV ventriculusVc nucleus caudalis (of the trigeminal brainstem nuclear

complex)Vd nucleus motorius nervi trigemini, pars dorsalisVeD nucleus vestibularis descendensVeL nucleus vestibularis lateralisVeM nucleus vestibularis medialisvh ventral hornVS nucleus vestibularis superiorVIId nucleus facialis, pars dorsalisIX nucleus glossopharyngeus ventralisX area X (of the basal ganglia; Figs. 1, 2, and 14B,C)X nucleus motorius dorsalis nervi vagi (Figs. 3, 10, and 14M)XII nucleus nervi hypoglossiXIIts nucleus nervi hypoglossi, pars tracheosyringealis13 lamina 13 of the optic tectum

430 J.M. WILD AND M.N. WILLIAMS

‘‘cortico-septo-spinalis’’ and Zecha’s (1962) ‘‘pyramidal tract’’were both described as occupying a position at the base ofthe medulla corresponding to that of the pyramid inmammals and were observed to enter the upper cervicalspinal cord (Kalischer) or to terminate chiefly in the dorsalcolumn nulcei (Zecha). However, no study using retrogradetracing techniques has thus far confirmed a telencephalicorigin of any long descending tract that might enter thespinal cord in birds, including parrots (Cabot et al., 1982;Gross and Oppenheim, 1985; Webster and Steeves, 1988;Webster et al., 1990). This negative evidence and the lackof any detailed or comprehensive modern account of theprojections of the rostral Wulst in birds has apparentlycontributed to the general view, mentioned above, thatpallial projections to the spinal cord are present only inmammals (e.g., Nudo and Masterton, 1988).

In the present study, we investigated the possibility thatthe rostral HA was the origin of an avian pyramidal tractin two species of passerines. In both pigeons and owls,neurons in this part of the brain have been shown toproject at least as far as the red nucleus, a major target ofdescending projections arising in association with thecorticospinal (pyramidal) tract in mammals (Karten, 1971;Kuypers, 1981; Armand, 1982; Wild, 1987; Wild, 1992).The results of the present study confirmed the presence ofa long descending tract that terminated in the red nucleus,among many other targets, that partly occupied a positionat the base of the medulla, and that entered the cervicalspinal cord predominantly ipsilaterally, and terminatedpredominantly contralaterally at the base of the dorsalhorn.

MATERIALS AND METHODS

Twenty-five zebra finches (Taeniopygia guttata) andeight green finches (Carduelis chloris) served as subjects.Surgical procedures were approved by and performedaccording to the guidelines of the Animal Ethics Commit-tee of the University of Auckland. Each bird was anesthe-tized with an intramuscular injection of an equal partsmixture of ketamine (50 mg/kg) and xylazine (20 mg/kg)and placed in a Kopf stereotaxic apparatus with the headtilted down at 45° to the horizontal (Stokes et al., 1974).Some of the injections were used to define anterogradeprojections, whereas others were used to verify the originof these projections by retrograde transport. Some birdsreceived injections of different tracers into different nucleion opposite sides of the brain, either to juxtapose afferentand efferent projections or simply to maximize the yield ofdata per bird. All injections were made by using glassmicropipettes (outer diameter 10–30 µm) and with eitherair pressure delivered via a picospritzer (General Valve,Fairfield, NJ), or iontophoresis (4 µA positive current, 7seconds on, 7 seconds off for 15–30 minutes). Tracers usedwere biotinylated dextran amine (BDA; Molecular Probes,Eugene, OR; 10,000 molecular weight [MW], lysine fixable,10% in phosphate-buffered saline (PBS), pH 7.4, and 1–2%cholera toxin B-chain, either unconjugated (CTB; ListBiological Laboratories, Inc., Campbell, CA) or conjugatedto horseradish peroxidase (McIlhinney et al., 1988).

Unilateral injections were made into the V-shaped HA ofthe rostral Wulst in 6 green finches and 14 zebra finches.In three of the zebra finches the injections were placeddorsally in the lamina, one dorsolaterally, one in themiddle of the widest part of the ‘‘V’’, and one dorsomedially.

In the remainder, and in the green finches, the injectionswere made more ventrally at various locations in the apexof HA. Placement of the injections was guided by electro-physiological responses to somatosensory stimuli evokedlargely in IHA, the somatosensory thalamorecipient laminathat defines the ventrolateral boundary of HA at the mostrostral levels of the brain. Tungsten microelectrodes, insu-lated except at their tips (Frederick Haer, 3–5 MV), wereused to record multiunit activity and potentials evoked bysomatosensory stimuli applied to contralateral parts of thebody in the form of air puffs, feather tweaks, taps, etc.(Wild, 1987; Wild, 1989; Wild, 1992; Wild, 1995; Wild,1997). Neural responses were monitored oscillographicallyand over a loud speaker. After functional identification ofthe ventrolateral boundary of HA, the tungsten electrodewas replaced by a tracer-filled glass micropipette, andinjections of various sizes were made in different cases byusing one or more pipette penetrations. For large injec-tions, two or three penetrations were made in the mediolat-eral direction, and picospritzer deposits of tracer weremade at several depths in the dorsoventral direction. Forsmaller injections, a single pipette penetration was madeat a stipulated depth in HA, and the tracer was depositediontophoretically.

To verify the origin of the projections within HA and todetermine whether the projections to different targetsarose from the same or different locations within HA,injections of CTB were made into the dorsal column andexternal cuneate nuclei, and other regions of the dorsolat-eral medulla (n 5 4), the medial mesencephalon, includingthe red nucleus and prerubral field (n 5 2), the intercollicu-lar nucleus of the midbrain medial to the central nucleus ofthe inferior colliculus (ICo; n 5 2), the nucleus spiriformismedialis (SpM; n 5 4), and the stratum cellulare externum(SCE) of the hypothalamus (n 5 1). Placement of most ofthese injections was also guided electrophysiologically byrecording neural responses to somatosensory stimuli ei-ther in the nucleus itself (Wild, 1989, 1995, 1997) or, in thecase of SpM, in the suprajacent nucleus uvaeformis (Uva;Wild, 1994). The injection in the hypothalamus was madeat the rostrocaudal level of the auditory nucleus ovoidalis,which was physiologically identified by using 1-millisec-ond click stimuli delivered via a hollow ear bar.

Survival times varied from 2 to 7 days, depending on thetracer and intra-axonal transport times. Birds were deeplyanesthetized with an intramuscular injection of an over-dose of ketamine (50 mg/kg) and xylazine (20 mg/kg) andperfused though the heart with saline followed by 4%paraformaldehyde in 0.1 M phosphate buffer, pH 7.4.Brains were postfixed for 5–15 hours, removed from theskull, and equilibrated overnight in 30% sucrose in PBS,pH 7.4. Serial transverse or parasagittal sections from theentire brain were cut at 30 µm on a freezing microtome andcollected in four series. Spinal cord sections were cut eithertransversely or longitudinally from cervical, brachial, andlumbosacral regions. For immunohistochemistry, sectionswere pretreated with 50% methanol containing 3% H2O2and thoroughly washed in PBS. BDA was visualized byusing Streptavidin peroxidase conjugate (Molecular Probes,Inc.) 1:1,000 in PBS containing 0.4% Triton X-100 (1–2hours at room temperature), followed by 0.025% 3,38-diamino benzidine (DAB) and H2O2. CTB was visualizedby using a polyclonal antibody raised in goat (List Biologi-cal Laboratories) at a dilution of 1:30,000 for 15 hours at4°C, followed by a biotinylated rabbit anti-goat IgG second-

PYRAMIDAL TRACT IN PASSERINE BIRDS 431

ary antibody (Sigma Chemical Company, St. Louis, MO),1:500 for 1 hour at room temperature, Streptavidin peroxi-dase conjugate, 1:1,000; 1 hour at room temperature, andfinally DAB and H2O2. If BDA and CTB were injected inthe same bird, the reaction product of the former was firstcolored black by the addition of 0.002% CoCl2 to the DABmixture, whereas that of the latter was left brown with noadded CoCl2. CTB-HRP was visualized by using tetra-methyl benzidine, according to the method of Mesulam(1978).

At least one series of sections was counterstained witheither Cresyl Violet, Giemsa, or Neutral Red for theidentification of neuronal groups. Labeled structures werephotographed and/or drawn with the aid of a drawing tube,and these drawings were scanned into a Macintosh 7100/80PowerMac computer and redrawn and labeled by usingCanvas (Pica).

RESULTS

Efferent projections

In the three zebra finches that received a BDA injectionat a dorsal location in rostral HA, few labeled fibers werefound caudal to the diencephalon. In contrast, in all thecases that received injections of either BDA or CTB inmore ventral parts of rostral HA, the projections weremuch more extensive, and it is these that are describedbelow. Irrespective of their size, these more ventral injec-tions were largely confined to HA and IHA by the boundarycreated by the latter and by the lamina frontalis suprema,which forms the lateral border of IHA (Figs. 1–4). How-ever, in cases receiving large injections, a variable amountof spread of tracer from the ventrally and rostrally placedinjections extended dorsally and caudally into rostralparts of the visual Wulst. Consequently, in addition to thelabeling of rostral Wulst efferents, there was in these casessome labeling of efferents originating in the visual Wulst,which was indicated by the presence of terminal fields invisually related nuclei in the diencephalon and mesen-cephalon, e.g., the ventral lateral geniculate nucleus, someof the pretectal nuclei, the optic tectum (predominantlylaminae 13 and 4), and the dorsal cap of the nucleus of thebasal optic root. In cases receiving smaller injections inventral HA that did not encroach on the visual Wulst,these projections to visual nuclei, which have been welldescribed in other avian species (Adamo, 1967; Karten etal., 1973; Bravo and Pettigrew, 1981; Rio et al., 1983;Miceli et al., 1987; Casini et al., 1992), were not observed,and in the present report they will be further referred toonly in passing.

Efferent fibers collected in the lateral part of the septo-mesencephalic tract (TSM), which coursed down the me-dial aspect of the hemisphere. On entry to the diencepha-lon, the tract formed two rami, as previously described(e.g., Huber and Crosby, 1929; Rio et al., 1983). The dorsalramus (TSMd; Fig. 4) was located dorsal to the optic tractand dorsolateral to the rostral pole of the nucleus rotun-dus. Although not generally appreciated, it carries fibersdestined for nonvisual and visually related nuclei. Theventral ramus (TSMv; Fig. 4) was initially located on themedial side of the lateral forebrain bundle, but finallyemerged ventral to the quintofrontal tract to run caudallythrough the base of the hypothalamus (Fig. 1Ab). In thedorsal thalamus, sparse terminations were observed in thenucleus dorsalis intermedius ventralis anterior (DIVA),

which supplies the somatosensory projection to IHA of therostral Wulst (see Fig. 13d). These terminations weresupplied by fibers that entered DIVA from above, viaTSMd. Diffuse terminations were also observed in dorsalregions of the stratum cellulare externum (SCE) of theposterolateral hypothalamus, these terminations becom-ing more dense in the cell-poor region dorsal to the nucleusof the basal optic root (nBOR; Fig. 5). In the caudal dorsaldiencephalon, a dense terminal field was present in therostrodorsal parts of the medial spiriform nucleus (SpM;Figs. 1c; 6b; 7b,d). In passerifomes, these parts formmedial and lateral ‘‘wings,’’ the latter extending to thelateral roof of the diencephalon and being located immedi-ately ventral to rostral levels of the nucleus uvaeformis(Uva; Wild, 1994) (Fig. 7A). Labeled fibers were seen toaccess SpM from the overlying TSMd, but it is possiblethat some terminations were also supplied by dorsallydirected fibers of TSMv. Ventral and ventromedial to SpM,dense terminations were also present throughout thecaudal part of nucleus principalis precommissuralis, theprerubral field and the medial part of the mesencephalicreticular formation (Figs. 1c; 2b; 3b). In transverse sec-tions, labeled fibers were seen to extend medially fromSpM to the central periaqueductal gray (GCt), whichreceived a diffuse terminal field (Fig. 7c), and ventromedi-ally to the red nucleus (Ru), which received a denseprojection, particularly to its ventrolateral part (Figs. 3b,e;6c,d). Projections to this ventrolateral part extended ven-trally on the lateral aspect of the ventral area of Tsai, inwhich sparse terminations were also observed. Termina-tions in SpM, GCt, and Ru were predominantly ipsilateral,but sparse projections crossed the midline in the vicinity ofthe nucleus innervated to terminate in the homologousnucleus on the contralateral side.

Caudal to SpM a laterally directed contingent of fibersheaded into the intercollicular region where it surroundedthe central nucleus of the inferior colliculus (ICc, alsoknown as the nucleus mesencephalicus lateralis, parsdorsal or MLd; Fig. 8c). Terminations were apparent allaround the border of the ICc but were particularly denselateral to it, i.e., in the external nucleus of the IC (Ex), andmedial to ICc. As indicated in a green finch that receivedan injection of CTB into the dorsal column nuclei and aninjection of BDA in the contralateral rostral HA, the BDAlabeled projections here overlapped the mesencencephalicterminations of the medial lemniscus, particularly at themedial border of ICc (not shown). A few fibers crossed inthe posterior commissure to enter the contralateral inter-collicular region.

As TSM left the mesencephalon to enter the pons, part ofit formed a distinct tract at the base of the brain, ventral tothe medial lemniscus, which at these levels is beginning tosend fibers dorsolaterally toward the inferior colliculus(Wild, 1987; Wild, 1997; present study). This part of TSMcontinued in this sublemniscal position at the base of thebrain throughout the remainder of the pons and uppermedulla, but many other TSM fibers passed caudally inmore central and dorsal regions of the pontine and medul-lary tegmentum (Fig. 2A,c,d). Some fibers even swept upinto the brachium conjunctivum to enter the cerebellum,but because of the special and unusual nature of thisprojection, it will be further described in a separate report(Wild and Williams, unpublished observations). The ven-trally situated tract was largely the caudal continuation of


TSMv, but the more diffuse brainstem projections couldhave been derived from either or both rami.

At caudal mesencephalic and rostral pontine levels,there was an extensive and diffuse projection to theipsilateral ventrolateral tegmentum, including the lateralmesencephalic reticular formation, the subcoeruleus ven-tralis, and the region ventral to the trigeminal motornucleus (Figs. 8b,d; 9A). There were also distinct projec-tions to a region medial to the principal sensory trigeminalnucleus (PrV; Fig. 9b), but no significant terminationswere observed within this nucleus. Slightly more caudally,there was a discrete terminal field overlying cells embed-ded in the dorsal aspect of the exiting facial nerve (notshown). This field was not related to the large neurons ofthe lateral vestibular nucleus, which overlies the facial

and vestibular nerve roots, but to smaller neurons resem-bling those of the superior vestibular nucleus. Sparseterminations were also observed in the medial vestibularnucleus. Throughout the base of the pons, a localizedprojection was given off from the ventral ramus to thedorsal cap of the medial pontine nucleus (Figs. 3c; 9A,c),and in the base of the medulla terminations were observedin the ventral lamella of the inferior olivary nucleus (Fig.2A,c).

Many fibers that were not part of the discrete ventralramus at the base of the brain passed through lateral partsof the caudal pons and rostral medulla in a widely dis-persed and extensive array, and it was not possible toascertain their specific terminations with any certainty(Figs. 1d; 2c,d). However, there was a distinct projection to

Fig. 1. A: Schematic drawing of a parasagittal section through thezebra finch brain showing the general trajectory of the descendingprojections through the brainstem that resulted from the BDA injec-tion shown in rostral HA (black, with shading signifying spread fromthe injection center). The projections through the hypothalamus andbrainstem are shown as originating (in fact, leaving) the ventralaspect of TSM as solid lines; these end either in arrowheads, signifyingthe direction of the continuing trajectory, or in inverted open arrows,

signifying terminations. Boxes b, c, and d each enclose an area shownin the correspondingly labeled darkfield photomicrographs. TSMv isshown passing through the base of the hypothalamus in b; fibers andterminations, supplied by both TSMd and TSMv, are shown in c; andfibers passing through, and partially terminating in, the ventrolateralmedulla are shown in d. For abbreviations, see list. Scale bars 5 200µm.


the lateral part of the tegmentum, immediately ventral tothe descending tract of the trigeminal nerve. More cau-dally in the medulla, the projections to this subtrigeminalregion became much more pronounced, being fed by fibersleaving the ventral ramus (Fig. 10A,b). These fibers courseddorsally up the lateral aspect of the medulla, giving offterminations to the subtrigeminal region and to the exter-nal cuneate nucleus as they did so. They skirted the parscaudalis of the nucleus of the descending trigeminal tract,gave extensive terminations to the cuneate and gracilenuclei, particularly to their more ventral parts, and thencrossed though the commissura infima to terminate evenmore densely in all the same nuclei on the opposite side(Fig. 10). A few fibers left the ventral ramus and crossedthe midline through the base of the medulla to add theirprojections to the contralateral dorsal column and externalcuneate nuclei.

Fibers entered the cervical spinal cord to descend,predominantly ipsilaterally, in the medial aspect of thelateral funiculus and through the base of the dorsal horn ofboth sides (Figs. 3d; 11a). The greatest density of termina-

tions occurred contralateral to the HA injection in moremedial aspects of the base of the dorsal horn, althoughsome terminations were also apparent in the central partof the gray matter, dorsal to the central canal (Fig. 11b,c).Other fibers descended in ventral parts of the ipsilaterallateral funiculus (Fig. 11a,d) and gave rise to sparseterminations in the tip of the ventral horn on the sameside. Fibers could be followed to about the level of C6 or C7,and no fibers or terminations were observed within thebrachial or lumbosacral enlargements.

Retrograde confirmation of the specific sitesof origin of the HA projections

All injections in putative target nuclei resulted in retro-grade labeling of cells that were confined to rostral HA, butthere was no obvious indication of a topographic organiza-tion of the origins of the projections, i.e., cells labeled frominjections in different nuclei were intermixed in HA. Allinjections except those in the medulla labeled HA cellspredominantly ipsilaterally. The injections in the dorsaland lateral medulla labeled cells in deeper regions of

Fig. 2. See legend for Figure 1. A: A parasagittal drawing depictingthe descending projections at a more medial plane than that shown inFigure 1. The boxed areas (b and c) enclose areas shown in the

correspondingly labeled darkfield photomicrographs. d: Another ex-ample of widely distributed labeled fibers passing through the ventro-lateral rostral medulla. Scale bars 5 200 µm in b and d; 100 µm in c.


Fig. 3. See legend for Figure 1. A: A parasagittal drawing depictingthe descending projections in a plane closer to the midline than thatshown in Figure 2. The dashed line terminating in DCN signifiesprojections that have a substantial crossed component to the dorsalcolumn nuclei. Boxes b, c, and d enclose areas are shown in correspond-ingly labeled photomicrographs; b and c are darkfield; d is brightfield;

b has been retouched at left to remove artifact. e: Brightfield photo-micrograph showing BDA labeled fibers and terminations in the rednucleus in a sagittal plane medial to that shown in b, which is at thelateral edge of the nucleus and includes part of the prerubral field. Forabbreviations, see list. Scale bars 5 200 µm in b and c; 100 µm in dand e.


rostral HA, with a slight contralateral predominance (Fig.12A). That the injections included the dorsal column andexternal cuneate nuclei was indicated by the fact thatmedial lemniscus was anterogradely labeled (Wild, 1997).Medial mesencephalic injections retrogradely labeled cellsthroughout rostral HA and cells in the deep cerebellar anddorsal column nuclei that project to the red nucleus (Wild,1989; Wild, 1992; Arends and Zeigler, 1991). The injections

in SpM were centered on the nucleus, as indicated byextensive anterograde labeling of the mossy fiber projec-tion to the cerebellum (Karten and Finger, 1976; Wild,1992), but none of them were confined to the nucleus, eachhaving some involvement of the adjacent pretectal nuclei.Retrogradely labeled cells were distributed throughout theentire dorsoventral extent of HA, but they did not extendto the most lateral part of the lamina (Fig. 12B). The

Fig. 4. A: Schematic frontal hemisection through the zebra finchbrain at the level of the rostral diencephalon depicting the dorsal(TSMd) and ventral (TSMv) branches of the septomesencephalic tract(short wavy lines) in relation to the lateral forebrain bundle (FPL) andquintofrontal tract (QF). The labeling was produced by injections of

BDA in rostral HA such as are shown schematically in the smallerscale superimposed figure a (solid black indicates the centers of twoinjections; hatched indicates spread from these injections). b: Dark-field photomicrograph of the projections in the region corresponding tothe boxed area in A. For abbreviations, see list. Scale bar 5 200 µm.

Fig. 5. A: Schematic frontal hemisection through the diencephalonof a zebra finch brain, depicting fiber and terminal labeling (shortwavy lines) in the caudal hypothalamus (SCE) resulting from a smalliontophoretic injection of BDA in the ipsilateral HA, such as is shownin the smaller scale superimposed schematic hemisection in a. In a,which is at a level close to the rostral pole of the brain, the injection

center is indicated as solid black, surrounded by spread, indicated byhatching. Small black dots indicate cells retrogradely labeled from theinjection. Part of the hypothalamic labeling is shown in the darkfieldphotomicrograph in b, which corresponds to the boxed area in A. Forabbreviations, see list. Scale bars 5 1 mm for the schematics; 200 µmin b.


injection in the hypothalamus labeled many neuronsthroughout rostral HA, some of them contralaterally,although they were concentrated in more ventral regionsof the lamina (Fig. 12C). Because of the proximity of theinjection to fascicles of TSMv, however, uptake by fibers ofpassage cannot be ruled out in this case. The injection inICo depicted in Figure 12E was centered at a somatosen-sory locus medial to ICc and labeled neurons in deepregions of rostral HA (Figs. 12D, 13a). It also produced thefollowing pattern of retrograde labeling that is typical ofinjections located anywhere in the shell of neurons sur-rounding ICc (MLd). Labeled neurons were distributedthroughout this shell bilaterally, indicating extensive inter-connections between its various parts (Fig. 12E). Retro-gradely labeled neurons were also present in the dorsalcolumn nuclei (Fig. 10f), medial lamina V of the upper fewcervical spinal segments (see Wild, 1995), the caudomedialpart of the paleostriatum primitivum (Fig. 13b; see alsoWild et al., 1993), the medial and lateral hypothalamus,and a region that surrounds the robust nucleus of thearchistriatum (Fig. 13c). The ICo injection also produced ashell of anterograde labeling around the thalamic auditorynucleus ovoidalis, bilaterally but predominantly ipsilater-

ally (Fig. 13d). The relation of this labeling to cells in DIVAthat were retrogradely labeled by an injection of BDA inthe rostral HA of the same case is also shown in Figure13d.

Retrogradely labeled cells resultingfrom HA injections

Several groups of intratelencephalic and extratelence-phalic neurons were labeled as a result of the HA injec-tions, but only the latter are noted here. One was thenucleus dorsalis intermedius ventralis anterior (DIVA),the principal somatosensory nucleus of the dorsal thala-mus (Fig. 13d; see also Wild, 1987; Wild, 1997). DIVA waslabeled predominantly ipsilaterally, but a few labeledDIVA neurons were located slightly more rostrally on thecontralateral side. Other retrogradely labeled cells werelocated in 1) nucleus subrotundus, a nucleus that appearsto have projections to widespread regions of the telencepha-lon; 2) the same part of the stratum cellulare externum(SCE) of the hypothalamus that received the anterogradeprojections from HA; 3) the base of the ipsilateral pontinetegmentum, just dorsal to the descending ventral ramus;and 4) the medial edge of the red nucleus. Nothing is

Fig. 6. A: Schematic frontal hemisection through the diencephalic-mesencephalic border region of a zebra finch. b: Area corresponding tobox b in A is brightfield photomicrograph showing BDA terminallabeling in the most rostrodorsal part of SpM. c: Area corresponding tobox c in A is BDA fiber and terminal labeling in the red nucleus, alongwith cell bodies retrogradely labeled by an injection of CTB into the

cerebellar cortex (cf Wild, 1992). d: Fiber and terminal labeling in thered nucleus of a green finch after an injection of CTB into theipsilateral rostral HA. Note also the sparse labeling in the contralat-eral red nucleus. For abbreviations, see list. Scale bars 5 200 µm in band c; 100 µm in d.


known about the last two projections. In cases with largeinjections, a few lightly labeled neurons were also found inthe nucleus dorsolateralis anterior thalami, pars lateralis,which projects to the visual Wulst (e.g., Karten et al., 1973;Nixdorf and Bischoff, 1982).

DISCUSSION

Long descending projections that reach at least as far asthe upper cervical spinal cord have been reported tooriginate from two regions of the avian telencephalon(Kalischer, 1905; Zecha, 1962; Karten, 1971; Zeier andKarten, 1971; Dubbeldam et al., 1997). One is the archis-triatum, the outflow from which via the occipitomesence-phalic tract in the dorsolateral tegmentum is said toresemble Bagley’s corticotegmental tract or bundle inungulates (Bagley, 1922; Haarsten and Verhaart, 1967).The other is the subject of the present study, namely, thehyperstriatum accessorium (HA), the projections of whichthrough the ventral brainstem were suggested by Ka-lischer (1905) and Zecha (1962) to be akin to the pyramidaltract of mammals. This suggestion is strongly reinforcedby the present results, summarized in Figure 14, which

demonstate a striking resemblance between the extratelen-cephalic projections of the rostral Wulst in finches and thepyramidal or corticospinal tract of mammals. Of course,birds do not possess a pyramidal shaped structure at thebase of the medulla, and although they may have neuronsin HA that are the equivalent of neurons in layer V–VI ofmammalian isocortex, in the sense that they project tothalamus, brainstem, and spinal cord, they are not pyrami-dal in shape. Strictly speaking, therefore, the term ‘‘pyra-midal tract’’ is not an appropriate designation for the basalor ventral branch of TSM. Nevertheless, the concept of apyramidal tract in mammals was for centuries less con-cerned with the cell types of origin, or their laminarlocation, than with the origins of the tract in the cerebralcortex, its partial decussation at the spinomedullary junc-tion, and its involvement in the contralateral clinicalmanifestations of various brain lesions (Armand, 1982).The present study has corroborated Zecha’s (1962) claimthat a long pyramidal-like tract originates in the dorsaltelencephalon of birds and follows a trajectory through thebrainstem like that of mammals, with predominantlycontralateral terminations in the dorsal column nuclei. Italso confirms Kalischer’s (1905) and Karten’s (1971) find-

Fig. 7. A: Schematic frontal hemisection through the diencephalic-mesencephalic border region in a zebra finch, caudal to the level shownin Figure 6. b: Area corresponding to box b in A is brightfieldphotomicrograph showing BDA fiber and terminal labeling in thedorsal part of SpM in relation to cell bodies retrogradely labeled by aninjection of CTB into the cerebellar cortex. Note that all parts of SpMproject to the cerebellum, but that HA projects only to the rostrodorsal

part of SpM. d: Dense terminal labeling in the medial wing of thedorsal part of SpM after an injection of CTB into the rostral HA of agreen finch. Note the absence of label in the ventral part of SpM(SpMv). c: Diffuse labeling in the central periaqueductal gray after aninjection of CTB into the rostral HA of a green finch. For abbreviations,see list. Scale bars 5 100 µm in b and c; 200 µm in d.


ings in the parrot and owl, respectively, that the tractoriginates in the rostral part of the Wulst and that itactually enters the spinal cord; in fact, in the two species ofpasserines studied here, we have shown that it projects atleast as far as C7. But, unlike the case for the owl, theprojections in the finches did not for the most part decus-sate at the bulbospinal junction, but descended largelyipsilaterally in the inner margin of the lateral funiculus,rather than the dorsal funiculus, as in the owl, beforeterminating predominantly contralaterally.

Species differences in the presence or absence of apyramidal decussation, funicular trajectory, and rostrocau-dal extent are also a feature of the mammalian pyramidalor corticospinal tract (Kuypers, 1981; Palmieri et al.,1993). As in finches, there is little or no pyramidal decussa-tion in the hedgehog, mole, klipdassie, or procavia, but inthese mammalian species the corticospinal tract travels inthe ventral funiculus. The pyramidal tract in finchesresembles that in the so-called primitive group of mam-mals, such as hedgehog, rabbit, goat, sloth, armadillo, andelephant, in terminating at relatively high spinal levelsand predominantly in the base of the dorsal horn (Ver-haart, 1967; Kuypers, 1981; Palmieri et al., 1993). Moregenerally, however, the predominantly contralateral termi-nation of the pyramidal tract in finches resembles that in

most mammals, including the uncrossed component of thepyramidal tract in primates, which also crosses beforeterminating (Kuypers, 1981; Schoenen and Grant, 1990).

Also like the mammalian pyramidal tract, most of theindividual fibers of the comparable tract in birds appear tobe rather thin; moreover, their pattern of termination atbrainstem levels is distinctly mammalian-like. As in mam-mals, these terminations can be grouped into those relatedto cells of origin of descending brainstem pathways, thoserelated to cerebellar relay nuclei, and those related torelay nuclei of ascending sensory systems (Armand, 1982).

Relation to cells of origin of descendingbrainstem pathways

The first group is largely related to the red nucleus, aspreviously noted by Karten (1971) in an owl and by Wild(1992) in pigeons. The red nucleus in birds projects to alllevels of the spinal cord (Wild et al., 1979; Cabot et al.,1982: Webster and Steeves, 1988; Webster et al., 1990),predominantly contralaterally, so that, even though HAdoes not appear to project beyond midcervical levels, itsinfluence may be relayed to all spinal levels via theHA-rubrospinal pathway. What kind of influence thismight be is currently unknown, partly because there is noinformation on the role of the red nucleus in birds in either

Fig. 8. A: Schematic frontal hemisection through the mesencepha-lon and upper pons of a zebra finch. b: Area corresponding to the box bin A, retouched in several places to remove artifact is BDA fiber andterminal labeling in the ventrolateral tegmentum. c: Area correspond-ing to box c in A is BDA fiber and terminal labeling in parts of the

intercollicualr nucleus surrounding the central nucleus of the inferiorcolliculus (ICC, a.k.a. MLd). d: BDA fiber and terminal labeling in theregion of the nucleus subcoeruleus ventralis (SCv), at a level slightlycaudal to that shown in A. b–d are darkfield photomicrographs. Forabbreviations, see list. Scale bars 5 200 µm.


motor or sensory functions. The predominant locus oftermination of rubrospinal fibers in the base of the dorsalhorn and intermediate area in pigeons (Wild et al., 1979)might suggest a role in either the control of sensory inputand/or the modulation of spinal refex circuitry via spinalinterneurons, rather than one concerned directly withmotor control. It is also not known whether, as in mam-mals, some of the fibers projecting to the red nucleus fromHA are collaterals of those projecting to the spinal cord.

Other HA projections to cells of origin of descendingbrainstem pathways may involve various groups of rhomb-encephalic neurons. In the upper pons, the diffuse projec-tion of the HA to the ventrolateral tegmentum is likely toinclude neurons of nucleus subcoeruleus ventralis, whichin other avian species has been shown to be a significantsource of descending projections to the cord (Cabot et al.,1982; Webster and Steeves, 1988). Other pontine andmedullary reticulospinal neurons may also be targeted by HAprojections, but until double retrograde-anterograde labelingstudies are performed, this must remain speculative.

Relation to cerebellar relay nuclei

The medial spiriform nucleus (SpM) in the caudalthalamus is by far the most prominent nucleus in thiscategory, with an extremely dense pattern of terminationsin the dorsal and rostral parts of this nucleus. The ventralpart of SpM, or at least part of it, receives an equally denseprojection from the major telencephalic outflow of thecaudal hemisphere, namely the archistriatum (Zeier andKarten, 1971; Wild, 1992; Wild and Farabaugh, 1996). Allparts of SpM provide the cerebellum with extensive mossyfiber projections (Karten and Finger, 1976; Wild, 1992;present study). A homologue of this nucleus in mammals isunknown.

The red nucleus may also relay HA projections to thecerebellum, for in birds, and possibly in some reptiles,there is a rubrocerebellar projection to both the deep nucleiand cortex (see Fig. 8c; Wild, 1992; Kunzle, 1983). HA alsoprojects to two other precerebellar relay nuclei, namely themedial pontine nucleus (PM) and the inferior olive (Wild,1992; present study). In birds, PM is a compact nucleus in

Fig. 9. A: Schematic frontal section through the pons of a zebrafinch, depicting the distribution of BDA labeled fibers (short wavylines), largely on the side ipsilateral to the injection in rostral HA.b: Area corresponding to box b in A is darkfield photomicrographshowing BDA labeled fibers and terminations in the dorsolateraltegmentum, medial to PrV. Note also the fibers that head toward the

cerebellum (Wild and Williams, unpublished observations). c: Areacorrespnding to box c in A is brightfield photomicrograph showingterminal labeling in the dorsal cap of the medial pontine nucleus afteran injection of CTB into the ipsilateral rostral HA in a green finch. Forabbreviations, see list. Scale bars 5 200 µm in b; 100 µm in c.


Fig. 10. A: Drawing of a frontal section through the medulla of azebra finch, at a level just caudal to the obex. Arrows indicate thedirection of fibers leaving the pyramidal tract (hatched) in the base ofthe medulla and crossing to the contralateral side through thecommissura infima of the dorsal medulla. b: area corresponding to boxb in A is darkfield photomicrograph showing BDA labeled fibers in thepyramidal tract (PyTr). c,d: Darkfield photomicrographs showingBDA labeled fibers and terminations in the regions enclosed by the

boxes c and d in A. e: Brightfield photomicrograph showing terminallabeling in the left cuneate nucleus of a green finch after an injecton ofCTB into the right rostral HA. f: Brightfield photomicrograph showingBDA fiber and terminal labeling in the ventral aspect of the rightdorsal column nuclei of a zebra finch, in relation to cell bodiesretrogradely labeled by an injection of CTB into the contralateral ICo(see Fig. 12E). For abbreviations, see list. Scale bars 5 200 µm in b–e;100 µm in f.


the base of the pontine tegmentum and resembles thepontine nuclei of mammals in its projections to the cerebel-lum via the contralateral brachium pontis (Brodal et al.,1950). However, although not specifically identified asnuclei, there are in birds many other neurons scatteredthroughout the pontine tegmentum that project to thecerebellum (present and unpublished results), but whetherany of these also receive a projection from HA will have tobe determined in future studies. The HA projection to theinferior olive is to the same part, the lateral part of theventral lamella, that receives a projection from the dorsalcolumn nuclei (Arends et al., 1984; Wild, 1989). Somatosen-sory/somatomotor information in thereby routed to thecerebellum via three separate systems: the climbing fibersystem via the olive, the mossy fiber system via SpM andPM, and the ‘‘multilayer’’ fiber system (Haines et al., 1986)via a direct projection from HA to the cerebellar cortex anddeep nuclei (Wild and Williams, unpublished observa-tions).

Relation to sensory relay nuclei

The major nuclei in this category are the dorsal columnand external cuneate nuclei in the caudal medulla, possi-bly certain cells in the cervical spinal cord, but not the

sensory trigeminal nuclei. Whether the subtrigeminalregion, which received the densest termination of projec-tions to the caudolateral medulla, may also have a role as asensory relay is not clear because the specific projections ofthis region have not been well defined. Generally, however,the HA projections to lateral and dorsal regions of thecaudal medulla and to the cervical spinal cord seem likelyto be primarily concerned with the control of somatosen-sory input arising in the body, and to some extent the beak,the latter because of the trigeminal projections to theexternal cuneate nucleus in birds (Dubbeldam and Karten,1978; Wild and Zeigler, 1996). In birds, this nucleus isprobably not homologous with its mammalian namesake,in that it is not exclusively concerned with upper limbproprioception, but receives primary spinal and trigeminalafferent projections mediating cutaneous and deep sensa-tion, rather than muscle spindle inputs (Van den Akker,1970; Wild, 1985; Dubbeldam and Karten, 1978; Wild andZeigler, 1996; Reinke and Necker, 1996). Regarding apossible cervical spinal relay, in both pigeons and passe-rines primary afferent projections from the wing have beenshown to terminate specifically in medial lamina V at thebase of the dorsal horn in all cervical segments rostral tothe brachial enlargement (Wild, 1985; Wild, 1997; Schulte

Fig. 11. a: Darkfield photomicrograph showing BDA labeled fibersand terminations in the upper cervical spinal cord of a zebra finch.Most labeled fibers are located on the right, ipsilateral to the HAinjection, and occupy the inner margin of the lateral funiculus. Notealso the fibers around the lateral aspect of the ventral horn. Theterminations are concentrated in the base of the dorsal horn, predomi-

nantly contralateral to the HA injection. These are shown at higherpower in the darkfield photomicrograph b (the arrow marks themidline), and in c, which is a brightfield photomicrograph of a nisslcounterstained section through the level of C3. d: Darkfield photomi-crograph showing the spinal projections at the level of C4. Forabbreviations, see list. Scale bars 5 200 µm in a; 100 µm in b–d.


and Necker, 1994), and cells in this general location atupper cervical levels, along with those from the dorsalcolumn and external cuneate nuclei, project to somatosen-sory regions of the mesencephalon and thalamus (Wild,1995; Wild, 1997; present study). In fact, Wild (1995)suggested that the spinal neurons in medial lamina V mayactually comprise a caudal extension of the dorsal columnnuclei (but see Schulte and Necker, 1994 for an alternativeinterpretation). In the present study, the HA projections tothe cervical cord, whether they descended in the lateralfuniculus or through the base of the dorsal horn, termi-nated predominantly in the vicinity of medial lamina V,bilaterally but predominantly contralaterally and, hence,

may be part of the same descending system for the controlof sensory input derived mainly from the contralateral sideof the body.

The apparent lack of a major projection from HA to thesensory trigeminal nuclei is noteworthy from both avianand comparative points of view. In birds, the pars caudalisof the spinal trigeminal nucleus receives dense projectionsfrom the alternative somatosensorimotor outflow from thetelencephalon, i.e., from the archistriatum via the occipito-mesencephalic tract (OM; Zeier and Karten, 1971; Wild,unpublished observations). This division of origin of de-scending projections to sensory relay nuclei (i.e., Wulstversus archistriatum) is probably a reflection of the fact

Fig. 12. Location of retrogradely labeled cells (black dots) in HAafter injections of CTB into the dorsal column nuclei (A), SpM (B), theposterolateral hypothalamus (C), and ICo (D). A: A medial sagittalsection that also shows the location of the injection (Inj.) on theipsilateral side; B: A right frontal hemisection, the SpM injection also

being on the right. C: A frontal section showing bilateral labeling aftera right-sided hypothalamic injection. D: A left frontal hemisectionshowing labeling after the injection in the ipsilateral ICo shown inblack in E. E: Retrogradely labeled cells (black dots) in ICo bilaterally.For abbreviations, see list. Scale bars 5 1 mm.


that a sensory trigeminal representation has not beenfound in the rostral Wulst, but instead is found in nucleusbasalis, most of the multisynaptic projections from whicheventually reach the archistriatum, rather than the Wulst(Wild et al., 1985; Wild and Farabaugh, 1996). As men-tioned above, the outflow from the archistriatum to brain-stem levels is via OM, which is said to resemble Bagley’sbundle in ungulates. This comparison receives some sup-port from the fact that, in the goat, it is this bundle ratherthan the pyramidal tract itself that terminates in thespinal trigeminal nucleus (Haarsten and Verhaart, 1967).However, in the goat, the Bagley bundle and the pyramidaltract originate from the same area of cortex, whereas inbirds OM and the pyramidal tract originate from twoentirely different areas of the pallium. In addition to thiscomparison, the pyramidal tract in finches was found togive rise to many fibers that did not descend through thepons and medulla as a compact bundle, but traveled

caudally in more central and dorsal parts of the tegmen-tum. Although it was not possible to determine the specificsites of termination of these widely dispersed fibers, manyof them probably ended in the lateral tegmentum, just asmany fibers in the bundle of Bagley do in the goat. Thus,finches may have two components that resemble Bagley’sbundle, one originating in the same cortical region as thepyramidal tract and terminating in the lateral tegmen-tum, as in the goat, and another originating in thearchistriatum that terminates in parts of the spinal trigemi-nal nucleus, among many other regions of the brainstem(Zeier and Karten, 1971; Wild and Farabaugh, 1996;Dubbeldam et al., 1997).

Another HA projection to what may be considered asensory relay was to the intercollicular region (ICo) sur-rounding the central nucleus of the inferior colliculus(ICc). This shell-like region is the nexus of several function-ally related projections, for in addition to the projections

Fig. 13. Brightfield photomicrographs showing retrograde andanterograde labeling after an injection of CTB into medial ICo such asis shown in Figure 12E. a: Retrogradely labeled cells in the left HA (themedial margin of the hemisphere is shown at right). b: Retrogradelylabeled cells in the caudomedial paleostriatum primitivum. c: Retro-gradely labeled cells around the robust nucleus of the archistriatum(RA; medial is the right.). d: Anterograde labeling around the periph-

ery of the right nucleus ovoidalis (Ov). The anterograde labeling fromthe injection shown in Figure 12E was predominantly ipsilateral, butthe labeling in the contralateral Ov is shown in d to illustrate therelation of Ov to the suprajacent DIVA, cells that were retrogradelylabeled by a BDA injection in the right rostral HA in the same case. Forabbreviations, see list. Scale bars 5 200 µm in a,c,d; 100 µm in b.


from HA, it receives distinct projections from 1) the dorsalcolumn nuclei and cells in medial lamina V of the uppercervical spinal cord (Leibler, 1975; Wild, 1989; Wild, 1995;Wild, 1997; present study); 2) a region of the archistriatumintermedium (Ai) that in songbirds surrounds RA and isthought to comprise the ‘‘auditory archistriatum’’ (Mello etal., 1998; but see Wild and Williams, 1999), or from amedial region of Ai in non-songbirds (Wild et al., 1993;Mello et al., 1998; present study); 3) large cells in thecaudal and medial parts of the paleostriatum primitivum,cells that may in turn receive their input, via the paleostria-tum augmentatum, from audiosomatic regions of thecaudomedial neostriatum, such as parts of the Field Lcomplex and nucleus interface (NIf; Wild et al., 1993;present study); and 4) the medial and lateral hypothala-mus (Berk, 1987; Berk and Butler, 1981; present study). Inboth songbirds and non-songbirds (e.g., Columbiformes),neurons in parts of ICo that surround the ICc, includingthe caudomedial nucleus of the torus semicircularis andthe core nucleus of the superficial preisthmic area (aspecialized somatosensory nucleus identified in pigeons;see Wild, 1995), project rostrally and terminate in or closeto nucleus ovoidalis, the principal auditory nucleus of thethalamus (Leibler, 1975; Schneider, 1991; Durand et al.,1992; present study). These afferent and efferent projec-tions of the intercollicular region surrounding ICc supportthe idea of its being a site of audiosomatic convergence andprocessing, distinctly reminiscent of the shell-like regionthat surrounds parts of the inferior colliculus in mammalsand includes the external and dorsal nuclei (Huffman andHenson, 1990; Wild, 1995). Moreover, the fact that the ICcitself receives projections from the dorsal column nuclei(Wild, 1995; Wild, 1997), the fact that nucleus ovoidalis(Ov) can also be partioned into ‘‘core’’ and ‘‘shell’’ regionsbased on their cytoarchitecture and their differential pro-jections to the caudal telencephalon (Wild et al., 1993;Vates et al., 1996), and the fact that the Ov shell receivesthe output of parts of the shell surrounding ICc, all suggestthat audiosomatic convergence may be a constant featureat all levels of the auditory and somatosensory pathwaysin the avian brain, including some parts of the telencepha-lon to which Ov and its shell project (Korzeniewska, 1987;Wild, 1995; Vates et al., 1996).

The most rostral of the sensory relay nuclei that receivesa projection from HA is the principal somatosensorythalamic nucleus, DIVA. Only sparse terminations wereobserved in this nucleus, although in those cases in whichthe HA injection also included parts of IHA, the presence ofretrogradely labeled cells in DIVA could have obscuredsome of these terminations. These results complementthose from studies of the efferent projections of the visualWulst, which terminate in dorsal thalamic visual nucleithat provide the input to IHA (Karten et al., 1973; Casiniet al., 1992).

Minor projection to the ventral horn

In addition to the majority of spinal terminations in thebase of the dorsal horn at upper cervical levels, there werealso some labeled fibers in the ventrolateral funiculus anda few terminations in the tip of the ventral horn where themotoneurons of various neck muscles are located (Zijlstraand Dubbeldam, 1994). Although direct projections fromthe pyramidal tract to spinal motoneuronal pools haveoften been regarded as present mainly in primates(Kuypers, 1981), they have more recently also been found

in rats (Liang et al., 1991). The fact that they are alsopresent in birds may seem at variance with the idea oftheir being related to manual dexterity, but the bird’s neckis an extraordinarily mobile device for placing the headand beak in grasping and manipulative positions. From afunctional point of view, therefore, the bird’s neck can beseen as analogous to the arm and wrist of higher primatesand may, therefore, be under partial direct ‘‘cortical’’control. Shiga et al. (1988) suggested that early-developingreticulospinal and possibly other bulbospinal axons thattravel in the lateral funiculus make monosynaptic contactswith the dendrites of spinal motoneurons in chicks, but thepossibility that pyramidal tract fibers contribute to suchcontacts should perhaps now be considered.

Relation of inputs to outputs in HA

In summary, HA of the rostral Wulst seems likely to besignificantly involved in the control of somatosensoryinput at several levels of the neuraxis. HA probably gainsaccess to primary somatosensory information via thethalamic projection of DIVA to IHA (Wild, 1987, 1997), inan analogous manner to the way in which HA at morecaudal levels gains access to visual information derivedfrom the projections of the principal optic nuclei of thethalamus to IHA of the visual Wulst (Karten et al., 1973;Shimizu et al., 1995). It should be noted, however, thatalthough the projections of DIVA are concentrated in IHA,they are not confined to this lamina, but extend medially toa lesser extent into HA itself (Wild, 1997; and unpublishedobservations in zebra finches), a fact that could suggestsome direct input onto descending projection neurons.Further detailed work is required to clarify the path ofinformation transfer through the laminae of the avianWulst (see also Shimizu et al., 1995).

Whether the rostral Wulst also has a significant role inmotor control remains to be determined, although thesubstantial projections of HA to the red nucleus, the regionof the subcoeruleus ventralis, and to extensive regions ofthe lateral medulla may all contribute to such a role. Thepossible effects of lesions to HA on movements or posturehave not been investigated, but subtle rather than dra-matic effects will require careful assessment. Overall, theextratelencephalic projections of the rostral Wulst of passe-rine birds resemble components of the pyramidal tract inmammals that originate from both parietal and frontalcortices, in that they descend to innervate both the variousprecerebellar and sensory relay nuclei and brainstemnuclei possibly involved in motor control. In birds, how-ever, the cells of origin of the pyramidal-like projections tothe various extratelencephalic sensory relay and premotornuclei appear to a large extent to be intermixed in rostralHA, but they overlap only to a certain extent with the cellsof origin of the intratelencephalic projections (Wild andWilliams, 1999). Whether HA cells collateralize to differenttargets remains to be assessed.

HA-hypothalamic connection

The reciprocal connections of rostral HA with the stra-tum cellulare externum are discussed last because thehypothalamus is not usually considered in the samecontext as the targets of the pyramidal tract. The presentfindings in finches confirm similar findings of a projectionof TSM to the posterolateral hypothalamus in the mallardduck (Dubbeldam, 1976), but a rationale for this connec-tion is lacking. In mammals, parts of the prefrontal cortex,


Fig. 14. Summary schematic chartings of the predominantly ipsi-lateral, extratelencephalic projections of the rostral Wulst—the ‘‘pyra-midal tract’’—in finches. The injections of BDA in rostral HA areshown in black in A, and the labeled fibers as short wavy linesthroughout the remaining sections. Particularly dense terminations,e.g., in SpM and Ru in H, are additionally indicated by dots. Theso-called septomesencephalic tract (TSM) courses through the medial

margin of the telencephalic hemisphere (B,C) and breaks up intodorsal and ventral rami in the rostral diencephalon (E). The tractenters the spinal cord caudal to level O and travels in the lateralfuniculus as far as C6–C7 (level P is at C2). Projections from HA to thecerebellum are not shown (Wild and Williams, unpublished observa-tions). For abbreviations, see list. Scale bar 5 1 mm.

Figure 14 (Continued)


particularly its medial, lateral, and orbitofrontal parts,have connections with the hypothalamus, including itsposterolateral nuclei (e.g., Takagishi and Chiba, 1991;Morecraft et al., 1992; Hardy, 1994; Buchanan et al., 1994;Kunzle and Lotter, 1996; Ongur et al., 1998). A ‘‘prefrontalcortex’’ has been postulated for the avian brain (e.g., Divacet al., 1994), but this is located much more caudally in theposterodorsolateral telencephalon and does not originateany extratelencephalic projections. An alternative sugges-tion might be that an avian prefrontal analogue to themammalian prefrontal cortex, if there is one at all, is likelyto lie anterior to a somatosensory/somatomotor area, as inmammals. In reality, this is impossible in the passerinebrain, because the somatosensory/somatomotor area isalready situated at the rostral pole of the brain, butperhaps the rostral HA incorporates several differentkinds of neurons, some of which are more closely related tothe hypothalamus than they are to the pyramidal tract. Animportant caveat to this suggestion, however, is that thereis currently no evidence, either from the present or anyother study, that the rostral HA receives a projection fromany thalamic nucleus that may be considered the avianversion of a mediodorsal nucleus (MD; Veenman et al.,1997). Apart from DIVA, the only thalamic nucleus identi-fied in the present study as a possible source of afferents torostral HA was the nucleus subrotundus (SRt), the nucleus

claimed by Medina et al. (1997) not to project to the rostralWulst in pigeons. This discrepancy may be due not to aspecies difference, but to the fact that the injections in therostral Wulst made in the study by Medina et al. (1997)were in the dorsal part of HA, whereas the rostral Wulstinjections in the present study were made in deep HA.However, the fact remains that SRt is not consideredcomparable with MD in mammals (Veenman et al., 1997).Further speculation about the specific meaning of thehypothalamic connection is unwarranted at the presenttime. From a broader perspective, however, it can be notedthat both telencephalic regions that send long descendingprojections as far as the lower brainstem, viz HA and thearchistriatum, also send projections to the hypothalamus,that from the archistriatum to the medial hypothalamusand that from HA to more lateral parts of the hypothala-mus and to the periaqueductal gray (Zeier and Karten,1971; present study). Like the archistriatum, therefore, HAmay be capable of exerting control over visceral/autonomicand somatosensorimotor components of behavior.

LITERATURE CITED

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Figure 14 (Continued)


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Rostral Wulst in passerine birds. I. Origin, course, and terminations of an avian pyramidal tract

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