rostral wulst of passerine birds: ii. intratelencephalic projections to nuclei associated with the...

Rostral Wulst of Passerine Birds:II. Intratelencephalic Projections

to Nuclei Associated With the Auditoryand Song Systems

J.M. WILD AND M.N. WILLIAMS

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

ABSTRACTWe have previously shown that the hyperstriatum accessorium (HA) of the rostral wulst

in zebra finches and green finches is the origin of a pyramidal-like tract with substantialprojections to the brainstem and cervical spinal cord. Here, we show that the HA also is theorigin of a set of intratelencephalic projections with terminal fields in the lateral part of thefrontal neostriatum, the shell surrounding the lateral magnocellular nucleus of the anteriorneostriatum, the lobus parolfactorius surrounding area X, the nucleus interface, auditoryfields L1 and L3, the shelf underlying the high vocal center, the dorsolateral caudalneostriatum, the dorsocaudal part of the nucleus robustus archistriatalis, and the ventralarchistriatum. The cells of origin of these projections are located predominantly laterally inthe HA, close to and sometimes within the intercalated HA, which receives somatosensoryprojections from the dorsal thalamus. The specific implications of these findings for auditoryand vocal function are unclear, but the apparent overlap of auditory and somatosensory inputsin several of these regions suggests the possibility of mechanisms for stimulus enhancementor depression, depending on the congruence of stimuli within a cell’s ‘‘in-register’’ multiplereceptive fields. J. Comp. Neurol. 413:520–534, 1999. r 1999 Wiley-Liss, Inc.

Indexing terms: zebra finch; area X; lateral magnocellular nucleus of the anterior neostriatum;

auditory lamina 113; high vocal center; nucleus robustus archistriatalis

On the basis of its afferent and efferent projections, theavian wulst generally can be divided rostrocaudally intotwo main regions: a larger and more caudal part that isrelated to the visual system and a smaller more rostralpart that is related to the somatosensory system. Thevisual and somatosensory afferent projections arise, respec-tively, from a group of principal optic nuclei and thenucleus dorsalis intermedius ventralis anterior (DIVA) ofthe dorsal thalamus, and they terminate primarily in athin lamina known as the intercalated hyperstriatumaccessorium (IHA) that flanks the HA laterally at rostrallevels and ventrally at more caudal levels (Karten et al.,1973; Bagnoli and Burkhalter, 1983; Wild, 1987, 1997;Funke, 1989a,b).

A major portion of the efferent projections of the wulstarises from the hyperstriatum accessorium (HA), whichhas both extra- and intratelencephalic targets (Huber andCrosby, 1929; Reiner and Karten, 1983; Shimizu et al.,1995). Extratelencephalic projections originating in HA ofthe visual wulst have been documented amply (Karten et

al., 1973; Bravo and Pettigrew, 1981; Rio et al., 1983;Miceli et al., 1987; Casini et al., 1992; Shimizu et al., 1995),and a pyramidal-like tract originating in the rostral HAhas been delineated recently (Wild and Williams, unpub-lished observations). Descriptions of the intratelence-phalic projections of rostral HA, however, have beenlimited to certain aspects of the somatosensory system inpigeons (Wild, 1987; Funke, 1989b). In the current report,therefore, we describe previously unidentified intratelence-phalic projections of rostral HA, projections that includedcertain nuclei related to the auditory and song systems.

Grant sponsor: Whitehall Foundation, Inc.; Grant number: R94R07;Grant sponsor: National Institutes of Health; Grant number: 2 R01NS29467–07.

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

Received 26 February 1999; Revised 27 May 1999; Accepted 30 June 1999

THE JOURNAL OF COMPARATIVE NEUROLOGY 413:520–534 (1999)

r 1999 WILEY-LISS, INC.

MATERIALS AND METHODS

The experimental procedures were carried out accordingto the guidelines of the Animal Ethics Committee of theUniversity of Auckland. Data from 51 male and femalezebra finches and eight male green finches contributed tothe current study. Twenty-one of the birds (13 zebrafinches and eight green finches) were used in previousstudies of the extratelencephalic projections of the rostralwulst (Wild and Williams, unpublished observations), anddata from an additional 30 birds were used in the currentstudy to assess further the afferent and efferent intratelen-cephalic connections of the rostral wulst. Some of thesesupplementary data were derived from archival cases thatwere used originally in other studies (e.g., Wild, 1994; Wildand Farabaugh, 1996). Briefly, the birds were anesthetizedwith an intramuscular injection of an equal parts mixtureof ketamine (50 mg/kg) and xylazine (20 mg/kg) and placedin a David Kopf stereotaxic frame (Kopf, Inc., Tujunga, CA)with the head tilted down 45° to the horizontal plane(Stokes et al., 1974). Injections of either biotinylateddextran amine [BDA; Molecular Probes, Eugene, OR; 10%in 0.1 M phosphate-buffered saline (PBS), pH 7.4] and/orunconjugated cholera toxin B-chain (CTB; List Laborato-ries, Inc., Campbell, CA; 1% in distilled H2O) or CTBconjugated to horseradish peroxidase (HRP; McIlhinney etal., 1988) were made through glass micropipettes (outerdiameter, 15–20 µm) into the HA and various other nucleithat were putative targets of HA projections either byiontophoresis (4 µA positive current for 15–30 minutes) orair pressure delivered through a Picospritzer (GeneralValve, Fairfield, NJ). BDA and CTB sometimes wereinjected in the same bird in different nuclei either on thesame side or on opposite sides of the brain. This was doneto assess the degree of convergence of the efferent projec-tions of each of two nuclei or to juxtapose afferent andefferent projections at a single locus.

Electrophysiological recordings of potentials and mul-tiple-unit activity evoked by somatosensory stimuli ap-

plied to various parts of the body were made from certaintelencephalic nuclei (e.g., IHA, nucleus interface, a.k.a.NIf) to guide the subsequent injection of tracers into ornear physiologically defined loci. Also, acoustic clicks deliv-ered at a rate of 1 Hz through a hollow ear bar were used assearch stimuli for the identification of either known audi-tory regions (e.g., the nucleus ovoidalis, parts of the field Lcomplex, or the nucleus basalis; Fortune and Margoliash,1992; Wild et al., 1993; Vates et al., 1996; Wild andFarabaugh, 1996) or to assess the possibility of auditory-evoked potentials in other regions, such as HA and IHA.Such recordings were made with tungsten microelectrodes(Frederick Haer; 3–5 MV) that were insulated except attheir tips. Recordings were monitored oscillographicallyand over a loud speaker. Spontaneous unit activity charac-teristic of that in the nucleus robustus archistriatalis (RA)of birds anesthetized with ketamine and xylazine (Wild,1993) was used to guide injections into or near the RA.

After survival times ranging from 4–7 days, birds in-jected with BDA and/or CTB were deeply anesthetized andperfused through the heart with saline followed by 4%paraformaldehyde (PFA) in 0.1 M phosphate buffer, pH7.4. Brains were blocked in either the transverse orsagittal plane, equilibrated in 25% sucrose overnight, andsectioned on a freezing microtome at 30 µm. Serial sectionswere collected in four series, one or more of which was usedfor the immunohistochemical visualization of either BDA,CTB, or both, as described elsewhere (Wild, 1995). Briefly,BDA was visualized by using streptavidin peroxidaseconjugate (Molecular Probes, Inc.) at a dilution of 1:1,000in PBS plus 0.4% Triton X-100 for 1 hour, followed by0.025% 3,38-diamino benzidine (DAB) and H2O2. CTB wasvisualized by using a polyclonal anticholeragenoid anti-body (List Biological Laboratories, Inc.) diluted 1:30,000 at4°C for 15 hours, followed by a rabbit anti-goat biotinyl-ated secondary antibody (Sigma Chemical Company, St.Louis, MO) diluted 1:200 for 1 hour, streptavidin peroxi-dase diluted 1:1,000 for another hour, and finally DAB plus

Abbreviations

Ad archistriatum dorsaleAi archistriatum intermediumAL ansa lenticularisBas nucleus basalisBO bulbus olfactoriusCA commissura anteriorCb cerebellumDIVA nucleus dorsalis intermedius ventralis anteriorE ectostriatumFA fasciculus archistriatalisFPL fasciculus prosencephali lateralisGLv nucleus geniculatus lateralis, pars ventralisHA hyperstriatum accessoriumHD hyperstriatum dorsaleHIS hyperstriatum intercalatus superiorHV hyperstriatum ventraleHVc high vocal center (previously hyperstriatum ventrale, pars

caudalis)ICo nucleus intercollicularisIHA hyperstriatum accessorium, pars intercalatusL1 more rostral of the two lamina that flank the principal thal-

amorecipient lamina of the auditory telencephalon (Fortune and Margoliash, 1992)

L2a principal thalamorecipient lamina of the auditory telen-cephalon

L3 more caudal of the two lamina that flank the principal thal-amorecipient lamina of the auditory telencephalon (For-tune and Margoliash, 1992)

LFM lamina frontalis supremaLFS lamina frontalis superiorLH lamina hyperstriaticalMAN lateral magnocellular nucleus of the anterior neostriatumLMD lamina medullaris dorsalisLPO lobus parolfactoriusNC neostriatum caudaleNF neostriatum frontaleNI neostriatum intermediumNIf nucleus interfaceOM tractus occipitomesencephalicusPA paleostriatum augmentatumPrV nucleus sensorius principalis nervi trigeminiPP paleostriatum primitivumQF tractus quintofrontalisRA nucleus robustus archistriatalisRSd nucleus reticularis superior, pars dorsalisRt nucleus rotundusSpL nucleus spiriformis lateralisSpM nucleus spiriformis medialisTn nucleus taeniaeTSM tractus septomesencephalicusV valeculaX area X

INTRATELENCEPHALIC PROJECTIONS OF ROSTRAL WULST 521

H2O2. At least one series was counterstained with eithercresyl violet or Giemsa for the visualization of nucleargroups. Birds injected with CTB-HRP) were perfused withsaline followed by 1% PFA and 1.25% glutaraldehyde in 0.1M phosphate buffer. Their brains were sectioned serially at40 µm on a freezing microtome and collected in two series,both of which were reacted with 3,38-tetramethyl benzi-dine, according to the method of Mesulam (1978), and oneof which was counterstained subsequently on the slidewith neutral red. The projections were charted with theaid of a drawing tube using both brightfield and darkfieldillumination, and they were photographed and/or scannedinto a Macintosh PowerMac computer (Apple Computers,Cupertino, CA) for digital representation.

RESULTS

Efferent projections resulting from HAinjections

All but three of the injections in HA were concentrateddeliberately in more ventral regions of the lamina, theirlateral extent being guided at surgery by the somatosen-sory recordings made from IHA, and were limited histologi-cally by the lamina frontalis suprema (LFM), which formsthe lateral border of IHA (Figs. 1A, 3A). No responses toauditory clicks or other acoustic stimuli (claps, jingles,whistles, etc.) were found in the HA or the IHA of therostral wulst. Some injections were large and encroachedon the caudally adjacent visual wulst, and some weresmaller and remained confined to the rostral wulst.

Because the injections were located virtually at therostral pole of the brain, the projections radiated caudallyin several directions. All but one were entirely ipsilateral.Those projections that radiated laterally can be appreci-ated best in the frontal plane (Fig. 1), whereas those thatpassed caudally at more oblique angles can be appreciatedbest in the sagittal plane (Fig. 3). From the injection site,fibers extended laterally in a wide arc throughout thefrontal neostriatum (NF) and terminated extensively in itslateral regions (Fig. 1D), particularly in relation to anaturally occurring lamina that divides the NF into me-dial and lateral parts (Figs. 1, 2A,B). The caudal parts ofthis field came to lie immediately dorsolateral to caudalparts of nucleus basalis (Bas; Fig. 1E), a nucleus that islocated more laterally at caudal levels than at rostrallevels (Fig. 1B–F).

More medially in the frontal neostriatum, another termi-nal field surrounded the lateral magnocellular nucleus ofthe anterior neostriatum (lMAN; Figs. 1C, 2C,D). Thisfield was more dense rostral to lMAN than in other parts ofthe surround. There were many labeled fibers withinlMAN, some of which presumably were fibers of passage,but others that had varicosities along their length mayterminate there.

Ventral to lMAN, a massive terminal field was presentin the lobus parolfactorius (LPO), which, in males, wasconcentrated densely in the region surrounding area X,particularly rostroventrally (Figs. 1B–E, 2C,G). Similar towhat was seen in lMAN, there were many fibers of passagewithin area X, but varicosities along the length of some ofthe fibers or at their terminations within X also wereapparent (Fig. 2F,G). In females, in which an area X is notapparent, the projection to LPO filled in the region wherearea X would be (Fig. 2H).

Other contingents of fibers leaving rostral HA coursedcaudally and dorsally through all the lamina that dividethe major regions of the pallium: the lamina medullarisdorsalis (LMD), the lamina hyperstriatica (LH), and thetwo frontal laminae, superior (LFS) and suprema (LFM;Fig. 3A,B). Those in LMD and, to a lesser extent, some inLH gave rise to distinct and dense terminal fields withinNIf and the secondary auditory fields L1 and L3 (Fig.3C–E; Fortune and Margoliash, 1992). A small terminalfield also was present in the paleostriatum augmentatum(PA), which is subjacent to these fields (Fig. 3E). Moredorsocaudally, fibers coursing through the LH and thefrontal laminae gave rise to terminal fields within the‘‘shelf ’’ underlying the high vocal center (HVc; Fig. 3F,G).The precise location of these terminal fields varied fromcase to case, but they all tended to be associated with morerostral parts of the shelf. Some fibers surrounded HVc bypassing between its dorsal border and the adjacent lateralventricle. Lateral to HVc, there was an extensive terminalfield in the dorsolateral part of the neostriatum caudale(Fig. 4A). In the caudal hemisphere, labeled fibers de-scended through the dorsal archistriate tract and gave riseto a small, discrete terminal field in the dorsocaudalborder region of RA (Fig. 4B,C) and in a part of theintermediate archistriatum located immediately lateral toRA (Fig. 4D). Another small terminal field was presentbilaterally in the rostral part of the ventral archistriatum(Fig. 4E).

Retrograde confirmation of the HAprojections

Injections of either BDA or CTB into most of the putativetargets of HA in the telencephalon all gave rise to retro-gradely labeled cells in the rostral HA (Figs. 5–7). Injec-tions immediately rostral to lMAN (Fig. 5A), or medial toarea X (Fig. 5C), or in the lateral NF (Fig. 5D) labeled cellsthat were concentrated in more lateral regions of HA (Fig.5a,c,d). Injections dorsolateral to caudal Bas produced asimilar pattern of retrograde labeling in the lateral HA(not shown). Large injections of CTB into area X (Fig. 5B)retrogradely labeled numerous neurons throughout thedorsoventral and mediolateral extent of the rostral HA, inventral regions of the IHA, in the hyperstriatum dorsale(HD), and in the ventral part of HV (Fig. 5b). In contrast,small iontophoretic injections of BDA centered within areaX labeled a few neurons that were located laterally in HA,close to IHA (not shown). Injections into NIf were guidedby electrophysiological recordings of robust somatosensoryresponses to stimulation of contralateral parts of the body(Wild, 1994). Small, iontophoretic injections of BDA intoNIf (Fig. 6A) retrogradely labeled neurons in the nucleusuvaeformis (Uva), a posterodorsal thalamic nucleus that isknown to project on NIf (Nottebohm et al., 1982; Wild,1994), and also labeled a few neurons in HA that wereconfined laterally, adjacent to IHA (Fig. 6a). Larger, Pico-spritzer injections of either BDA or CTB that included theNIf and parts of either field L1 or field L3 (Fig. 6B)retrogradely labeled cells in Uva and in parts of thenucleus ovoidalis as well as many neurons in the rostralHA, the majority of which were clustered ventrolaterally,some even in the IHA (Figs. 6b, 7A). Injections thatincluded the HVc and the HVc shelf (Fig. 6C) labeledneurons that tended to be scattered throughout HA,although, in two cases that involved large CTB injections

522 J.M. WILD AND M.N. WILLIAMS

into this region, a distinct band of cells was located in theventrolateral HA, and some were located close to theventral margin of the hemisphere, possibly in the HD(Figs. 6c, 7B). Similarly, large injections of CTB into thedorsolateral caudal neostriatum (Fig. 6D) also labeledneurons scattered throughout HA but tended to leave theapex of the ‘‘V’’-shaped lamina free of labeled neurons(Figs. 6d, 7C). In cases that involved BDA injections thatwere confined largely to the RA, no retrogradely labeledcells were found in the HA. Large injections of CTB that

were centered on the RA but that inevitably includedadjacent parts of the archistriatum and neostriatum retro-gradely labeled a few neurons in the medial HA (notshown). The ventral archistriatum was not investigated.

Intratelencephalic afferents to HA

Sources of afferents to HA were indicated both by thepresence of retrogradely labeled cells in several regions ofthe telencephalon (including other laminae of the wulst)after injections into HA and by the presence of fibers in HA

Fig. 1. A–H: Rostrocaudal series of schematic frontal hemisectionsdepicting the projections of the hyperstriatum accessorium (HA)throughout more rostral parts of the zebra finch brain. The injectionsof biotinylated dextran amine (BD)A are shown as solid black in A,

with spread from the injections indicated by hatching. The antero-grade labeling is indicated by short, wavy lines, and retrogradelylabeled cells are shown as black dots. For abbreviations, see list.


Figure 2


after injections into the target nuclei of HA projectionneurons. However, most of the HA injections were notdesigned optimally or purposely, either in terms of theirsize or their location, to define sources of afferents withinthe wulst itself; hence, these results are not illustrated.Suffice it to say that injections of BDA that were confinedto HA and did not encroach on IHA, retrogradely labeledneurons in parts of the nearby IHA, but the great majorityof labeled wulst cells were located in the HD (see alsoShimizu et al., 1995). In finches, the HD forms the lateralpart of the combined lamina that, in Figures 1A, 5a–d, and6b–d, is designated HIS/HD. The same lateral part of thislamina also doubles as the route of entry of thalamicafferent fibers destined for the IHA. In other words, lateralHD cells are embedded in the LFS.

With regard to the regions outside the wulst thatreceived a projection from HA, most of these also sent aprojection back to HA. On the basis of retrograde labelingafter injections into HA, this was more obvious in CTBcases than in BDA cases, because CTB always retrogradelylabeled more neurons than BDA in a region in which itanterogradely labeled a terminal field (e.g., in NIf, L1, andL3; compare Fig. 3D with Fig. 3E). However, irrespective ofthe type of tracer injected into HA, retrogradely labeledcells were found in the lateral part of NF, including theregion dorsolaterally adjacent to caudal regions of nucleusbasalis (Figs. 1D–G, 2A,B); in the region surroundinglMAN, particularly rostrally (Fig. 2D,E); in NIf, fields L1and L3, and caudal PA subjacent to these structures (Figs.3E); in the HVc ‘‘shelf ’’ (Fig. 3G); in the dorsolateral caudalneostriatum (retrograde labeling not shown); and bilater-ally in the ventral archistriatum (not shown). No labeledcells were found in the archistriatum intermedium (Ai) orthe RA.

After injections of BDA into several of the target nucleiof the HA projections, labeled fibers frequently were

observed in the rostral HA. In most cases, however, suchfibers generally did not give rise to the type of denseterminal field to which the HA projections gave rise, butthey were scattered diffusely throughout the HA (e.g., seeFig. 6a). An exception to this rule was in the case of aninjection into the lateral frontal neostriatum, which pro-duced the terminal field in ventrolateral HA shown inFigure 7D.

DISCUSSION

The intratelencephalic projections of the HA of therostral wulst described in the current report becameobvious when an attempt was made to identify the sourceof an avian pyramidal tract (Wild and Williams, unpub-lished observations). They were somewhat surprising,therefore, in terms of their target specificity, because HAhas not been linked previously to either the auditorysystem or the song system of song birds. However, of all ofthe parts of the telencephalon that the HA might haveinnervated, most of the parts that were innervated, in fact,are associated in some way with the auditory and songsystems. The sections below discuss these associations andother projections.

Lateral frontal neostriatum

Projections to a similar region from rostral HA havebeen noted by Shimizu et al. (1995) in pigeons, althoughthe lateral neostriatal terminal field in finches was locatedrelatively more caudally than the terminal field in thelateral frontal neostriatum (NFL) depicted by Shimizu etal. (1995). NFL in pigeons also has been shown to receive aprojection from the periectostriatal belt (Ritchie, 1979;Shimizu et al., 1989), which may suggest the possibilitythat, according to Shimizu et al. (1995), the NFL is a site ofconvergence of information derived from the thalamofugaland tectofugal visual pathways. It is not clear, however,whether the injection into the rostral HA depicted inFigure 5A of the study of Shimizu et al. (1995) was locatedin a visual region of the HA or in a region of overlap ofvisual and somatosensory representations (cf. Deng andWang, 1992). In the current study, small iontophoreticinjections of BDA that were confined to the very rostral,ventral, and presumably nonvisual (somatosensory) partof the HA gave rise to the projection to the NFL. Further-more, retrogradely labeled cells were found in the rostralHA after injections into the NFL, as they were in pigeonsin the study of Shimizu et al. (1995). Although theseconsiderations do not rule out the possibility that the NFLis a site of convergence of visual information derived fromthe two main visual pathways, they do suggest either thatNFL is a site of convergence of somatosensory and visualinformation or that visual and somatosensory regions ofthe HA have contiguous but nonoverlapping projections tothe NFL.

NF region adjacent to nucleus basalis

In the current study, the most caudal part of theterminal field in the NF approximated the caudal region ofthe Bas. The Bas in zebra finches receives a distinctauditory projection from the intermediate nucleus of thelateral lemniscus, as in other birds (Delius et al., 1979;Arends and Zeigler, 1986; Wild and Farabaugh, 1996; Wildet al., 1997). Bas also has short axonal projections to theadjacent NF (Wild et al., 1985; Veenman and Gottschalk,

Fig. 2. Series of brightfield (A–F) and darkfield (G,H) photomicro-graphs showing anterograde and retrograde labeling in the frontalneostriatum and basal ganglia after injections of BDA (A–G; zebrafinch) or cholera toxin B-chain-horseradish peroxidase (CTB-HRP; H;green finch) in the HA. A: Anterograde and retrograde labeling in thelateral neostriatum frontale (NF; frontal section). B: View similar tothat shown in A but in a Nissl-counterstained section to show thenucleus basalis (lateral border demarcated by arrowheads, medialborder demarcated by the lamina medullaris dorsalis; LMD), and thedistinct lamina (at the arrows) that divides the lateral neostriatumfrontale into lateral and medial parts. The terminal field here isdifficult to see, but the retrogradely labeled cells can be seen clusteredat the curved arrow. C: Sagittal section, with rostral to the left,through area X and the lateral magnocellular nucleus of the anteriorneostriatum (lMAN; asterisk). D: Higher power view of labeling inlMAN shell and surrounding regions (sagittal section; rostral is to theleft; the asterisk marks the center of lMAN). E: Labeling in lMANshell ventral to lMAN. The border is marked by the dashed line(frontal section). F: High-power view of anterograde labeling in themiddle of area X. G: Anterograde labeling in and around the medialperiphery of area X (sagittal section; rostral is to the left). H: Terminallabeling in the lateral part of the lobus parolfactorius (LPO) in afemale green finch (right side; frontal section). The arrowheads pointto the lamina medullaris dorsalis (LMD) and define the dorsal andventral bounds of the crescent-shaped nucleus basalis (Bas) lateral toLMD. Bas is unlabeled but, in this darkfield photomicrograph, isbrighter relative to unlabeled parts of the LPO. The labeled septomes-encephalic tract (TSM) appears as a narrow, white strip on the medialaspect of the hemisphere at left, and the ventricle that is immediatelylateral to TSM is marked by arrows (cf. Fig. 1F). Scale bars 5 200 µmin A–D,G,H, 100 µm in E,F.


Fig. 3. A: Schematic summary drawing of the projections resultingfrom injections of BDA into HA, lateral spread from which is shaded.The projections are indicated by solid lines that end either as arrows,signifying the direction of the continued projection, or as invertedarrows, signifying terminations. B–G: Darkfield (B,F) and brightfield(C–E,G) photomicrographs depicting HA projections to and fromvarious structures. B: BDA-labeled fibers in the lamina hyperstriaticaen route to the high vocal center (HVc) shelf and more lateral parts ofthe dorsocaudal hemisphere. C–E: BDA-labeled terminal fields in the

nucleus interface (NIf), and in laminae 1 and 3 (L1 and L3). In C,which is a right sided, frontal, lightly counterstained section, thearrowheads point to the lamina medullaris dorsalis. D and E aresagittal sections in which the terminal fields in L1 and L3 flankthe unlabeled primary thamorecipient auditory lamina L2a.F: BDA-labeled terminal field in the HVc shelf of a zebra finch (rightside; frontal section). G: CTB-labeled terminal field together withretrogradely labeled cells in the HVc shelf of a green finch (right side;frontal section). For other abbreviations, see list. Scale bars 5 200 µm.

1986; Dubbeldam and Visser, 1987; Wild and Farabaugh,1996), thereby implicating the connection of the NF withthe HA identified in the current study as one by whichauditory information could reach the HA. The HA couldthen transmit this information to the NIf, the auditoryfields L1 and L3, and the HVc shelf, thereby providing analternative route of entry of auditory information to thesong system. Whether such a circuit actually functions in

this way remains to be determined, but the followingobservations are germane. Although evoked responses toauditory stimuli (e.g., clicks) have been reported from thewulst in chickens and pigeons (see, e.g., Adamo and King,1967; Delius and Bennetto, 1972), the localization of theseresponses, particularly with respect to the rostrocaudaldirection, was either unspecified or too imprecise to placethem unequivocally in the rostral HA. Their relatively

Fig. 4. Fiber and terminal labeling in various structures afterinjections of BDA into the ipsilateral HA of the zebra finch (all aresagittal sections; rostral is to the left). A: Terminal field in thedorsolateral caudal hemisphere roughly corresponding to the locationof the injection shown in Figure 6D. B: Small terminal field in thedorsocaudal nucleus robustus archistriatalis (RA), the border of whichis marked with a dashed line. A few labeled fibers can be seen entering

RA from above. C: The RA terminal field at higher power in aNissl-counterstained section. Arrowheads point to the dorsocaudalborder of RA. D: Terminal field in the archistriatum intermedium (Ai)lateral to RA; the dorsal border of the archistriatum is indicated byarrows. E: Small terminal field in the ventral archistriatum (indicatedby arrows). The ventral margin of the hemisphere appears at thebottom. Scale bars 5 200 µm in A; 100 µm in B,D,E, 50 µm in C.


Fig. 5. A–D: Schematic, right-sided transverse hemisectionsthrough the rostral telencephalon from four different zebra finchesshowing the location of injections (solid black areas) of BDA intorostral lMAN shell (A), into the LPO medial to area X (C), and into thelateral NF (D). B: An injection of CTB into area X that spreads

throughout the nucleus (hatched area). a–d: Corresponding schematicchartings of the distribution of retrogradely labeled cells (1 black dot 51 cell) in single, 30-µm-thick hemisections through the rostral wulst(medial is to the left) resulting from the injections shown in A–D. Forabbreviations, see list. Scale bar 5 1 mm.


short latencies (5–10 msec), however, are consistent withan origin or a relay in the Bas and the adjacent NF. In thecurrent study, as in a recent study in pigeons (Deng andWang, 1992), no auditory responses ever were recorded inthe rostral HA or the IHA, and, although such responsescould have been suppressed by anesthesia at two synapsesremoved from the Bas, somatosensory responses in theIHA were very robust, as was found previously under thesame anesthetic regime (Wild, 1997). Furthermore, recent

anatomical investigations suggest that parts of the neo-striatum in close proximity to caudal Bas receive a projec-tion from the principal thalamic somatosensory nucleus,DIVA (Wild, unpublished observations), and, although it isnot known with certainty which body parts are repre-sented in this region, it may be the skin and feathers of theinternal and external auditory meatus. This would suggestthat auditory and adjacent tactile mechanosensory recep-tors are represented in adjacent regions of the Bas-NF

Fig. 6. A–D: Schematic, right-sided transverse hemisections fromfour different zebra finches showing the location of injections of eitherBDA (A) or CTB (B–D) into the hemisphere. The small injection in A iscentered on the NIf. The larger CTB injection in B is centered (solidblack area) on the NIf, L1, and L3, with spread (hatched area) toadjacent regions. In C, the injection covers the HVc and the underlyingshelf. In D, the injection is centered (black area) in the dorsolateralneostriatum, with spread (hatched area) to adjacent regions. In D, a

terminal field resulting from the injection is shown in the dorsolateralpart of the Ai. a–d: Corresponding schematic chartings of the distribu-tion of retrogradely labeled cells (1 black dot 5 1 cell) in single,30-µm-thick, right-sided hemisections through the rostral wulst result-ing from the injections shown in A–D. In a, the short, wavy linesindicate anterograde labeling resulting from the BDA injection shownin A. For abbreviations, see list. Scale bar 5 1 mm.


complex, similar to the situation in budgerigars (Wild etal., 1997).

Basal ganglia and nuclear componentsassociated with the anterior forebrain

pathway for vocal learning

Similar to what is seen in mammals, projections to thestriatal parts of the basal ganglia in birds originate inmany regions of the telencephalon (Veenman et al., 1995),including the HA of the visual wulst (Shimizu et al., 1995)and the HA of the rostral wulst, as confirmed by retrogradetracing in the current study. The projection from therostral HA to the LPO identified here in passerines wasparticularly dense in both males and females. In males,however, the greatest concentration of the projectionssurrounded area X, although area X itself appeared toreceive a rather diffuse projection as well, in part suppliedby fibers that also may have been passing through. This‘‘fibers-of-passage problem’’ makes it difficult if not impos-sible to assess the validity of the HA projections to area Xby using retrograde tracing techniques. A similar caveatholds true for possible HA projections to lMAN. However,HA was found to project unequivocally and densely toparvicellular regions surrounding lMAN, particularly ros-trally, regions that collectively have been called the lMANshell (Johnson et al., 1995). This shell receives a major

input from a ventral/medial part of the thalamic nucleusDLM, the dorsal/lateral part of which projects to lMANcore (Johnson et al., 1995). A core-and-shell organizationalso may characterize the descending inputs to DLM fromthe basal ganglia, with projections to dorsal and lateralparts of DLM originating in g-aminobutyric acidergic(GABAergic) area X neurons (Bottjer et al., 1989; Luo andPerkel, 1999) and projections to other parts of DLMoriginating in GABAergic neurons in parts of the LPO thatsurround area X (Perera et al. 1995; Luo and Perkel, 1999).HA may participate in this core-and-shell projectionalschema to the extent that it innervates the pallidal-likecomponents of area X and the region of LPO surroundingarea X (see Luo and Perkel, 1999).

Although there currently is no direct evidence for theinvolvement of lMAN shell in song learning, the regionoriginally was identified on the basis of age-relatedchanges—increases followed by decreases—in the volumeof anterograde labeling of its DLM afferents, changes thatcorrelate in time with the development of song during thejuvenile period (Johnson and Bottjer, 1992). Because thenumbers of DLM neurons do not change during the sameperiod, it was hypothesized that there must be somechange in the morphology of DLM axons (Johnson andBottjer, 1992). Perhaps the input from HA to lMAN shellhas something to do with this change; however, the

Fig. 7. Photomicrographs of retrogradely labeled cells in the HA.A: Cells in the ventrolateral HA after an injection of CTB into the NIf(lightly counterstained). B: Cells in the ventrolateral HA after aninjection of CTB into the HVc and the HVc shelf (uncounterstained).C: Retrogradely labeled cells in the dorsolateral HA (counterstained)

after an injection of CTB into the dorsolateral caudal hemispheresimilar to that shown in Figure 6D. D: Fiber and terminal labeling inthe ventrolateral HA after an injection of BDA into the lateral NF(darkfield). IHA, hyperstriatum accessorium, pars intercalatus. Scalebars 5 200 µm in A,C; 100 µm in B,D.


possibility of age-related changes in this projection has notbeen explored.

NIf, field L complex, and caudomedialpaleostriatum augmentatum

HA was found to have strong reciprocal links with all ofthese structures in the current study, confirming somesimilar but less extensive observations in the pigeon (Wild,1987; Funke, 1989b). Neurobehavioral (lesion) studies ofthe NIf, electrophysiological recordings of NIf neuronsduring singing, and the NIf connections with the Uva andthe HVc all suggest that the NIf is an important compo-nent of the song system (Nottebohm et al., 1982; Mc-Casland, 1987; Wild, 1994; Okanoya and Hosino, 1998). Itsconnections with the auditory system, however, are moreindirect. Although the NIf is adjacent laterally to theprimary auditory thalamorecipient field L2a and is close toL2a’s flanking laminae (namely, L1 and L3), it does notappear to receive axonal projections from these structures(Fortune and Margoliash, 1992, 1995; Vates et al., 1996).However, it does receive a projection from the caudolateralhyperstriatum ventrale (clHV), which is connected recipro-cally with L1 and L3 and with other parts of the field Lcomplex (Vates et al., 1996). Thus, it is possible thatauditory information of a highly processed nature istransmitted to the HVc through the NIf (Margoliash et al.,1994). On the other hand, Wild (1994) proposed on hodologi-cal, electrophysiological, and comparative grounds thatthe NIf in songbirds was homologous with a somatosen-sory or somatosensory/visual region of the caudomedialneostriatum in pigeons, and this was confirmed in thecurrent study, in which the predominant electrophysiologi-cal response in the NIf was that evoked by somatosensorystimuli, although less robust auditory responses also wererecorded sometimes at the same sites. Thus, somatosen-sory information that is relayed to the NIf may be derivedfrom two sources: HA and Uva (Wild, 1994; current study).In contrast to NIf, L1 and L3 are linked to thalamicauditory inputs more directly and, like the subjacentcaudomedial PA, show ZENK mRNA and protein inductionto presentation of conspecific vocalizations (Bonke et al.,1979; Wild et al., 1993; Mello and Clayton, 1994; Vates etal., 1996; Mello and Ribeiro, 1998). Consequently, L1 andL3 have never been thought of as anything but auditory innature. However, because no auditory responses ever wereobserved in HA or IHA of the rostral wulst, the HAprojections to L1, L3, and PA may convey somatosensoryinformation to these regions. It is of interest in this respectthat cells immunopositive for ZENK protein have beenreported in the rostral HA of the zebra finch, although suchcells are present in birds unstimulated by song play backsand may be located in the visual wulst (Mello and Ribeiro,1998). Their specific location, however, has not been de-picted. In any case, the HA projections to NIf and L1 andL3 suggest that these areas may be sites of audiosomaticconvergence, which would be consistent with observationsof such convergence at midbrain and thalamic levels of theauditory and somatosensory pathways (Wild, 1995; Wildand Williams, unpublished observations; see below). So-matosensation, therefore, may have a role in vocal control(Wild, 1994) that is mediated by the projections of the NIf,L1, and L3 to HVc and the HVc shelf (Fortune andMargoliash, 1995; Vates et al., 1996). What this role maybe is not clear, especially because it appears to involvesensory input from the body rather than from a structure

like the beak, which is obviously involved in vocal produc-tion (Westneat et al., 1993; Suthers et al., 1996; Suthers,1997). Perhaps somatosensory feedback from the body isassociated with the learning and production of characteris-tic movements or postures during vocalization. The projec-tions of the NIf, L1, L3, and PA back onto the HA also maybe involved in the premotor control of these movementsand postures through the pyramidal tract-like projectionsof the HA to the brainstem, cerebellum, and spinal cord(Wild and Williams, unpublished observations).

HVc shelf

Like the regions that have been shown thus far to projectto it (namely, L1, L3, and clHV), the HVc shelf generallyhas been considered to be an auditory region and, again,contains cells in which ZENK mRNA and protein areinduced by hearing conspecific song (Mello and Clayton,1994; Vates et al., 1996; Mello and Ribeiro, 1998). In thecurrent study, we found that there are other inputs to theshelf that may be somatosensory in nature; however, we donot know whether the terminal fields that are supplied bythe HA overlap any of those that are supplied by L1, L3,and clHV. Vates et al. (1996) have suggested that the shelfmay be organized mediolaterally, with inputs from differ-ent sources forming parasagittal slices or slabs. Althoughthis may provide a means for the separation of inputsbiased in favor of either auditory or somatosensory informa-tional content, there was no clear evidence from thecurrent study that was consistent with such an organiza-tion.

The output of the shelf in zebra finches is largely to aregion of the archistriatum that surrounds the RA, aregion that Mello et al. (1998) called the ‘‘auditory archis-triatum.’’ The possibility of somatosensory components ofthis descending projection from the shelf complicates thispicture. The extratelencephalic projections from theperi-RA region in the zebra finch resemble those from aventromedial component of the archistriatum in pigeons,and they are predominantly to peripheral regions of nucleiof the ascending auditory pathway, such as the nucleusovoidalis and the central nucleus of the inferior colliculus(ICC; a.k.a. MLd; Wild et al., 1993; Mello et al., 1998; Wildand Williams, unpublished observations). Again, however,it can be noted that the ‘‘peri-ICC’’ region, which is aspecific target of descending projections from the peri-RAregion, is the same region that receives ascending projec-tions from the dorsal column nuclei and descending projec-tions from the rostral HA (Wild, 1995, 1997; Wild andWilliams, unpublished observations). Moreover, parts ofthese peri-ICC regions project rostrally to regions surround-ing nucleus ovoidalis (Leibler, 1975; Schneider, 1991;Durand et al., 1992; Wild and Williams, unpublishedobservations). Together, these observations illustrate aclose association of somatosensory and auditory projec-tions within both ascending and descending sensory path-ways in the avian brain and call into question any monopo-listic or ‘‘isolationist’’ view of the functional organization ofsensory systems (cf. Stein and Meredith, 1993).

Archistriatum

Whereas the lMAN core projects to the RA (Bottjer et al.,1989), the lMAN shell provides topographically organizedprojections to an arc-shaped region of the archistriatumlateral to RA (Johnson et al., 1995). Johnson et al. calledthis region the archistriatum dorsale (Ad), but we contend


that the true dorsal archistriatum is actually a cytoarchi-tecturally and chemoarchitecturally distinct, narrow re-gion that is situated dorsal to the Ad of Johnson et al. Wetherefore take this opportunity to rename the Ad ofJohnson et al. the archistriatum intermedium (Ai). TheHA is linked to Ai not only by virtue of its dense input tolMAN shell, but it also appears to project directly to Ai,although only to a dorsal and caudal portion. HA alsoappears to project to a caudal portion of RA as well,although neither of these projections was confirmed specifi-cally by retrograde tracing. It is possible that the projec-tion to Ai could be explained by the labeling of collateralaxons of lMAN shell neurons, which may project to bothHA and Ai; however, whether the projection to RA can beexplained in a similar manner cannot be determinedunequivocally from the present data. Some of the cells thatwere labeled retrogradely in the lMAN shell and the HVcshelf after injections into the HA, as shown in Figures2D,E and 3G, were located at the very borders of lMANand HVc, and the processes of these cells sometimesextended into either HVc or lMAN; however, whether it isthese cells that provide the input to RA cannot be deter-mined. Thus, irrespective of whether the projection todorsocaudal RA derives from HA or not, it is a particularlyintriguing issue, because singing in male zebra finches isfollowed by ZENK gene expression, specifically in whatappears to be this same ‘‘dorsal cap’’ or posterior region ofRA (Jin and Clayton, 1997; Jarvis et al., 1998). Thiscorrelation is tantalizing but, so far, is without a functionalrationale.

Although no attempt was made to confirm the putativeHA projection to the ventral archistriatum by retrogradetracing, retrogradely labeled cells were found bilaterally inthe same part of the ventral archistriatum after injectionsof CTB into the HA, indicating reciprocal connectionsbetween the HA and the ventral archistriatum. A similarbilateral projection to the wulst from the ventral archistria-tum was noted by Bagnoli and Burkhalter (1983) in thepigeon.

Dorsolateral caudal neostriatum

This part of the hemisphere has not been implicated inthe song circuitry, nor do we feel it necessarily should besimply because it receives a projection from HA. The visualwulst and auditory and somatosensory parts of the neostria-tum, including the frontal neostriatal regions adjacent tonucleus basalis, also send projections to this generalregion of the dorsolateral hemisphere, probably in allavian species (Bonke et al., 1979; Wild et al., 1985, 1993;Dubbeldam and Visser, 1987; Shimizu et al., 1995; Wildand Farabaugh, 1996). All of these peripherally locatedfields then project in a topographic fashion onto thearchistriatum (see Fig. 6D), which then originates projec-tions to intra- and extratelencephalic targets (Zeier andKarten, 1971; Veenman et al., 1995; Wild and Farabaugh,1996; Davies et al., 1997; Dubbeldam et al., 1997).

Organization of HA projection neurons

The cells of origin of the various extratelencephalicprojections of the so-called septomesencephalic or ‘‘pyrami-dal’’ tract (TSM), including cells projecting to the cerebel-lum, appear to a large extent to be intermixed within deepand medial regions of the rostral HA (Wild and Williams,unpublished observations). The cells of origin of the in-tratelencephalic projections, particularly of those project-

ing to nuclei associated with the auditory and song sys-tems, are concentrated mainly laterally in the HA, althoughthere is considerable overlap with cells of origin of theextratelencephalic projections, especially in more ventralparts of the V-shaped lamina. Cells that project to the NIf,for instance, are located preferentially close to the inputlamina, IHA, and some of those that apparently project toL1 and L3 are located even within IHA, raising the distinctpossibility of direct contacts from somatosensory thalamicafferents. Overall, then, cells of origin of extratelence-phalic projections are concentrated ventrally and medially,whereas cells of origin of intratelencephalic projectionsoccupy more lateral regions and, to some extent, middleand more dorsal regions of HA. Although these somewhatdifferent distributions do not constitute anything like amammalian ‘‘sublaminar’’ organization of cortical outputneurons, they provide the first intimation of some kind ofspatially ordered output of HA neurons in relation totarget nuclei. Thus, although the HA of birds is notintrinsically laminated, it contains neurons that project tomany different parts of the brain, including parts of thedorsal thalamus, and to the spinal cord (Wild and Wil-liams, unpublished observations). In effect, then, the HA isanalogous to layers II–III and V–VI of the mammalianneocortex all rolled into one, although neurons comparablewith layer III that project to the contralateral hemisphereappear to target only the ventral archistriatum and arerelatively few, perhaps because of the lack of a corpuscallosum (see also Shimizu et al., 1995).

CONCLUSIONS

In summary, the present study has defined an extensiveset of projections from the rostral HA to several specificnuclei and regions that have been associated in variousways with either the auditory system and/or the songsystem. Because the principal thalamic input to the rostralwulst is somatosensory, it is possible that somatosensoryinformation also is routed to these nuclei and regions. Thespecific functional consequences of this for audition andvocalization are both unknown and not intuitively obvious.However, the phenomenon of multiple sensory conver-gence in association areas is well documented in mamma-lian cortex (for review, see Stein and Meredith, 1993), inwhich, similar to the superior colliculus, there is spatialregister of single-cell receptive fields of multisensory neu-rons, leading to either enhancement or depression ofresponses, depending on the relative temporal and spatialcongruence of stimuli within those receptive fields (Wal-lace et al., 1992). Thus, the convergence of auditory andsomatosensory inputs in the NIf, L1, and L3, for instance,if present at the level of single neurons, could provide ameans for selectively enhancing responses to stimuli thatcovary in space and time. In addition, because the connec-tions of the HA with intratelencephalic nuclei generallyare reciprocal, and because the HA also is one of the majorsources in the avian telencephalon of projections to extratel-encephalic targets (Reiner and Karten, 1983; Wild andWilliams, unpublished observations), a significant meansis provided thereby for the control of responses that may beassociated with singing and/or its auditory reception.

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