Brain,Behavior and Evolution Editor-in-Chief: R. Glenn Northcutt. La Jolla. Calif. Reprint Publisher: S.Karger AG, Basel Printed in Switzerland Brain Behav Evol 1994:44:247264

Daniel Margoliash" Eric S. Fortune' DistributedRepresentation in the MitchellL. Sutterh AlbertC. Yu' SongSystem of Oscines: B. DavidWren-Hardin'' A. Dave' Evolutionarylmplications and

' Departmentof OrganismalBiology and Anatomy, The University of Chicago, FunctionalConsequences Chicago,Ill.; b Center for Neuroscience, University of Califomia, Davis, Calif.; " Committee on Neurobiology, The University of Chicago,Chicago, Ill., USA

Key Words Abstract Hierarchical This paper reviews the organizationalprinciples and implications that have Parallel emergedfrom the analysisof HVc, a forebrainnucleus that is a major site of sen- Distributed sory, motor, and sensorimotorintegration in the song control systemof oscine Redundant passerinebirds (songbirds). Anatomical, physiological, and behavioral data sup- Sensorimotorintegration port the conclusion that HVc exists within a hierarchically organizedsystem Forebrainevolution with parallelpathways that convergeonto HVc. The organizationof HVc is dis- Bird songsystem tributed and redundant,and its outputsexhibit broad divergence.A similar pat- tern of connectivityexists for neostriatumadjacent to HVc. This and other data supportthe hypothesisthat the song systemarose from an elaborationor dupli- cation of pathways generally present in all birds. Spontaneousand auditory responseactivity is stronglycorrelated throughout HVc, with auditoryresponses exhibiting strongtemporal modulation in a synchronizedfashion throughout the nucleus.This suggeststhat the auditoryrepresentation of songis encodedin the synchronizedtemporal pattems of activation,and that the predominantselectiv- ity for the individual's own songthat is observedfor HVc neuronsresults from interactionsof auditory input with centralpattem generatorsfor song. Most, or all HVc neuronsare recruitedduring singing.The auditory responseand motor recruitmentpropefiies of individual HVc neuronshave no simple relationship, and the spontaneousactivity in HVc may build up in the secondspreceding a song.To the extent HVc participatesin perceptualphenomena associated with song, production and perception are not tightly linked in adults but may be linked by shareddevelopmental processes during periodsof sensorimotorleam- itrg.

Dr. Daniel Margoliash O 1994S. KugerAG, Basel Department of Organismal Biology md Anatomy The University of Chicago 1025E. 57rh St. Chicago, IL 60627 (USA) ture with neuronalfunction. In particular,the nucleusHVcl Abbreviations is a major site of integrationin the song systemwhere sen- A Archistriatum sorimotor transformationsrelated to syllable and song Am Nucleus ambiguus structureprobably occur. This paperwill review recentdata 'Autogenous'song AS demonstratinga distributed,time-domain representation for cDLP Nucleus dorsolateralisposterior thalami pars caudalis song in HVc, including anatomicalobservations, physio- CPGs Central pattern generators recordingsin preparations, physio- DIP Nucleusdorsointermediusposteriorthalami logical anesthetized and DLM Nucleus dorsolateralisanterior thalami, pars medialis logical recordingsand lesion studiesin singing birds. The DLP Nucleus dorsolateralisposterior thalami analysis of HVc's anatomy and physiology has yielded DM Dorsomedial subdivision of nucleus intercollicularis insights into the organizationof episodic behaviors,audi- DMP Nucleusdorsomedialis posterior thalami tory temporalpattem processing,sensorimotor integration, HV Hyperstriatum ventrale the relationshipbetween production and perceptionof IMAN Lateral magnocellular nucleus of the anterior neostriatum and mMAN Medial magnocellular nucleus of the anterior neostriatum song.Additionally, we reinterpretthe forebraincircuitry in N Neostriatum and around HVc from an evolutionary perspective,con- NC Neostriatum caudale cluding that the caudal forebrain componentsof the song NCM Caudomedial neostriatum systemare an elaborationof a systemwhich was probably Nd Dorsal caudal neostriatum present NI Neostriatum intermedium in ancestralforms. NIDL Neostriatumintermediumparsdorsolateralis NIf Nucleus interfacialis HVc within the Contextof the SongControl System NIVL Neostriatumintermediumparsventrolateralis The motor system for song production comprisesdis- nXIIts Nucleusnervihypoglossi,tracheosyringealcomponent crete forebrain, midbrain, and brainstemnuclei that sub- OM Tractus occipitomesencephalicus servea limited setof discreteepisodic behaviors (songs and Ov Nucleusovoidalis RA Nucleus robustus archistriatalis calls) (fig. 1). The HVc is a major site of integrationwithin RAm Nucleus retroambigualis the song system and participatesin the two major song SMS Syllable of maximum synchronization system forebrain pathways. One forebrain pathway in- TCS Temporalcombinationsensitive cludesnucleus interface (NIf), HVc, and the robustnucleus TMS Time of maximal synchronization (RA) in the and Uva Nucleus uvaeformts of the archistriatum caudal telencephalon WTS White+hroated sparrows the caudal subdivision of the posterior thalamic nucleus X Area X (cDLP) in the thalamus- previously called nucleusuvae- formis (Uva); seebelow andWild tl993al - andultimately projectsto the brainstemhypoglossal nucleus, which inner- lntroduetion vates the syrinx, the vocal organ in birds. Lesion and chronic recording experimentsdemonstrate that these nu- The richnessof behavioralphenomena associated with clei are involved in moment-to-momentcontrol of song songleaming, production, and perceptionin oscinepasser- production [Nottebohm et al., 1976, 1982; McCasland, ine birds [seeKroodsma and Miller, 1982] is supportedby 1987;Williams andVicario, 19931.A second,more rostral a richnessof neurobiologicalcomplexity of the song con- pathwayinvolves projections between HVc, areaX (X), the trol system.Although the analysisof songsystem circuitry lateral magnocellularnucleus of the anterior neostriatum at the cellular level is incomplete,for somenuclei there is (MAN), and RA in the telencephalonand the medial divi- now sufficientinformation to besin to relateneuronal struc- sion of the dorsolateralthalamic nucleus (DLM) in the tha- lamus.Lesion studiesdemonstrate X. IMAN. and DLM are not necessaryfor songmaintenance in adult birds, but they 1 TheHVc is anucleus originally identified as ventral caudal hyper- implicate thesenuclei in juvenile song development striatum [Nottebohm et al.,1976] but is now thought to be in the dor- [Bott- sal caudal neostriatum [Nottebohm, 1987]. The suggested revision jer et al., 1984;Scharff and Nottebohm,1991; Sohrabji et 'High (or Higher) Vocal Center' (HVC) retains the acronym for con- a1.,19901. Lesions of the rostralpathway may also result in sistencywith the substantialquantity ofprevious literature but is inad- song degradationin open-endedleamers, such as canaries equatebecause it has funcitonal implications, and becauseit does not (Serinuscanarius), during seasonalperiods of adult song describe the position, shape,or size of the nucleus or its cellular con- stituents.We propose adopting the acronym as the proper name. This development[Nottebohm et al., 1990], or in other species is not inconsistent with old terminology (e.g. field L) nor with some during experimentallyinduced periods of adult song plas- new termhology (e.9. areaX). ticity [Monison and Nottebohm,1993].

248 Margoliash/Fotune/Sutter/YuAVren-Hardin/ Organization of Song System: Dave Functions and Origins I I Telencephalon Fig. 1. Schematic of the song system. I I Arows indicate the direction of major pro- I jections. Subdivisions of nuclei (esp. Ov, Dorsal thalanurs Field L, and RA) are not represented. The Midbrain projectionof RA onto DLM lwild, 1993b]is Brainstem difiicult to confirm with retrograde tracers. RAm Am nXIIts Note HVc is the major site of convergence, /tt and RA is the major output structure [seealso respfatory laryngea-l synnx wild.1994t.

The unidirectional,and mostly unilateralconnectivity of own song than to conspeci{icsongs [seeMargoliash, 1987]. song system nuclei supports a hierarchical organization Such responseselectivity implies hierarchical organization scheme,within which HVc has a specialposition. HVc is and a high degreeofconvergence, organizationalprinciples the major site of convergencein the telencephalon,and it generally observedin auditory systems [e.g. Konishi, l99l; gives rise to two efferentroutes to RA, the major telence- Carr,19921. Furthermore, HVc is a nexus for auditory input phalic output structure(fig 1). One efferentpathway is the to the song system: lesions of HVc abolish auditory song direct projection of HVc caudally and ventrally onto RA selectivity otherwise seenin both of HVc's efferent targets, [Nottebohmet a1.,I976];the secondpathway is the indirect area X and RA fDoupe and Konishi, l99l:' Vicario and projection to RA via the rostral pathway, HVc-+area Yohay, 19931.The concept of a hierarchical organizationin X+DLM -+ IMAN-+RA [Nottebohmet al., 1916, 1982; the song system is also supported by motor properties of Okuhataand Saito, 1987; Bottjer et al., 19891.The indirect HVc. In zebra finches (Taeniopygiaguttata), HVc stimula- 'recursive' pathwayhas alsobeen called lWilliams, 1989; tion during singing causesa re-settingof the pattem of song Nottebohm,19911, however multiple but separateroutes syllables,whereas stimulation in RA affects only the acous- from the samesource (HVc) to the sametarget (RA) does tic structure of the syllable being produced [Vu et al., not constitutea feedbacksystem. More recently Wild 19931. On average, there is a sequential recruitment of U993bl presentedpreliminary evidence that RA may pro- nuclei at the onset of singing, with earliest recruitment of ject to DLM, which would providean anatomicalsubstrate the NIf neurons, followed in order by HVc, RA, and the for possiblefeedback pathways within the forebrain,if not tracheosyringeal subdivision of the hypoglossal nucleus the highly specificform of feedbackimplied by recursion. (nXIIts) lMcCasland, 1987]. This temporal order follows The reinterpretationof nucleusUva as homologousto the the caudal pathway's connectivity. caudaldivision of DLP in non-oscineshighlights a source of multimodal input to the song system,potentially includ- ing proprioceptive feedback fOkuhata and Nottebohm, MultiplePathways through HVc: 19921.Multimodal activity in cDLP, which projects to Gonvergenceand Divergence HVc, may also help to explain visual flash evoked re- sponsesrecorded in HVc [Bischofand Engelage, 1985]. We were interested in characterizing the anatomical or- Physiologicaland behavioral evidence also suggest that ganization of auditory input to HVc because it is an essen- HVc actsas a major integrativesite for sensory,motor, and tial component for an understanding of the physiological sensorimotorprocessing in the song system.The auditory properties of HVc. Neither field L, which was the presump- responseproperties of HVc developduring the sensorimo- tive source of auditory input to HVc, nor HVc itself, had tor phaseof songleaming fVolman, 1993),and it has been been defined in cytoarchitectonic terms. Technically, such hypothesized that HVc neurons are actively involved definitions are needed to determine the extent of tracer during developmentin shapingthe motor programfor song injections and the resulting pattems of labelling. Also, in via auditoryfeedback fMargoliash, l99ll.In adults,audi- the absence of such cytoarchitectonic definitions numerous tory neuronsin HVc are selectivefor the individual bird's authors have adopted a variety of definitions for field L and own song, exhibiting stronger responsesto playback of HVc, which has led to some confusion conceming bound-

4,40 aries,nomenclature, structure, and afferentsof thesenuclei. Afferents of HVc We attemptedto resolve these issues in the zebra finch Our recent experimentsusing fluorescentand biotinyl- [Fortuneand Margoli ash,1992, 1994, unpubl. observ.]. ateddextrans injected into HVc have demonstrateda direct Field L is the primary thalamorecipienttelencephalic projectionof field L into HVc, as well as other connections auditory strucfurein birds, receiving input from ovoidalis [Fortuneand Margoliash, 1994].All projectionswere con- and surroundingareas [Karten, 1968; Bonke et al.,1979a; firmed with anterogradeinjections, although in somecases Kelley andNottebohm,19791. Brauth et a1.,1987;Hdusler, fibers-of-passageprevented final conflrmation.Since struc- 1988;Bell et al., 1989;Wild et al., 1990;Durand et al., tures ventral to HVc also receive inputs from field L (see 1992;Wild et al., 19931.In oscines,we showedthat field L below), it was necessar:yto make some small tracer injec- is a complexof 4 or 5 subdivisions- Ll, L2a,L2b, L3 and tions that were confined to HVc. Injection sites that ap- L, with the distinction betweenLZb andL uncertain[For- pearedto be restrictedto HVc labeled axons within RA; tune and Margoliash, 19921. These subdivisions wrap injections that appearedto encroachupon the neostriatum around and insert into each other in a complex, three- ventral to HVc labeledaxons around as well as within RA. dimensionalorganization. They can be differentiatedby the This finding will be retumedto later. We usedthe distribu- morphology of Nissl stainedcells and arrangementof cell tion of axonsaround RA as a secondcriteria for determin- clusters.Four types of Golgi-stainedneurons occur in field ing the extent of an injection site for our retrogradeexperi- L in the zebrafinch and correspondto those describedfor ments. the Europeanstarling (Sturnus vulgaris) [Saini and Leppel- Field L.Injections of biotinylated dextransrestricted to sack,19811. Types 1 and 2 neurons,which are the largest HVc labeledcells in subdivisionsL1 and L3. Thosecells neuronsin field L, are the major projectionneurons. that filled well enoughto be classifiedwere eithertype 1 or We also showedthat male HVc has 3 cytoarchitectonic type 2 as defined in Golgi material [Fortuneand Margoli- regions,a ventral caudomedialregion with denselypacked ash, 19921.There was no apparenttopography of labeled small and medium-sizedcells, a dorsolateralregion with cells within Ll or L3. Labeled cells were distributed large oriented oblong or ovoid cells and cell clusters ar- throughoutL1 and L3, but more cells were labeled in Ll ranged into rows, and the commonly recognizedcentral than in L3 in all cases.Injections of biotinylated dextrans region with large, darkly staining cells and cell clusters restricted to HVc retrogradelylabeled small numbers of [Fortune and Margoliash, 1994, unpubl. observ.]. The cells in the fleld L complex(< 100),whereas injections of orientedcell region had not beenpreviously described.All fluorescentdextrans restricted to HVc labeled somewhat 3 regions of HVc in males project to area X and to RA, more (> 100). Sincefield L is tonotopically organized(see although the ratio of X-projecting to RA-projecting cells below), the sparselabeling throughoutLl and L3 subdivi- may vary acrossregions. Interestingly, all major cytoarchi- sionsimplies that there is broad convergenceof frequency tectonicfeatures of HVc's subdivisionsmay result from the information onto HVc. We found severaltypes of Golgi- action of hormonesearly in life: a female treatedwith hor- impregnatedaxons within HVc that have broad arboiza- monesearly in life (generouslydonated by M. Konishi) had tions, but none that have small, densespatially-restricted all 3 subdivisions,whereas HVc in untreatedfemales can- arborizationsas would be expectedin a topographically not be subdividedand is distinct from all the male subdivi- organizedprojection. This suggeststhat inputsto HVc pro- sions. ject broadly throughoutHVc. Originally, it was thought that field L projectedto the Nucleus interfacialis.The NIf, which is apposedIoLZa 'shelf' ventral to HVc and that an arearostral and lateralto and L1 near the lateral edge of the field L complex, is a field L projecteddirectly into HVc [Kelley and Nottebohm, cytoarchitectonicallydistinct nucleusthat projectsto HVc l9l9l. That report, however, was basedon an incomplete [Nottebohmet al., 1982]. Restricteddextran injections of cytoarchitectonicdefinition of field L - including L2abfi HVc densely labeled cells throughout NIf [Fortune and probably excluding Ll and L3. Subsequently,the projec- Margoliash,l994l.The projectionof NIf onto HVc alsodid tion of NIf onto HVc was discovered[Nottebohm et al., not appearto be topographic.Small injections into HVc 19821.Since NIf is apposedto Ll and L2a, Nottebohm et labeledfewer cells in NIf than did larger injections,but in al. [1982] postulatedthat the direct projectionsinto HVc all caseslabeled cells were seenthroughout NIf with a scat- from rostrolateralfield L describedby Kelley and Notte- tered distribution. bohm [1979] were the projectionsof NIf and not of field L. Most of the labeled cells in NIf had the morphological Thus, a direct connectionbetween the auditory telencepha- characteristicsof type 5 cells as seen in Golgi material lon and the song systemhad not beenestablished. [Fortuneand Margoliash,1992), which have dendritesre-

250 Margoliash/Fortune/Sutter/YuAVren-Hardin/ Organizationof SongSystem Dave Functionsand Orisins strictedto NIf, but HVc injections also labeledcells along Uva [Fortuneand Margoliash,1994]. If Uva is homologous the rostral border of NIf that had extensive dendritic arbor- to caudalDLP of non-oscinespecies (see below), then the izationsextending into adjacentLl. SuchNIf cells had fusi- areasurounding Uva that projectsto HV may representa form somata,not oblong as is typical for type 5 neurons. sepa.ratesubdivision of DLP. We did not determinethe Thesecells may representa separatemorphological type of positions and possible overlap of the regions of HV that NIf neuron that receivesauditory input from Ll and pro- receivefrom the areasuffounding Uva, that arereciprocally jects to HVc. Thus, Ll may modulate HVc activity indi- connectedwith field L, andthat projectimmediately ventral rectly through NIf. to HVc. All 3, however,are in caudalHV. Neostriatum Ventralto HVc. Caudal to field L and the The Shelf.Some controversy surrounds the deflnition of ectostriatum there is a large, poorly characterizedregion the structureimmediately ventral to HVc, the 'shelf'. The known as the caudal neostriatum (NC). Various names shelf was originally describedas an a.reamedial and poste- have been applied to potentially overlappingparts of this rior to ventral HVc, basedon pattemsof anterogradelabel- region, including Nd (dorsalneostriatum) and NCM (cau- ing in autoradiographsafter injection of tritiated amino domedialneostriatum). This areaincludes neostriatum ven- acids into field L of canaries [Kelley and Nottebohm, 'shelf', tral to HVc, and also includes the which we con- 19791.The shelf asdescribed by cytoarchitecture,however, sider separately(see below). Ventrally located HVc neu- is distinct along the lateral and anterior bordersof ventral rons commonly have dendritesthat extendoutside of HVc, HVc but fades out medially and posteriorly [Fortune and in somecases for hundredsof microns.Thus, axons synaps- Margoliash,1994, unpubl. observ.l. That is, the pattemof ing nearto but not within HVc may be potential sourcesof labeling describedby Kelley and Nottebohm [1979] is not input to HVc. The neostriatumcaudal to the field L com- co-extensivewith the fiber-rich areajust ventral to HVc. It plex and ventral to HVc is auditory [Scheichet al., 1979; is not uncommonin the literatureto find the cytoarchitec- Katz and Gumey, 1981; Miiller and Leppelsack,1985; tonic and hodological definitions of the shelf used inter- Stripling et al., 7994; Margoliash, unpubl. observ.l, and changeably. may form yet anotherpathway for auditory input into HVc. There is also somequestion as to whetherthe shelf pro- Injections restrictedto neostriatumventral to HVc are jects to HVc. In our restricteddextran injections of HVc, difficult to interpret,because with the standarddorsal ap- we did not label any neuronsin the shelf, though we rou- proach the pipette passesthrough HVc, and becausethe tinely labeledmore distantcells in field L, NIf, Uva and the injectionwill intemrpt fibersprojecting tolfrom HVc. In our medial magnocellularnucleus of the anterior neostriatum studies,we comparedthe pattem of labeling of injections (mMAN). The severe flbers-of-passageproblem around restrictedto HVc with the pattem of labeling of injections HVc and appositionof the shelf to HVc makeit particularly that encroachedventrally beyondHVc. We confirmedeach difficult to assessthis putative projection with anterograde putative projection with an injection of complementary labeling from extracellularinjections restricted to the shelf. (anterogradeor retrograde)tracer into the putativeprojection Unfortunately, the intracellular data are also unclear. In target.The datasupport the conclusionthat Ll andL3 of the vivo intracellular labeling showed that the axons of shelf field L complex project onto neostriatumventral to HVc neuronsramify within HVc [Katz and Gumey, 1981], but [Fortuneand Margoliash, 1994].This confirmsKelley and subsequentexperiments using living brain slices, which Nottebohm's |l979l result, although labeling is not re- permit direct visual guidanceof the electrode,showed that stricted to the shelf (see below). Neostriatumventral to axonal arborizationsof shelf neuronsavoid HVc lL. Katz. HVc also receivesinputs from the ventral hyperstriatum reportedin Margoliash,19871. (HV), which is reciprocallyconnected with field L. Field L input to HV is primarily from Ll and L3 [Fortuneand Mar- Intrinsic Connectionsand Outputs goliash,19941, and HV projectionsterminate primarily with- Any injection site that impinged on any of the 3 regions inL2a [Bonke et al., 7979a;Wild et al., 19931.The ventral of HVc labeledcells in all 3 regionsof HVc. We probably hyperstriatumis auditory [Heil and Scheich,1991; Miiller labeledcells via their intrinsic projectionsbecause they are andLeppelsack, 1985; Margoliash, 19861, thus neostriatum by far a larger componentof axons within HVc than are ventral to HVc may receive auditory input from field L HVc's extrinsicprojections. In eachcase there were differ- directly and indirectly from HV. There are severalparallel encesin the distribution of labeledcells in HVc, and there pathways,therefore, whereby field L may influenceHVc. was no consistenttopographical pattem acrosscases. In all Additionally, tracer injections centeredin caudal HV cases,axons were also extensivelylabeled throughout HVc retrogradelylabeled cells in a shelf region that surrounds [seealso Katz andGumey, 1981].This web of connections

251 could support considerablecommunication between all mMAN, NIf, and RA in the forebrain. (The distinction parts of HVc. betweenthe medial and lateral aspectsof MAN may not be Injectionsof anterogradetracers into HVc demonstrated presentin all songbirds.)This set of cytoarchitectonically that the outputsof HVc exhibit massivedivergence. Axons distinct forebrain nuclei has been recognizedonly in the of HVc neuronsramify extensivelythroughout their target oscines,and similar nuclei are not readily visible in subos- sites,either X or RA [Fortuneand Margoliash,1994; Bott- cine brains fNottebohm, 1980; Kroodsma and Konishi, jer et al., 19891.Single axons from HVc extendover large 19911.The relationshipof song systemnuclei to forebrain parts of areaX, giving rise to sparseterminations through- structuresin non-oscinebirds is not well understood. out. Single HVc axons appearto ramify extensivelyonce Parrotsand allies,the other extensively-studiedexample they reachRA, althoughthe extentof the arborsis difflcult of vocal leaming [see also Baptista and Schuchmann, to estimatebecause even small extracellularinjections la- 19901,also have cytoarchitectonicallydistinct forebrain belednumerous axons. The projectionsof HVc onto areaX nuclei related to vocal production.Originally, it was con- andRA did not appearto be topographic[Fortune and Mar- cluded that the similarity in the connectionsof analogous 'HVc' 'RA' goliash, I994l.In contrast,there is someevidence for a top- nucleilabeled and [Patonet al., 1981]implied ographic projection of RA onto the hypoglossalnucleus a similar evolutionary origin for the forebrain structures [Vicario, 1991],and the hypoglossalnucleus has at least involved in vocal control in psittacinesand oscines.This somedegree of myotopic organizationlVicario and Notte- view has been recently challengedby an analysis of the bohm, 19881.This suggeststhat singleHVc axonsgener- budgerigar( M elop sittacus undulatus,) vocal control system, ally contributeto activationof all syringealmuscles. These which showed that many details of budgerigarforebrain data areconsistent with a hierarchicalscheme of organiza- connectionswere different than thosein oscines[Striedter, 'HVc' 'RA' tion of the motor systemfor song. 1994].For example, and of the budgerigardo not receivedirect or indirect input from field L [Hall et al., Summary 1993; Striedter,1994f. These significantdifferences be- In summary,we find a massiveconvergence of inputs tween the vocal control systemin songbirdsand the bud- onto HVc, with multiple parallel pathways including the gerigar has motivated a changein the nomenclatureof the field L complex, NIi cDLP, neostriatumventral to HVc, budgerigarforebrain nuclei away from the implied homol- and intrinsic HVc. Each of these projections may be ogy fStriedter, 1994]. Some elementsof the budgerigar sourcesof auditory input to HVc, and none of theseinputs telencephalicsystem involved in vocal control may be in- appearto be topographicallyorganized. Additionally, the dependentadaptations of non-homologouspathways, while field L projectioninvolves at least2 subdivisionsand 2 cell others may be independentadaptations of homologous typesfrom eachsubdivision, and there is evidencefor 2 cell pathwaysalso used for vocalcontrol by oscines. types in NIf that project onto HVc. These data supporl In our own studies,we notedthat injectionsof HVc that separatelines of inquiry, one regardingthe functional im- includedneostriatum ventral to HVc anterogradelylabeled plications of the convergence/divergenceof information an areasurrounding RA [Fortune and Margoliash, 1994]. flow throughHVc, a secondregarding the evolutionaryori- Injectionsof X (possiblyalso involving tissuesurrounding gins of this pattemof connections.We will addressthe sec- X) retrogradelylabeled cells in neostriatumventral to HVc ond questionfirst. as well as in HVc proper.Thus, the outputsof one or more areasimmediately ventral to HVc areparallel to the outputs of HVc itself. Moreover, we establishedthat field L pro- InterspecificGomparisons: jects both to HVc and areasventral to HVc. The similarity Evolution of the Song System of connectionsof HVc and neostriatumadjacent to HVc raisesthe possibility that HVc aroseas an elaborationor Our recentanatomical studies give someinsight into the duplicationof an ancestralstructure in the caudalneostria- evolution of the songsystem. There is compellingevidence tum that is commonto birds. that vocal leaming hasevolved independently at leastthree times, in the oscines,psittacines, and in some of the hum- Forebrain mingbirds [Nottebohm, 1972]. This implies the song sys- The song systemfollows the generalpattem of reptile- tem aroseas an independentadaptation of oscinepasserine bird forebrainorganization lUlinski and Margoliash, 1990] birds. All oscines apparently have a song system [e.g. and the generalarchitecture for the flow of sensoryinfor- DeVoogd et a1., 19931,including area X, HVc, IMAN, mation in the forebrainof birds. Figure 2 showsthis pattem

252 Margoliash/Fortune/Sutter[uAVren-Hardin/ Organization of Song System: Dave Functions and Origins IHVI { I l I -l l-ruua II

Fig' 2. ComparisonoftheconnectivityofHVc(a),NCadjacenttoHVc(b),andNd/NIVL(c)innon-songbirdspe- cies.a Afferents and efI'erentsof HVc as demonstratedin the zebrafinch. b Afferents and efferentsof NC adjacentto HVc [seeFortune and Margoliash,1994]. Parentheses indicate a regionadiacent to a structure.The dottedline indicates that the (Uva) recipientarea of HV may not be equivalentto the areaof HV that projectsto (HVc). c Connectivityof Nd/NIVL asdemonstrated in non-songbirdspecies (see text). The termsNIVL and NIDL areused exclusively in bud- gengars.

fbr the auditory system by summarizing our recent results not known. There is an overall topography, such that the and those from previous studies of the ascending auditory efferents of the field L complex are medial to the efferents pathways of non-songbirds. This general architecture of the ectostriatum [Ulinski, 1982]. Topography within be_qinswith a projection of a dorsal thalamic sensory nu- each of theseprojections has not been addressed,except the cleus onto a structure between the intemediate and caudal projection of field L onto HVc in zebra finches is non-ropo- neostriatum.This connection in the auditory system is the graphic [Fortune and Margoliash, 1994]. projection of nucleus ovoidalis (Ov) and associatedareas The last projection in this general pathway is from the onto the field L complex [Karten, 1968; Bonke er al., caudal neostriatum onto the archistriatum. In pigeons, the 1919a;Brauth et al., 1987; Durand et al., 19921,and in rhe visual and auditory areas in the caudal neostriatum project visual system it is the projection of rotundus onto the ecto- onto the archistriatum [Shimizu and Karlen, l99la, Wild et striatum [Karten and Hodos, 1970]. The somatosensory al., 19931.In the zebra finch, we have shown that the cau- pathway is not as well described,though the emerging pic- dal neostriatum projects onto the archistriatum [Forlune ture is that DLP, a multisensory nucleus fKorzeniewska and Margoliash.19941. and Giinttrktin, 19901, projects onto a discrete area The HVc, which residesin the caudal neostriatum,is sit- between the field L complex and the ectostriatum fGamlin uated in the middle of this topographical series of projec- and Cohen, 19861. tions, apparently at the junction of all 3 sensory pathways. The second projection in this general pathways is from The visual projections from the ectostriatum are lateral to the neostriatal structure onto the caudal neostriatum. Both HVc, and auditory projections from the field L complex are the field L complex and the ectostriatal complex are known medial and ventral to HVc. Since we expect the somatosen- to project to the dorsal areas of the caudal or lateral neo- sory projections to terminate between the visual and audi- striatum [Bonke et al.,l9]9a; Shimizu and Kar-ten,l99lal. tory projections, HVc may be near these inputs as well. In The projections of the neostriatal somatosensory area are our laboratory, Mr. Peter Bell originally suggested that

253 nucleusUva in zebrafinches had similar position and effer- cies. Wild U993al concludedthat Uva is homologousto entsas did DLP (which is multisensorybut primarily soma- the caudalsubdivision of DLP (cDLP). tosensory)in otherspecies. A Hypothesisfor the Evolution of the SongSystem Uva and DLP Figure 2 showsa comparisonof the pathwaysdescribed We find that the morphology of cells in Uva, and the in this repofi and those seenin previousreports, including relationshipof Uva to other dorsalthalamic nuclei, are sim- those of Bonke et al. ll919al, Kelley and Nottebohm ilar in many respectsto nucleusDLP in pigeons(Columba 19791, Brauth et al. [1987], and Brauth and McHale livia) lseealso Wild, l993al.In pigeons,DLP projectsonto t19881.The primary differencesbetween the patternsseen the intermediateneostriatum [Kitt and Brauth, 1982;Gam- in the zebraflnch and thosein other speciesare the projec- lin and Cohen,19861. A reconstructionof flgure8A-D of tions of mMAN onto HVc, HVc onto areaX, and field L 'cup' Gamlinand Cohen [1986], which showsthe projection area onto a sunoundingRA. In other respects,however, of DLP on the neosftiatum,is similar in shapeto NIf shown the projections are similar. These similarities include the in figure 12 of Fortune and Margoliash [1992]. The area pathwaysfrom DLP through the neostriatum(N) to caudal where DLP fibers terminate is also cytoarchitectonically neostriatum(NC), from Ov to NC through both the field L distinct. The photomicrographof the DLP projection area complex and HV, and the projectionsof dorsalNC and the in pigeons(fig.9,A. of Gamlin and Cohent19861) is similar field L complexonto the archistriatum(A). Thesepathways to the appearanceof NIf shownin figure 4E of Fortuneand are parallel to thoseof the song system(fig.z). Margoliashll992l.In addition,Gamlin and Cohent19861 The songsystem itself is an autapomorphyof the oscine stated that injections of retrogradetracers into HV and passerines[Kroodsma and Konishi, 19911,but the path- more dorsalstructures labeled a few cells in DLP. They did ways that are parallel to the song systemmay be generally not describethe distribution of thesecells, but the result is presentin otherspecies of birds (fig.2).Thesedata suggest not dissimilar to that obtainedfrom injections into HV of the hypothesisthat the song system of oscine passerines the zebrafinch, where cells were labeledalong the dorsal, evolved from pathwaysthat are plesiomorphic - specifl- caudal,and rostral edges ofUva. cally, that HVc and RA evolved as an elaborationor dupli- Korzeniewskaand Giintiirktin [1990] showedthat DLP cation of pathwaysthat are commonto birds [seealso Bre- in pigeonscontains neurons that respondto somatosensory, nowitz, I99Ial. For example,during evolution HVc may visual, and auditory stimuli. If we assumethat Uva is have arisenfrom a subdivisionof caudal neostriatumthat homologousto DLP, then this can help to explain auditory becamecytoarchitectonically distinct with increasedfunc- activity in Uva lOkuhataand Nottebohm, 1992]. The Uva tional specialization,presumably associated with auditory- could be a sourceof auditory input to HVc as well as the feedbackmediated song learning. pathway for the visual responsesin HVc described by The caudal neostriatummay generally exhibit integra- Bischofand Engelage [1985]. tive mechanismsinvolved in perceptualphenomena (for a We have beenunable to determinethe location of DLP relateddiscussion, see Shimizu and Karten [1991b]).This in zebra finches. The position of DLP as shown in the is consistentwith the generalflow of sensoryinformation in Stokeset aI.ll914l canaryatlas is largelyinconsistent with avian forebrains,in which NC receivesinput from primary thatshown in thepigeon atlas fKarten and Hodos, 1967l.In sensoryareas and in turn projectsto archistriatum.Recent the canaryatlas DLP is shown along the dorsal surfaceof experimentssupport this hypothesis,implicating areasof the occipitomesencephalictract (OM). In pigeons, DLP NC other than HVc in conspecificsong recognition in os- doesnot contactOM at all. Stokeset al. ll974l recognized cinebirds [Mello etal.,1992].In pigeons,the outputof Nd, this uncertainty - in their plate 2l DLP is shown in two the part of NC that receivesfrom L1 and L3, projectsonto locations,medial to OM and the dorsalintermediate poste- areasof the archistriatumthat give rise to bilateral projec- rior thalamicnucleus (DIP), and lateralto the dorsalmedial tions to areassurrounding thalamic and midbrain auditory posteriorthalamic nucleus (DMP). In the pigeonatlas, DLP structures[Wild et al., 19931.This suggeststhe hypothesis is lateral and caudalto DIP. In L3.00 of the pigeon atlas, that the ancestralcaudal neostriatal structure that gave rise thereis a dark band which appearsto be markedas DLP in to HVc originally had an auditoryfunction, and that part of the accompanyingline drawing. This dark band is similar the specializationinvolved acquiring projectionsto archi- in appearanceand position to Uva seenin zebra finches. striatuminvolved in motor control. Lastly, Wild [1993a]showed that the afferentsof DLP and Uva areidentical in severalsongbird and non-songbird spe-

254 Margoliash/Fortune/Sutter/YuAVren-Hardin/ Organizationof Song System: Dave Functionsand Origins (a) 20 o (b) c50 o o o .9 .9, (E -vt^ $ cL CL tr tr (,o o Bo O {n o o '=o o '6ieo (E o. CL ct 10 it z z

n- -rF -1.0 "0.s 0.0 0.5 1.0 -0.5 0.0 0.5 1.0 Gonspecificsong selectivity Reversesong selectivity

Fig. 3. Responseselectivity of 329 zebrafinchHVc single units cific songand AS. Note that the averageresponse to conspecificsongs recordedin 24 urethane-anesthetizedbirds. a One or more conspecific is close to the spontaneousrate (0.0); many conspecificsongs elicit - songs and the bird's own song (autogenoussong AS) were pre- overall inhibition. b The responseto forward and reversedAS was sented,resulting in 378 pair-wisecomparisons. Response is definedas comparedfor 99 singleunits. Response is definedas in a. In almostall averagespikes/s over an entiresong minus spontaneousrate. Conspe- cases,forward song elicited a strongerresponse. For both a and b, cific selectivity is the responseto conspecificsong/response to AS. extremevalues are collapsedinto the outermostbins of each graph. For example,selectivity index = 1.0implies salneresponse to conspe- Songswere typically presentedfor I 0 or 20 repetitions.

Selectivityfor AutogenousSong: both with subdivisionand speciesfBonke et al., I9j9b; DistributedRepresentation within A Hierarchy Heil and Scheich, 1985, I99l; Mtiller and Leppelsack, 1985; Miiller and Scheich, 1985; Rijbsamenand Dcjrr- Theunidirectional flow of informationbetween most or scheidt,1986; Lim, 19931.In general,L2a neuronshave all of the forebrain constituents of the song system, the high spontaneousrates and robust responses to tonebursts, position of HVc within those pathways, and the conver- whereasneurons in Ll and L3 have lower spontaneous gence and divergence of information flow through HVc ratesand, in somecases, weak responses to tonebursts [e.g. suggeststhat HVc is relatively high within a sensoryhierar- Bonke et al., I9l9b; Scheichet al., 19791.Neurons of Ll chy and that information within HVc may be organized in a and L3 also tend to exhibit greaterselectivity for species- distributed fashion. The functional realization ofthese ideas specificvocalizations [Leppelsack and Vogt, 1976;Scheich is explored in the next three sections. First, auditory re- et al., 1919;Leppelsack, 1983; Mori and Striedter,19921, sponses in HVc are compared with those in field L. In the which may be based in part on broad tuning curves, re- second and third sections, auditory and motor data are pre- quirementsfor severalspectral peaks, or temporalrequire- sented that provide evidence for a distributed representation ments.Thus, the field L input to HVc is likely ro exhibit for song, and suggest that the distributed representation some specializationfor complex, species-specificsounds, encodes song in the time domain. althoughthe physiology of the neuronsthat project to HVc hasnot beenexplicitly described. Auditory Responses in HVc and in Field L In contrast,there is no evidenceof tonotopic organiza- In severalspecies the projection ofovoidalis onto field L tion in HVc fMargoliash,1987]. The HVc neuronstend to has been shown to be topographic [Bonke et al., \979a; respondpoorly to tonebursts (see below) but areselective 'autogenous' Bigalke-Kunz et al., 1987; Brauth et al., 1987; Bell et al., for the individualbird's song (AS) [Margo- 19891.A tonotopic organization exists for fleld L, varying liash,1986; Margoliash and Konishi, 19851, a propertythat

255 resultsfrom tuning to parametersof AS [Margoliash,1983, TemporalOrder Sensitivity of HVc Auditory Neurons. 1986;Margoliash and Fortune, l992l.In a recentanalysis, Stimulus selectivity can result from spectral specificity, 329 single units in the HVc of 24 wethane-anesthetizedtemporalspecificity, or both. Becausefrequency is mapped zebrafinches were testedwith AS, conspecificsongs, tone in the auditoryperiphery, spectral flltering hasbeen empha- and noisebursts, and other stimuli [D. Margoliashand E.S. sized as a mechanism for achieving selectivity. Recent Fortune,unpubl. observ.l. (The combinationsensitive prop- computationalwork, however, has demonstratedthat an erties of a subsetof these cells has been previously re- auditory neuron's time-domain responseproperty - for ported, where details of the experimentalprocedures are example,the phasic and tonic componentsof response- described;see Margoliashand Fortune tl992l.) The re- can more strongly affect the neuron'sresponse to complex sponsesto conspecificsongs were almost always weaker stimuli (in a least-squared-errorsense) than static parame- than the responsesto AS (fig.3a). The responsesto tone ters of tone burst responsessuch as the frequency tuning bursts were also generally quite weak. For only 13 of 69 curve[Bankes and Margoliash, 1993]. In HVc, thereis evi- neurons was the peak response(30 ms bin) to any tone dencethat analysisin the temporal domain is crucial. For burst strongerthan the peak responseto AS. (Since tone example, HVc neurons systematicallyprefer forward AS burstsare much shorterduration than songs,peak ratesare comparedto reversedAS, two stimuli with different time- a more meaningfulcomparison than averagerates.) If any- varying featuresthat shareidentical overall spectra(fig.3b). thing, the actual distribution is even more skewed, since The song selectiveproperties of HVc units also suggestthe tone burst tuning is not rewarding in HVc and was not importanceof time-domain processing.Most single neu- always attemptedfor weakly respondingcells. Selectivity rons in the HVc of zebrafinches were highly selectivefor for AS may obtain generallyin the HVc of oscinebirds - AS. When the responserate (spikes/s)of the populationof similar results have been obtainedin multiunit recordings HVc single units was correctedfor spontaneousactivity, in white-crownedsparrow s (Zonotrichia leucop hrys) [Mar- the averageresponse to conspecificsongs was near zero, goliashand Konishi, 1985;Margoliash, 19861 and in pre- and many songselicited overall inhibition (fig.3a). If HVc liminary singleunit datain white-throatedsparrows (Zono- contributesto song recognition [e.g. Margoliash, 1986; trichia albicollis)[Margoliash, unpubl. observ.], and multi- Brenowitz, 1991b1,these data suggestthat the temporal unit datain canariesand mockingbirds(Mimus polyglottus) pattem of responseto conspecificsongs, rather than the lMcCaslandand Konishi, 1981]. absolutestrength of response,is likely to be the most salient The selectivityfor AS apparentlyfirst emergesat the level cue for recognition. of HVc - neuronswith comparablepropenies are not recog- Studiesof HVc temporalprocessing have focusedon nizedin field L [Margoliash,1986; Lim, 1993],nor in pre- sensitivity to combinationsof sounds.Temporal combina- liminary datafrom Uva [Okuhataand Nottebohm,1992] or tion sensitive(TCS) neuronshave been described in white- neostriatumventral to HVc [D. Margoliash,unpubl. observ.]. crowned sparrows[Margoliash, 1983] and zebra finches The auditoryresponses of NIf may exhibit somedegree of [Margoliashand Fortune, 1992;Lewicki andDoupe, 19931. songselectivity [M.L. Sutter,A. Dave,and D. Margoliash, In general,non-linear summation of excitationto temporal unpubl. observ.l.The broad distributionof field L neurons sequencesof notes [Sugaet a1.,1978; Margoliash, 1983; thatproject to HVc makethis conclusionparticularly difflcult McKennaet al., 1989;Olsen, 19941 or to spectralcompo- to establishfor field L. In perhapsthe mostdirect comparison nentsof a note [Fuzesseryand Feng, 1982;Langner et al., to date,Margoliash t19861 examined the multiunit properties 1981;Sutter and Schreiner, 1997; Margoliash and Fortune, of both HVc and field L in 3 adult white-crownedsparrows. 19921is a widely recognizedphenomenon in the auditory The HVc recordingsexhibited highly statisticallysignificant systemused to generatehigher-order response properties. strongerresponses for AS comparedto conspecificsongs, In mostcases, combination sensitivity is closelyassociated reversedAS, frequency-shiftedAS, andtwo otherparametric with processingfor species-specificvocalizations. modificationsof AS. Two of the birds had beenreared in the In white-crownedsparrows, all TCS neuronsresponded laboratory;HVc recordingsin thosebirds exhibitedstronger to a sequenceof two syllables but not to either syllable responsesto AS thanto the tutor songs.In contrast,the field when presentedin isolation[Margoliash, 1983]. The TCS L recordingsin the same3 birds with the samestimulus rep- neuronswere highly selective,responding most strongly to erloiresexhibited responses to AS that wereweaker or com- AS, more weakly to other songsfrom the samedialect, and parableto the responsesto other stimuli, with the exception typically not at all to songsfrom other dialectsor to simple 'song- that a weakpreference for forward AS comparedto reversed arlificial stimuli. Thus these neuronswere termed AS wasobserved. specific'. The responseselectivity of song-specificneurons

256 Margoliash/Fortune/Sutter/YuAVren-Hardin/ Organizationof SongSystem: Dave Functionsand Origins was based,in parl, on specificityto parametersof AS. This from releaseof C1 inhibition at the offset of 51 combined was best demonstratedin caseswhere it was possibleto with excitationof C2 by 52 to producesuprathreshold exci- synthesizecomplex artificial soundsthat mimicked the nat- tation of C2. Selectivityfor autogenoussong was proposed ural signal yet permittedparametric modification. In these to result from unspecifiedmechanisms that tunedCl selec- cases,changing the frequencyof either the leading or fol- tively for Sl and tunedC2 selectivelyfor 52. This model iowing element in the sequencereduced the response was one of potentially many that could accountfor all the strength.The TCS neurons were quite insensitiveto the known dynamical properties of TCS neurons in white- durationof the first elementof the sequenceor to the dura- crowned sparrows, especially very broad tuning to the tion of the intervalbetween the elements.In general,these durationof 51 or the intervalbetween 51 and 52, phasic neuronshad long integrationtimes (up to 1 s), longer than responsenear the onset of 52, maintenanceof the TCS field L neuronslSchafer et al., 1992]. property even in caseswhen 51 and 52 are identical, and Recentsingle unit studiesof the zebra finch have con- lack of responseif 51 and 52 were presentedsimultane- firmedand extended these results. In the zebrafinch, approx- ously [Margoliash,1983]. It is notewofihythat the long irnatelyI57o (481329)of the cells were strictly temporal- integrationtimes in HVc precludesthe useof delaylines, as combinationsensitive (TCS), responding with excitationto a hasbeen proposed for TCS neuronsin bats [Kuwabaraand sequenceof soundsbut not to the individual soundspre- Suga,19931. sentedin isolation [Margoliashand Fortune, 1992]. In all Recent intracellular recordings in zebra finch have cases,TCS cellsresponded much more stronglyto AS than extendedthe analysisof temporalorder sensitivityin HVc. to any conspecificsong tested. It shouldbe notedthat the Lewicki and Doupe ll993l presentedpreliminary evidence 'inhibitory-rebound' long periodsof time neededto unambiguouslyestablish the for the modelof Margoliash[1983] as TCS propertysuggests that l5o/ois probablya significant well as for the two other mechanisms.In the 'long-short' underestimateof the sizeof thepopulation. model, long-lastingdepolarization produced by 51 com- Different classesof zebra finch TCS neuronsrequired bined with a shofter-durationdepolarization produced by differenttemporal sequences of songelements. Some neu- 52 to achievesuprathreshold excitation. In the 'burst-firing' ronsrequired a sequenceof 2 parts(notes) of a singlesylla- model,depolarization by 52 produceda burst if preceded ble. Other neuronsrequired a sequenceof 2 discretesyl- by a hyperpolarizingpotential produced by 51; 52 alone lablesof song.Most remarkably,other neurons required a producedfew spikes.Interestingly, the burst-firing model sequenceof 3,4, or in somecases even 5 discretesyllables producesa strongernon-linear response than the two other of AS in the properorder. Additionally, in somecases the models.Below we note that the burstingactivity of HVc TCS responseat a given syllableof song requiredprior neuronsis probablysynchronized throughout HVc. excitation3 or more syllablespreceding the TCS excita- The models of Margoliash [1983] and Lewicki and tion, but the prior excitationitself did not requirea tempo- Doupe ll993l proposepossible mechanismsfor the final ral sequenceof soundelements (i.e., was not TCS). In all (or non-linear)stage of various circuits that exhibit tempo- casestested, the interval betweensyllables could be ex- ral order sensitivity,but they do not explainhow specificity tendedby hundredsof millisecondswithout compromising for syllablesof autogenoussong is achieved.From the per- theTCS response. Thus, there was a broadrange of typesof spectiveof circuit analysisof songleaming, this limitation TCS neuronsin the zebrafinch HVc, with individual neu- implies lack of insight into the neuronalelements modified rons exhibiting integrationtimes of up to I s and up to 5 during songleaming. Each bird singsa different song;HVc syllablesof AS. neuronsare tuned to the parametersof the bird's own song. Moclels of TemporalOrder Sensiriviry.Specific circuit Which elementsof the circuit reflectthe idiosyncraticprop- modelshave beenproposed to explain temporalorder sen- erlies of HVc auditoryneurons? From a modelingperspec* sitivity in HVc. In no small way, these are of interest tive, this limitation is particularly significant in the zebra because they can potentially describe a neural circuit finch, where someHVc TCS neuronsintegrate a sequence directlyinvolved in songlearning. For easeof exposition, of up to 5 complex syllables before exhibiting excitation rve definecell C1 which projectsto cell C2; C2 exhibits [Margoliashand Fortune, 1992]. temporalorder sensitivity to the stimulussequence Sl fol- The logicalextension of the Margoliash[1983] two-cell 'inhibitory- lowed by 52. Margoliash[1983] proposedan model that accommodatesa requirementfor multiple syl- rebound' two-cell model for TCS neurons in white- lables to elicit the TCS responseis to add more cells in crowned sparrowHVc basedon extracellulardata. In that series,with the last cell exhibiting the TCS response.This model,C1 inhibitedC2 suchthat reboundexcitation of C2 is an unattractivesolution because:(1) it is not parsimoni-

25'7 o (b) g, o h w \q o o '*,L .Y ,u dzv (n oo o (E o La (E o 5 'o*B rn o ^ t o o ^oO o10 810 o ",o" o o -; (! o o3oil o o o O. o. a o 0.1 0.2 0.3 0.4 0.5 Normalizedvector strength

Fig.4. Relationships between spontaneous and driven (re- pattem doesnot emergefor low spontaneousrate neurons.b Stimulus sponse)properties of zebra finch HVc single units. The spontaneous is AS, presentedto 293 units. The vector strength (phasicness)of rate is calculated over 30 s of spontaneousactivity (whenever those spontaneous-correctedresponse was calculated over duration of each data were collected) or over 1 s preceding each repetition of AS. syllable. Normalized vector strength is the average of the vector a Spontaneousdata for 267 tnits. The index of bursting measures strengthofresponses to all syllablesweighted by the numberofspikes 'clumping' spike in time: 0 implies equal inter-spikeintervals for all each syllableelicited. Most temporal combinationsensitive neurons spikes; 1 implies all spikesoccurred simultaneously (a limit condi- (seetext) havelow spontaneousrates and respondin a phasicmanner tion). High spontaneousrate neurons tend to be bursty whereasa clear to song.

ous; (2) it predictsthe numbersof TCS neuronsshould go level' temporalfeatures of song.This is consistentwith the down with sequencelength (more 2-syllablethan 3-syllable hierarchicalorganization of the motor systemas judged by TCS neurons,etc.), but the data indicate there are roughly electricalstimulation of HVc and RA during singing [Vu et equal numbersof TCS neuronsin all different classes,and al., 79931.The intrinsic propertiesof these sensorimotor (3) such an extensionstill doesnot predict many other sa- HVc circuits are exhibited, in part, during spontaneous lient featuresof HVc activity. For example,in HVc high bursting. From this perspective,the analysis of TCS and spontaneousrate neurons (>2.5 spikes/s)exhibit a bursting other song-selectiveproperties in HVc relatesto how audi- pattem of spontaneousactivity (fig.4a). When stimulated tory input modulatesCPGs. by AS, these neuronsrespond tonically throughout song Global Synchronyof Spontaneousand Auditory Activity. (fig.ab). In contrast, virtually all TCS neurons are low The propertiesof HVc neuronsare influenced by correlated spontaneousrate neurons(< 2.5 spikes/s);Margoliash and activity observedthroughout HVc. This can be visualized Fortune ll992l). The TCS neuronsmay or may not burst most easily in multiple electrodeexperiments. Simultane- spontaneously(fig.4a), but they almost alwayshave phasic ous recordingsfrom two electrodesdemosntrate that spon- responsesto song (fig.ab). Presumably,phasic TCS neu- taneousbursting in HVc is remarkablysimilar throughout rons derive their responseproperties by convergencefrom the nucleus.For example,figure 5 shows30 s of spontane- the more numeroustonic/bursting neurons. ous activity in two sitesin HVc, separatedby 850 pm that The spontaneousbursting of individual HVc neurons were recordedin a urethane-anesthetizedzebra finch. The reflectsgreater complexity (more time constants)than the pattem of multiunit bursting is highly conelated,although highly regular spontaneousactivity commonly seenin RA not all bursts are well correlated (compare traces at [Mooney, 1992]. One possible interpretationof this com- 14-16 s). This degree of correlationoccurs regularly plexity is in terms of centralpattem generators(CPGs) - throughoutHVc, althoughwe have yet to analyzeit syste- 'higher- HVc neurons participate in circuits that encode matically or at the single unit level.

258 Margoliash/Fortune/Sutter/Yunvren-Hardin/ Organizationof Song System: Dave Functionsand Origins Fig. 5. Correlated spontaneous activity in HVc. Spontaneous activity from two recording sites in HVc separatedby approxi- pm. mately 750 The first 15 s of data are I shown in the top panel,the following 15 s of 15 data are shown in the bottom panel. Note that many bursts of activity occur in synchrony.

The global temporal correlation of spontaneousHVc nousresponse to song.Typically, syllablesof the sametype activity suggeststhat stimulus-drivenactivity might also as the SMS occuning in other motifs elicited much weaker exhibit temporal correlation.This suggestionwas con- responses,and some syllables of different type than the firmed in an investigation of the spatial distribution of SMS elicited strongresponses but only in non-SMSmotifs. extracellularresponses to AS in the HVc of zebrafinches Thus, there was strongand consistenttemporal modulation lsutter and Margoliash,1994]. Within eachof 7 urethane- of the auditory responsethroughout HVc that was not pre- anesthetizedbirds, multiunit and single unit responsesto dicted by any obviouslocal acousticalfeatures. AS were similar acrossthe entire spatialextent of HVc (up The intra-individual similarity of responseproperties to 1.3 mm). This effect was not apparentin an 8th control throughoutHVc providesa logic for examiningthe aggre- bird with recordingsjust outsideof HVc. For eachbird, a gate activity of HVc [Sutter and Margoliash,1994]. A narrow rangeof times elicited the strongestpeak responses measure of the aggregate(population) responseof the (calculatedwith 25 ms bins),called the time of maximum nucleuswas derived by summing multiunit data acrossall synchronization(TMS). Within a bird, 34-75Voof record- recordingsites of eachbird ('groupPSHT' - post-stimulus ing sites exhibitedthe same TMS. The position of the time histogram).The aggregateresponse exhibited phasic TMS was generallyunchanged as the window of integra- excitationat most syllable onsetsand offsets.Additionally, tion was variedfrom 10-150 ms, demonstratingthe TMS a recovery processafter the end of responseto AS was effect wasrobust. Each TMS was associatedwith a syllable observedwith a long inhibitory component.The durationof of maximum synchronization(SMS). The positions of the the recoveryvaried more than an orderof magnitudeacross SMS varied considerablyacross birds. In 4 birds, the SMS individuals (300 ms- 6 s). Featuresof the temporal mod- was in the first motif (a motif is a temporalsequence of syl- ulation of the responsewere relatedto the durationand rel- lablesthat is repeatedone or more times to form a song);in ative strength of the recovery. This implies a long-time 2 birds, the SMS was the introductorynote of song,and in course process across the nucleus helps to shape the I bird the SMS was the secondsyllable of the last (third) responseto AS, and that the durationand magnitudeof the motif. There were no apparentacoustical features of the processvaries from bird to bird. Thus is consistentwith the SMS or the precedingsyllable (morphologicaltype, dura- view that oscillatorsor otherpattem-generating circuits that rion, amplitude)that could accountfor the global synchro- are broadly distributedhelp shapeHVc auditoryresponses.

259 We concludethe auditory representationof song in the uted representationof AS within the level of resolutionof zebra finch HVc is distributed and redundant[Sutter and the lesions. Margoliash, 19941.The pattem of excitationand inhibition Most birds exhibited a downward frequencyshift, but 3 in responseto AS is strongly temporallymodulated, and is of 4 birds with the lowest frequency songs exhibited an globally similar becauseof strong correlation of activity upward shift in frequency.We hypothesizethe population 'drive' acrossHVc. A temporally-encodedrepresentation may pro- activity of HVc provides to RA. Loss of drive vide a useful referenceframework for differencedetection results in lower tension of syringealmuscles (and intemal in relationshipto conspecificsongs or for error detectionin tympaniform membranes),which producesdownward fre- relationshipto auditory feedback. quency shifts when the song is above natural modes of vibration of the syringealintemal tympaniform membrane, The Organizationof HVc during Singing but upward frequencyshifts when songis below the natural Studiesof HVc as a motor structureprovide further evi- modes of membranevibration. This implies a remarkably dencefor distributedrepresenlations in HVc. In one study, simple code - the output of HVc is distributedthroughout we examinedthe effects of small lesions on the songsof the part of RA that projectsto the hypoglossalnucleus, with white-throatedsparrows (WTS) [Hardin and Margoliash, the total output of HVc being a meaningfulparameter. Of 1992, unplbl. observ.l. Songsin white throated sparrows course,many codesthat have time-varying characteristics comprisesimple descendingor ascendingwhistles particu- could exhibit sucha global behavior. larly amenableto detailed analysis, typically three long Some songsof lesionedbirds were distorted.The num- introductorywhistles ('notes') followed by a seriesof short ber of distoted songssignificantly increasedwith the size whistles organizedinto triplets. In the wild, the absolute of the lesion(R'= 0.666, p < 0.01).Distortions were char- frequencyof notes and frequencyratio of successivenotes acterizedas a loss of fine control of the frequencyof whis- is very stableacross songs [Borror and Gunn, 1965;Lem- tles - an increasein frequencyvariability within a whistle. mon andHarris, I974;Hurly et al., 19911.We focusedour Typically, for individual whistlesthe effect was all or none analysison the first three notesof song.Bird's songswere - eithera whistle was distortedor it was not. Although dis- extensivelyrecorded prior to and 6-28 days after lesions, tortions could begin with any of the first 3 notes,with the which were made by small injections of ibotenic acid to exception of 1 bird, the notes following a distorted note minimize damageto fibers-of-passage.The extent of dam- were very likely to also be distorted(p<0.01, binomial agewas calculatedby comparingHVc volumesof lesioned test). The degree of distortion tended to increase in a and control sidesof the brain in transversesections. Birds sequenceof distortednotes. Songs were more likely to ter- submittedto left HVc lesions(size: 2-100Va,n= 14),right minate with distortednotes. Thus, the temporal dynamics HVc lesions(size:29*79Va,n= 3; this speciesis left later- of the population of HVc neurons is resistantto loss of alized ll-emmon [1973]), and 3 controls spared HVc. large parts of the population, but once an abnormal Lesionsfrom < 267oof HVc (13 birds total) producedper- dynamic stateis achieved,the systemhas difficulty recov- manenteffects including a changein the frequencyof song; ering. The abnormalstate increases the probability of com- lesions of I07o or smaller (4 birds) producedonly tempo- plete loss of coordination. Such behavior would be ex- rary effects,or no effects.Postoperatively, the variability in pectedfrom a systemthat achievesand maintainsits popu- the duration of notes also increased,although the mean lation dynamicsthrough a high degreeof correlatedactiv- durationsdid not change. ity, althoughother explanationscannot be ruled out. With a single exception (a bird singing an abnormal song),birds sangall notesof song after the lesions.In2 of 13 birds with permanentfrequency shifts, all notesof songs The BehavioralSignificance of Auditory were equally effected,and in 11 of 13 birds there were sig- Responsesin HVc: Funetionaland Evolutionary nificant changesin the frequencyratios of successivenotes Links Between Production and Perception (p < 0.01). The magnitudeof frequencyshift for eachof the first three notes of song was strongly (and signiflcantly) In the previoussection we describedthe organizationof positively correlatedwith the size of the lesion. Different HVc, concluding that there is a distributedrepresentation parts of song were not affecteddifferently by the location for songboth for auditory and motor states,that this repre- of lesionswithin HVc, althougha unique effect of medio- sentationis redundaht (similar throughout), and that the caudal lesions on the initial note of song cannot be ruled principal code for song is in the temporal rather than the out. This suite of observationsis consistentwith a distrib- spatialorganization of neuronalactivation. In this final sec-

260 Margoliash/Fortune/Sutter/YuAVren-Hardin/ Organizationof Song System: Dave Functionsand Orieins tion 'uveexamine some of the implications of auditory form of that linkage. In humans,a motor theory of speech responsesin HVc. perception generally assefis that the articulatory mecha- nisms recruitedduring speechproduction are alsorecruited Tlrc Process of Song Perception during the perceptionof like speech,with the pattem of The HVc auditory neurons exhibit exquisite selectivity recruitement being similar if in a somewhat vaguely tbr the individual bird's own song - the one song the bird definedfashion [Libermanet al., 796]; Liberman and Mat- i: most unlikely to hear a neighbor sing. Auditory activity tingly, 19851.A parallelmotor theory of songperception in HVc is inhibited during singing [McCasland and Koni- has beenproposed based on the claim that playbackof dif- shi. 19811,and in any case most adult birds do not rely on ferenttypes of songcomponents selectively activates pools auditory feedback to maintain song [Konishi, 1965; Notte- of motor neurons in different parls of the hypoglossal bolrrn, 1980; Marler and Sherman,1982: Price, 1979; Nor- nucleus[Williams and Nottebohm,1985]. That observa- deen and Nordeen, 19921.What then is the functional role tion, however,results from a very small dataset for a map- of highly selective auditory responsesin the adult HVc? ping study (14 recordingsin 4 animals).It is difficult to Birds can recognize individuals on the basis of song alone understandhow a topographic arrangementof syllables [Falls, 1982]. In almost every speciestested to date, the basedon acousticsis consistentwith the myotopicorgan- bird's own song has a special statusas an external stimulus, izat\onof the hypoglossalnucleus fVicario andNottebohm, releasing a level of territorial behavior that is intermediate 19881,especially when there is evidencethat at leastsome between the effects of establishedneighbors and unknown syringealmuscles are involved in producingmost syllables conspeciflc strangers[e.g. Brooks and Falls, 1975; McAr- of song [Vicario, 1990].Also, to datethere is no known thur. 1986; see Falls, 19821. In playback experiments in pathwaythat leadsfrom the hypoglossalnucleus back into specieswith reperloiresof different song types, individuals the brain, as would be requiredfor auditory-relatedactivity n.ratchsong type most consistently when challenged with in the hypoglossalnucleus to haveperceptual significance. one of their own songs, a behavior thought to increase An alternativeview of the relationshipbetween produc- information exchange between singers [e.g., Falls et al., tion and perceptionarises from considerationsof song 1982; Falls, 19851.These data support the hypothesis that learning. During development,HVc auditory response adult songbirds perceive conspecific songs by comparing propertiesare shapedduring motor leaming fVolman, 'reference' them to an internal of their own songs or other 19931;this resulthad beenpredicted and hypothesizedto known songs [Morton, 1982]. Further evidence to suppol-t contributeto the processof matchingthe memorizedsong this hypothesis exists in the form of playback experiments model with auditory feedbackduring the trial-and-error rvith acoustically degraded songs. Birds distinguished bet- phaseof songdevelopment [Margoliash, 1987]. How does ter between degraded and undegraded songs when they auditoryfeedback become decoupled from singingduring were familiar with those songs than when the songs were development?In a recentset of experiments[Yu and Mar- novel [McGregor et al., 1983; McGregor and Falls, 1984; goliash,1992,1993, and unpubl. obseru.l, we wereable to McGregor and Krebs, 19841. achievedirect recording of multipleand single HVc unitsin With these considerations in mind, Margoliash [1986, singing zebra finches,which is technically challenging 19871proposed that the representationof AS in HVc acts as becauseof the small size of songbirdsand becauseof a referenceagainst which conspecilic songs are compared. movementartifacts during singing. In our smallsample (11 Support for a role of HVc in song recognition has come multiunit clustersand 13 singleunits extracted using spike fiom a few laboratory studies that show adverse effects on waveformclassification techniques recorded from 8 sitesin discrimination following HVc lesions [Nottebohm et al., 7 birds), the neuronal recruitment PSTHs when the bird 1990; Brenowitz, I99lbl. In general, these effects are not sang its song were completelydifferent from the auditory strong or the results are somewhat ambiguous; for example, responsePSTHs when the bird heard its song. In many the lesions of female canary HVc that resulted in loss of cases the change from auditory to motor properlies discrimination between conspecific and heterospecific occurredover a periodof about5 s prior to singing,during 'spontaneous' songs fBrenowitz, l99lb] may have also involved more which the rates of neuronsincreased by rnedial aspectsof NC. Thus, the role for HVc in song per- 5-10x. This suggeststhat auditoryand motor systemsact ception has not been well established. over different spatiotemporalregimes of neuronalpopula- If the motor system for song production is also involved tions - havedifferent statepropefiies. This is not consistent in song perception then this demonstrates a linkage be- with the suggestionthat a linkage betweenproduction and tu'een production and perception but does not explain the perceptionof song results from closely related states[cf.

261 Nottebohmet al., 19901.Rather, production and perception Acknowledgments may sharedevelopmental processes and thus exhibit link- The work reviewed here was supported in part by grants from the agesin the adult 1987]. In this schemesuch fMargoliash, NIH (NS25677), rhe NSF (IBN-930977l), and the Whitehall Founda- linkagesresult only from sharedchanges during periodsof tion (M9l-03), M.L.S. was supported by NIH NRSA (l F32 songleaming. DC00075), and A.C.Y. was supported by NIH NRSA (1 F31 MH1015r).

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264 Margoliash/Fortune/Sutter/YuAVren-Hardin/ Organization of Song System: Dave Functions and Origins