Three Models of Song Learning: Evidence from Behavior

Peter Marler Department of Neurobiology, Physiology, and Behavior, University of California, Davis, Davis, California 95616

Received 18 June 1997; accepted 2 July 1997

ABSTRACT: Research on avian song learning widespread ocurrence of species-speci®c song univer- has traditionally been based on an instructional sals that are recognized innately but fail to develop model, as exempli®ed by the sensorimotor model of in songs of social isolates. A third model combines song development. Several large-scale, species-wide instruction, in the memorization phase, with selection ®eld studies of learned birdsongs have revealed that during song production. An overproduced repertoire variation is narrowly restricted to certain aspects of of plastic songs previously memorized by instruction song structure. Other aspects are suf®ciently stereo- is winnowed by selection imposed during social inter- typed and so widely shared by species' members that actions at the time of adult song crystallization. Selec- they qualify as species-speci®c universals. The limita- tion during production is well established as a factor tions on natural song variation are dif®cult to recon- in the song development of several species, in the form cile with a fully open, instructive model of song learn- of action-based learning. The possible role of selective ing. An alternative model based on memorization by processes in song memorization meritsfurther selection postulates a system of innate neural tem- neurobiological investigation. ᭧ 1997 John Wiley & Sons, plates that facilitate the recognition and rapid memo- Inc. J Neurobiol 33: 501±516, 1997 rization of conspeci®c song patterns. Behavioral evi- Keywords: birdsong learning; instruction-based learn- dence compatible with this model includes learning ing; learning preferences; selection-based learning; preferences, rapid conspeci®c song learning, and song memorization

INTRODUCTION with a contradiction that threatens to undermine the principles upon which many current investigations Studies of the physiological basis of song learning are based. The nature and extent of variation in in birds have traditionally been dominated by what some natural birdsongs proves to be quite limited, is essentially an instructive model. This is the so- to a degree that it is hardly compatible with viewing called ``sensorimotor model'' of vocal learning, song learning as an open process. with song acquisition followed after some interval The basic case for the dependence of oscine song by retrieval and production of memorized songs, development on learning remains unchallenged. all proceeding with relatively few constraints aside Species after species of songbird has been shown from the obvious physical limitations on sensory to develop abnormal song when deprived of the processing and sound production. Over the past de- opportunity while young to learn from older birds cade, however, students of song variation under nat- (Kroodsma and Miller, 1982, 1996; Catchpole and ural conditions have become increasingly concerned Slater, 1995). The ubiquity of geographical song traditions, often so restricted and so well de®ned that we do not hesitate to identify them as local Contract grant sponsor: PHS; contract grant number: dialects, speaks to the pervasive role of learning in MH14651 avian vocal development (Baptista, 1976; Baptista ᭧ 1997 John Wiley & Sons, Inc. CCC 0022-3034/97/050501-16 and King, 1980; Baker and Cunningham, 1985). 501

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Learned bird songs are highly individualistic, so that phenomenon. This may require us to reexamine the with experience birds and bird watchers alike use principles upon which theories of song learning are them for personal identi®cation. The fact that an based. It is in this spirit that the following specula- individual can readily be taught to sing a nonnatal tive review of three alternative models of the song- dialect given tutoring at the appropriate phase of learning process is cast: one based on instruction, development (e.g., Petrinovitch, 1985), and even the second on selection, and the third a hybrid model songs of other species in some cases (e.g., Baptista incorporating elements of both. and Morton, 1981), favors a view of song learning as relatively free of constraints. The importance of learning in songbird vocal MODEL 1: LEARNING BY development is thus unquestioned, and the ®ndings INSTRUCTION: THE SENSORIMOTOR of a large and burgeoning body of researchers on MODEL many aspects of the neural basis of vocal plasticity attest to the validity of this conclusion. But now The widely used sensorimotor model, primarily in- comes the paradox. As ornithologists have painstak- structive in nature (e.g., Konishi, 1965, 1985; Bott- ingly documented geographic variation in the songs jer and Arnold, 1986; Nottebohm, 1993), originated of different oscines throughout the species range, with studies of local dialects and effects of deafen- ®rst impressions of almost endless variability in ing on song learning in the white-crowned sparrow acoustic morphology have proved to be deceptive. (Marler and Tamura, 1962, 1964; Konishi, 1965). Careful analysis has repeatedly revealed a limited The songs that males develop when raised in social repertoire of notes, syllables, and patterns from isolation are abnormal, lacking any trace of the which all songs of a given species are constructed. home dialect. Any dialect, natal or alien, can be Each species has its own distinctive set of relatively instated by playing tape recordings to a male during stable core attributes. The attributes that qualify as the sensitive period for song acquisition, originally universals vary with the taxon, focused sometimes de®ned in this species as between 10 and 50 days in phonology, sometimes in syntax. In birdsongs in of age. Recent work shows that the sensitive period which the major species universals are phonologi- usually begins later than originally thought, around cal, variability is greater in such features as the 20 days, and peaks in the next 30 days, with some order in which different syllable or note types are acquisition possible later, up to 100 or 150 days. sequenced, the intonation with which they are ut- Tape and live tutoring yield similar results (Marler, tered, the subset of the note type lexicon used, or 1970; Baptista and Petrinovitch, 1986; Nelson, aspects of syntax, rather than in the basic, categori- 1997). The timing of the peak can vary by up to a cal structure of the phonological core elements. month in different populations (Nelson et al., Where the dominant universals lie in the syntactical 1995). domain there are more degrees of freedom in song Songs are memorized at this time, and production phonology, as is well illustrated by birds that mimic of imitations usually begins some weeks or months other species, such as members of the mockingbird later. Exposure to song is unnecessary at this time; family. song development is guided by memory, proceeding Thus, far from displaying the almost unlimited by reference to an acquired auditory template (Ko- variability often assumed, variation in certain as- nishi, 1965; Marler, 1976). The work of Konishi pects of learned bird songs as heard in nature is on effects of deafening on song development dem- highly constrained. These limitations are at odds onstrated the crucial role of auditory feedback for with the traditional sensorimotor view of song learn- conversion of memorized song into produced song. ing. Given the uncertainties of copy error, the likeli- Early-deafened males of a variety of species pro- hood of drift as song patterns are passed from gener- duced highly abnormal songs (e.g., Konishi, 1964, ation to generation, and perturbations of the trans- 1965; Dittus and Lemon, 1970; Price, 1979; Marler mission process by intergenerational changes in the and Waser, 1977; Marler and Sherman, 1985), and acoustic environment in which songs are learned, it in the white-crowned sparrow, males deafened is unlikely that any aspects of song structure would when young produced the same highly degraded remain uniform over time throughout an entire spe- song whether they were deafened before song train- cies range if song learning were a fully open pro- ing or after song training but before song production cess. Yet, the existence of species-speci®c core fea- (Konishi, 1965). As production proceeds, auditory tures in learned bird songs is now well-enough doc- feedback becomes less important for the mainte- umented to suggest that it may be a universal nance of song structure after a certain degree of

/ 8p2d$$1890 09-15-97 17:38:50 nbioa W: Neurobio1890 Three Models of Song Learning 503 pro®ciency has been accomplished (Nottebohm, Jerne, 1967; Changeux et al., 1984) and especially 1966, 1968). Late deafening had less effect on the championed in a series of important publications by song of mature males, although recent studies may Edelman (1978, 1981, 1987). Selective learning has require some revision of this judgment (Nordeen already been invoked as a factor in song develop- and Nordeen, 1992). The effects of deafening and ment, imposed at a late stage during the winnowing the separation in time of memorization and produc- of imitations of songs acquired in an earlier, instruc- tion (Marler and Tamura, 1964; Konishi, 1965) lead tive phase (Marler and Peters, 1982; Nelson, 1992; to the widely accepted ``sensorimotor model'' of Marler and Nelson, 1993; Nelson and Marler, song learning. 1994). The present model extends the notion of An issue that is unaddressed by this model, and selection to earlier stages of the learning process and by most behavioral and neurobiological studies that assumes that extensive pre-encoding of information have been guided by it, is the degree to which song- about species-speci®c song structure embodied in birds possess foreknowledge about the song of their innately speci®ed brain circuitry provides the basis species. Despite the existence of learning prefer- for the initial process of song memorization. Audi- ences in young male songbirds, especially as em- tory experience is assumed to operate on this preor- bodied in so-called ``innate song templates'' (Koni- dained circuitry in a selective fashion, either directly shi, 1965; Marler and Sherman, 1983), the most or indirectly, so that some subset of the innate common view is that the songbird brain will partici- knowledge that it encodes becomes committed to pate in learning and reproducing virtually any song the future guidance of motor development by audi- that the bird can be persuaded to memorize, within tory feedback. the limitations of its vocal apparatus. This view is The key component in the model is a set of audi- reinforced by the ease with which birds that are tory mechanisms that collectively display highly se- mimics can imitate a huge variety of animate and lective responsiveness to sounds heard during the inanimate sounds, and the fact that even nonhabitual sensitive period for song memorization. These mimics will memorize and reproduce songs of other mechanisms are viewed as operating in parallel to species under certain conditions. In practice, the the auditory pathways normally used for receiving sensorimotor model has usually been viewed as in- and processing sound which are not normally em- structive in nature, with the underlying assumption, ployed in song learning although they can be under either explicit or implicit, that birds know little or certain conditions, as when an alien song is learned. nothing about their species song until appropriate Instead, song memorization is viewed as normally auditory instructions have been received. engaging a song-speci®c pathway especially dedi- cated to the detection and recognition of conspeci®c song and preferential commitment of the songs MODEL 2: LEARNING BASED heard to memory. As conceptualized, two kinds of ON SELECTION functionally distinct mechanisms operate in this song-speci®c pathway, with rather different roles in An alternative to the common assumption that prior development. Both are de®ned as templates, serving to auditory experience of song, oscine brains are initially for the selective ®ltration of incoming audi- relatively uninformed about the structure of their tory stimuli, emphasizing some sounds over others, species song, is to assume that the naive songbird and ensuring that they receive the subjects' full at- brain has extensive foreknowledge about the natural tention. The templates encode suf®cient information song patterns of its species. Instead of modeling the to detect conspeci®c songs and distinguish them process of song acquisition as if it were based on from other sounds with which they might be con- instruction, an alternative is to invoke a process of fused in nature, especially other birdsongs. The selection, operating on preexisting circuitry. Efforts properties of this song recognition circuitry are in- to develop a model of this nature, proceeding nately pre-encoded, serving to detect the set of through several iterations (e.g., Marler, 1984), most acoustic universals that characterizes the normal recently by Marler and Nelson (1992), have placed singing behavior of each species. Some of these primary emphasis on the existence of species-spe- characteristics are panspeci®c, such as the con- ci®c universals in natural birdsongs and on the fail- trolled tonality that is characteristic of so many bird- ure of many of these universals to develop in songs songs. Others are species speci®c, de®ning the set of birds raised in social isolation. of features that is unique to and shared by all species The concept of selective learning mechanisms members. These include such features as spectral is well entrenched in neurobiological theory (e.g., structure and the patterns of amplitude and fre-

/ 8p2d$$1890 09-15-97 17:38:50 nbioa W: Neurobio1890 504 Marler quency modulation that collectively de®ne song its natural environment. They sensitize the bird to phonology, and the temporal features that make up the subset of sounds most important to it from the the typical syntactical patterns of the species song. viewpoint of song development: namely, the song Templates of two developmental forms are pos- patterns of its own species. Other sounds are less tulated: latent templates and preactive templates, potent in capturing the bird's attention but are not distinguished by the spontaneity of their activation. excluded from its awareness. In certain circum- The initial patterns of selective responsiveness of stances, as is typical of mimics such as mocking- both are under genetic control. Preactive templates birds and starlings, sounds of other species may become available at a certain stage of development bypass or override the song-speci®c pathway, as for the bird's use by auditory feedback, activated will be discussed later. Most songbirds do not mimic as a function of normal processes of growth and in nature, however, focusing their song-learning development. If, for example, a bird is raised in abilities preferentially on members of their own spe- isolation with no song stimulation, preactive tem- cies. The template system is viewed as the primary plates will guide its song development. They will mechanism for achieving that focus. In special situa- specify certain phonological and/or syntactical fea- tions, as when raised without access to conspeci®c tures of the species song, becoming available to song or with a heterospeci®c live tutor, even birds guide the motor development of song. They thus that do not customarily mimic will learn songs of coincide with what were previously de®ned as in- other species, and there are records of this occurring nate song templates (Konishi, 1965). How these even when conspeci®c song is accessible, especially templates become preactive is not clear. They may under conditions of very high arousal. In these be activated endogenously in the course of matura- cases, it is postulated that processing will be medi- tion, or early self-stimulation may be required, as ated by general auditory mechanisms, and not by by the bird's own nestling or ¯edgling calls. The the song-speci®c pathway. The second function of diagnostic feature of preactive templates is that the template system is to participate in the commit- stimulation by another individual is not required for ment of songs to memory. Once memorized, the them to participate in the motor development of information is of value in later life in many ways: song by auditory feedback. not only in guidance of the bird's own song develop- Latent templates, on the other hand, require acti- ment but also in the perceptual processing of the vation by speci®c auditory stimuli before exerting songs of others. The third function that the template an in¯uence on motor development. The process of system serves is to guide the motor development of activation by sounds matched to their own set of the bird's own song repertoire. innate phonological and/or syntactical speci®ca- tions also facilitates the commitment of those same sounds to memory. Thus, both preactive and latent Behavioral Evidence Supportive templates contribute to the process of song memori- of a Neuroselective Model zation and later, to motor development. Once acti- vated by auditory stimulation that satis®es their in- Four main lines of behavioral evidence are consis- put criteria, latent templates acquire the potential tent with the hypothesis that selective processes play that preactive templates already possess to in¯uence a role in the normal process of conspeci®c song subsequent motor development by auditory feed- learning. First is the fact that remarkably few audi- back. Without effective stimulation, latent templates tory experiences of song are suf®cient for the mem- may never exert an overt effect on behavior, or they orization of conspeci®c song to occur. Second, there may participate in the perceptual processing of the are learning preferences, typically with a bias fa- songs of others. voring conspeci®c songs. Third, large-scale analy- ses of song variation have repeatedly revealed the Functions of the Template System existence of acoustic universals. These recur in the natural singing behavior of all species members, From a behavioral point of view, song templates as often unique to a species within a given songbird conceptualized serve three primary functions. First, community. The fourth and ®nal point is that many they sensitize the young bird to certain patterns of of these universals fail to develop in males reared auditory stimulation from the environment, provid- in social isolation, and even more are lacking from ing a basis for selective responsiveness in the face the songs of early-deafened birds. These various of the enormous variety of audible but biologically lines of circumstantial evidence are consistent with irrelevant sounds that the young organism hears in a neuroselective model of song memorization.

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A Few Experiences Are Often Adequate well as being given priority in guiding subsequent for Learning song development.

In the ®eld it is impossible to determine the number of heard songs necessary for normal development. Learning Preferences In laboratory studies, it is common to expose birds W. H. Thorpe (1958, 1961) was one of the ®rst to to hundreds or even thousands of repetitions of song deduce that song learning preferences must exist. If models, either from tape recordings or from live songbirds learn to sing, and yet for the most part tutors. Such experiments are designed to optimize rarely copy sounds of other species, mechanisms the likelihood that learning will take place and do must exist to impose selectivity on the learning pro- not usually specify how few song stimuli are suf®- cess. Thorpe demonstrated that captive chaf®nches, cient. But in some cases, we have evidence of the Fringilla coelebs, failed to learn several kinds of minimum number of experiences of a song type arti®cial songs and tape recordings. It is hard to necessary for its memorization and imitation, and be sure whether this failure resulted from active the number is sometimes surprisingly small. A male rejection or from de®ciencies in the training para- white-crowned sparrow learned from 120 repeti- digm. Learning of other, more acceptable models tions of a song type over a 20-day period (Petrinov- offered in a choice situation would have rati®ed the ich, 1985). Three European blackbirds (Turdus training procedure. Also, as in most other song- merula) each learned one song motif from a range learning studies, because evidence for or against of 12±50 presentations on a single day (Thielcke- acquisition was drawn from analyses of the songs, Poltz and Thielcke, 1960). At the peak of his sensi- a role for motor constraints in selectivity cannot be tive period for acquiring tape-recorded songs, a excluded. There are hints from some of Thorpe's male song sparrow learned parts of a taped song classic experiments that motor limitations may in- from 30 exposures in 5 min on a single day (Peters deed play a role, as though the vocal apparatus can et al., 1992). The most remarkable case comes from cope more easily with conspeci®c songs than with studies of song learning in the nightingale (Luscinia other sounds. One male chaf®nch that learned ele- megarhynchos) (Hultsch and Todt, 1989; Todt et ments of a tree pipit song (Anthus trivialis), chosen al., 1979). Four males faithfully copied a string of because it bears some resemblance to chaf®nch 12 different song types presented once per day for song, eventually discarded them and reverted to ``a 15 days. In another group, one male acquired 90% modi®ed version of its innate or Kaspar Hauser of a string of 21 song types presented twice per day song'' (Thorpe, 1958). Similarly, one male chaf- for 5 days. Thus, each song type was heard only 10 ®nch exposed to canary song when young produced times. In another experiment, one male learned an canary imitations in its plastic song, but discon- entire string of 60 song types heard only once per tinued them at the time of song crystallization day for 20 days. This bird not only memorized the (Thorpe, 1958). Thorpe invoked sensory predispo- 60 song types, but also acquired much information sitions as an explanation, but it is equally possible about the order in which they were presented in the that production constraints were responsible for this training program. rejection of heterospeci®c material late in the pro- There are indications from the avicultural litera- cess of motor development. ture that rapid and precise memorization of a few A similar result was obtained with the swamp song stimuli is a special feature of conspeci®c song sparrow (Melospiza georgiana) (Marler and Pe- learning. Lore among bird fanciers has it that a bird ters, 1977, 1982). Male swamp sparrows nor- raised in a mixed-species aviary in isolation from mally reject song sparrow songs as models for members of its species, normally destined to learn vocal learning, but by experimenting with syn- eventually from its companions, requires only brief thetic songs in which phonological and syntactical exposure to conspeci®c song for it to be learned to cues were independently varied (review in Marler the exclusion of other species (see Huxley, 1942, and Peters, 1989), swamp sparrows were induced for examples). Again, few experiences are often to learn some song sparrow material. By follow- suf®cient. These remarkable feats of rapid memori- ing song development closely, it was possible to zation of complex sound patterns hint at special capture the ®rst efforts at imitation in plastic song auditory processing brought to bear on the task of of 34 swamp sparrows exposed to simple repeti- song learning. Song stimuli matching the speci®ca- tive swamp-sparrow-like trills that consisted ei- tions of both preactive and latent templates may ther of swamp sparrow (474) or song sparrow be memorized especially quickly and accurately, as syllables (458). At this stage, they sang 116 imi-

/ 8p2d$$1890 09-15-97 17:38:50 nbioa W: Neurobio1890 506 Marler tations of swamp sparrow syllables and 34 imita- sible for the learning preferences that the birds dis- tions of song sparrow syllables, but when their play (Marler and Peters, 1987, 1988, 1989). Evi- overproduced plastic song repertoires crystal- dently, song-learning preferences are innate. As al- lized, they still discarded more of the song spar- ready indicated, however, analyses of the attrition row syllables (91%) than of the swamp sparrow and crystallization of plastic songs suggests that mo- syllables (59%). Again, rejection of heterospec- tor constraints may contribute to the favoring of i®c song material in late stages of motor develop- conspeci®c song. Thus, ®nal proof of purely sensory ment suggests that the vocal circuitry and appara- contributions to song recognition and memorization tus of these swamp sparrows were more comfort- as a basis for selective learning remained elusive. able reproducing conspeci®c than heterospeci®c The need for learning preference tests that are songs. independent of the production of imitations led to Thorpe may also have been premature in con- several new approaches. Dooling and Searcy (1980) cluding from his chaf®nch experiments that ``the developed a cardiac measure of the responsiveness chaf®nch has the inborn blueprint conferring on it of newly ¯edged sparrows to tape-recorded songs. a tendency to learn to pay attention to certain kinds The results indicated preferential responsiveness to of sounds and certain types of phrase only'' conspeci®c song, stronger in swamp than in song (Thorpe, 1958, p. 84). In addition to the confound- sparrows, as early as 3 weeks of age. The procedure ing of sensory and motor constraints, early experi- was demanding, however, and only ®ve subjects ence was not adequately controlled. Several of were usedÐthree males and two femalesÐunder- Thorpe's experimental subjects were not raised by mining the signi®cance of the results but also serv- hand but were captured after ¯edging at an age of ing as an important reminder that selective song several weeks, providing them with ample opportu- responsiveness in females is a valid subject for nity to learn attributes of chaf®nch song prior to study. being brought into the laboratory. Resolution of this methodological dilemma Experimental controls of early experience were came when Nelson quanti®ed the calling behavior more complete in later studies on learning prefer- of young sparrows in the laboratory in response ences of North American sparrows. Hand-reared to playback of tape-recorded songs, showing that white-crowned sparrows given a choice of tape-re- newly ¯edged white-crowned sparrows of both corded songs of white-crowned and song sparrows sexes call more to conspeci®c than to heterospec- favored their own species (Marler and Tamura, i®c (song sparrow) song (Nelson and Marler, 1964; Marler, 1970). However, early develop- 1993). Whaling et al. (1995) went on to replicate mental stages of song production were only casually this result and to demonstrate strong respon- studied, so once again a role for motor constraints could not be excluded. More exhaustive analyses of siveness in young, naive subjects not only to com- learning preferences were conducted with two other plete white-crown songs but also to arti®cial members of the same family, the swamp sparrow songs consisting of repetitions of single song ele- (Melospiza georgiana) and the song sparrow (Mel- ments, including whistles, buzzes, and complex ospiza melodia) (reviewed in Marler and Peters, and simple trill syllables. 1989). Males taken as nestlings and raised by hand There is thus unequivocal evidence of selective in the laboratory were presented with a choice of responsiveness to conspeci®c song stimulation prior learning equal numbers of tape-recorded songs of to any song production, including subsong. Evi- both species. Isolated males displayed a highly sig- dently sensory mechanisms exist that enable the ni®cant preference for learning their own species' young songbird to discriminate between conspeci®c song. Despite evidence that song learning does not and heterospeci®c song. The innate knowledge take place in nestling songbirds (Slater, 1983; about their species song that young sparrows display Marler and Peters, 1987), there remained a linger- is based not on a single sign stimulus, but on multi- ing doubt that song experience in the nest might ple characters, suggesting that they possess remark- in¯uence later behavior as in some precocial birds. ably complete internal representations of the normal Although this seemed unlikely in an altricial spe- singing patterns of their species. The physiological cies, hatched at a much earlier developmental stage, means by which this is accomplished is unknown. in a second study, birds were taken as eggs from Until recently, it has not been the subject of detailed nests in the wild and raised in the laboratory. Choice investigation (Whaling et al., 1995). Yet, innate experiments with them yielded the same results, selective responsiveness may conceivably hold the showing that early nestling experience is not respon- key to understanding the memorization phase of the

/ 8p2d$$1890 09-15-97 17:38:50 nbioa W: Neurobio1890 Three Models of Song Learning 507 process of learning to sing, perhaps as represented from generation to generation. Under such circum- in this neuroselective model of song development. stances, the boundaries around the song patterns of a given species should be fuzzy and changing, with Species Universals in Learned Songs a high degree of variability. Descriptive analysis of and Their Failure to Develop in Isolates the typology of swamp sparrow song revealed a different picture (Marler and Pickert, 1984). Any Learned birdsongs are incredibly variable. In addi- known natural swamp sparrow song can be de- tion to the widespread occurrence of local dialects, scribed by reference to a lexicon of six note types, songs of no two individuals are precisely identical, de®ned on the basis of such basic characteristics as and as already noted, birds rely on the individual duration, bandwidth, and the pattern of frequency differences that are always present in learned songs modulation. Much the same typology results if it is to identify one another personally (review in Falls, derived from sound spectrograms by eye (Marler 1982). It was therefore unexpected when several and Pickert, 1984) or by statistical procedures such efforts to characterize the song patterns of an entire as multidimensional scaling (Clark et al., 1987; Nel- species revealed that variation in the natural song son and Marler, 1989). There is a certain order to patterns of some birds is more constrained than an- the way in which these note types are assembled ticipated. Along with the song characteristics that into a song syllable, with rules that vary from one vary between individuals and populations, there are locality to another. For example, a New York song always others that are shared, and a surprising num- syllable typically begins with a type I note and ber of natural song features proved to be species closes with a type VI note, with one or more notes speci®c. Occurrence of these species universals, suf- of some other category in between. The Minnesota ®cient in some cases to describe the major features dialect has an opposite rule, with song syllables of all known natural song variants, contradicts pre- typically beginning with a type VI note and ending vious impressions of almost unlimited variability with a type I note. Males and females will learn in the culturally transmitted patterns of birdsong, either dialect depending on individual experience. casting doubt on the very concept of instructive In females, the experience appears to determine the models of learning unconstrained by special predis- song type that they ®nd most stimulating sexually, positions. With a neuroselective model of song presumably one that they will favor in a mate, when learning, however, the existence of species univer- they reach reproductive maturity (Balaban, 1988). sals in song would be predicted. Here are a few Thus, instead of the expected unmanageable de- examples. gree of variability, a highly ordered system was found with predictable rules operating on a surpris- Universals in Swamp Sparrow Song ingly limited number of basic acoustic patterns. Su- perimposed on the basic typology, there is a signi®- The simple trilled song of the male swamp sparrow cant degree of within-category variation in note is stereotyped in overall structure and variable in morphology from bird to bird. This variation, to- the construction of the repeated syllables that make gether with the many different ways in which note up the 2-s song. Swamp sparrow songs develop ab- types can be combined to create a syllable, leaves normally in social isolates and are highly degraded ample room for dialects and individual variability, in birds deafened early in life (Marler and Sherman, so that no two individuals even in the same popula- 1983, 1985). In addition to individual differences tion have exactly identical songs. Territorial males in the syllables from which swamp sparrow songs are, in fact, highly responsive to individual differ- are constructed, there are also learned dialects, each ences as a basis for neighbor±stranger discrimina- thought to cover some hundreds of square miles. tion (Searcy et al., 1981a, 1982). Species recogni- Learning early in life determines which local dialect tion, on the other hand, in both sexes appears to a male sings, and also the dialect to which females be based on those song features that are species are most responsive (Balaban, 1988). Thus, swamp universals (Searcy et al., 1981b,c). sparrow song satis®es the criteria for a culturally transmitted behavior. If purely instructive processes Universals in Songs of Canaries, were responsible, there should be a tendency for the Buntings, and Other Species song patterns present in a population to drift over time, as songs are transmitted over generations, as Songs of male domestic canaries, Serinus canaria, birds invade new habitats, with new acoustic envi- a traditional subject for research on the neural basis ronments, and as transmission errors accumulate of vocal learning, can be de®ned on the basis of

/ 8p2d$$1890 09-15-97 17:38:50 nbioa W: Neurobio1890 508 Marler about 10 distinct syllable types, each with some note types, some with considerable within-category degree of within-category variation. The presence variation, others with relatively little (Sossinki and of these ``tours'' in all canary songs has been known Bohner, 1980; Bohner, 1983; Williams, 1990). by generations of fanciers who breed and display Learning determines which variants are used and certain strains competitively for their prowess as their sequencing (Price, 1979). Of special interest singers (Guttinger, 1985, 1979). Canary songs are is the ®nding by Clayton (1990a,b) that songs of an learned by acquiring particular sets of note catego- island subspecies on Timor have a structure rather ries and particular sequences of note types (Waser different from those in Australia. Thus, species uni- and Marler, 1977). Obvious copying occurs in se- versals in song structure vary not only between spe- quencing and at the level of subtypes within the 10 cies, but also from one subspecies to another. These major categories, varying in subtle aspects of pitch song universals have survived many generations of or modulation rate. Male canaries raised in auditory breeding in captivity. Once again, songs are abnor- isolation have an abnormal song, lacking several of mal if males are raised in isolation and even more those features that are universal in the song of canar- degraded in deaf birds (Price, 1979; Williams et al., ies with normal social experience (Guttinger, 1979; 1993). Marler and Waser, 1977; Waser and Marler, 1977). Songs of the wood thrush, Hylocichla mustelina, As in the swamp sparrow, so in the domestic canary are among the most beautiful of all to human ears. we can speak of universals in note typology that They have three parts, a, b, and c, of which b are generally distributed but lacking in birds raised is especially in¯uenced by learning (Whitney and in isolation. Miller, 1985; Whitney, 1989). Inspection of hun- Universals are also present in songs of the indigo dreds of songs led to the conclusion that all natural bunting, famous from the research of Thompson b-phrases, wherever they occur in the species range, (1970, 1976), Shiovitz and Thompson (1970), Shi- fall into about 20 rough categories, each with a ovitz (1975), Emlen (1971, 1972), Payne et al. degree of within-category variation. These b- (1981), and Margoliash et al. (1991), but on a phrases develop abnormally in isolation (Lanyon, different scale. Here there is a specieswide syllable 1979; Whitney and Miller, 1987). Songs of wood repertoire of something over 100 types. The same warblers, such as the chestnut-sided warbler, Den- catalog, ®rst developed by Thompson, has been droica pensylvanica, which has two distinct song used for nearly 30 years to describe thousands of types, are learned, and develop abnormally in isola- indigo bunting songs in all parts of the species' tion (Byers and Kroodsma, 1992). One song type range. Individuals and populations differ in song of this species has proved to be remarkably uniform structure, and there are local dialects (Payne, 1983) throughout the species range (Byers, 1996). The based on which subset of the specieswide syllable prothonotary warbler, Protonotaria citrea, is a simi- repertoire is used and the ordering of the syllables lar case (Bryan et al., 1987), with similar song within the song. Baker and Boylan (1995) recently patterns recurring in different parts of the species updated the species-universal catalog, now totaling range. Baker and Boylan (1995) reviewed other 127 syllable types for the indigo bunting, Passerina examples. There can be no doubt that specieswide cyanea, and 122 syllable types for the closely re- song universals are a frequent feature of learned lated lazuli bunting, Passerina amoena (cf. Thomp- birdsongs, a predictable correlate of a selection- son, 1968), all recurring ``at similar frequencies based learning process. of abundance in different populations at different times.'' Again, song develops abnormally in isola- Summary of Evidence and Replay tion (Rice and Thompson, 1968), and normal song of the Selection-Based Model patterns are learned and transmitted by cultural transmission (Payne et al., 1981; Payne and Payne, The four lines of evidence reviewed suggest that a 1993). selective model of song learning is worthy of further investigation. The ease and precision with which a The Zebra Finch few exposures suf®ce for conspeci®c songs to be memorized and reproduced by a naive subject are It is the subject of scores of studies of song learning notable, consistent with a neural system especially and its neural basis, but little effort has been directed dedicated to the tasks of song recognition and com- to descriptive studies of zebra ®nch song structure. mitment to memory. Other models cannot be ex- Nevertheless, inspection of published analyses al- cluded on this basis, however. More direct and com- ways seems to reveal the same four or so basic pelling is the evidence for learning preferences, im-

/ 8p2d$$1890 09-15-97 17:38:50 nbioa W: Neurobio1890 Three Models of Song Learning 509 plying neural mechanisms that focus the young be capable of sustaining song learning in some cir- bird's attention selectively on conspeci®c song pat- cumstances. Even highly selective song learners can terns. Most striking are the demonstrations of spe- be persuaded to learn alien songs if those of their cies-speci®c universals in the structure of learned own species are withheld. Especially when highly songs, many of which fail to develop in birds raised aroused by social stimulation, this can occur in the in isolation. These birds behave as though they pos- presence of conspeci®c song stimulation, bypassing sess extensive innate knowledge about their species the template system. It is presumed that this will song, but cannot transform that knowledge into pro- take more time and effort than learning own-species duced song without the experience of matched songs, which as we have seen can be very rapid and sounds in the songs of others. Such behavior is con- precise. All birds can be taught to give an arbitrary sistent with a selection-based model of the song response to alien songs, but interestingly, sensitivity memorization. to individual differences is typically greater with The essential postulate of this model is that spe- conspeci®c songs than with those of other species, cies-speci®c song universals are pre-encoded in the consistent with the idea that template-based acquisi- brain, and that every young male of a species has tion would confer greater sensitivity to acoustic de- the potential to produce all universals. A plausible tail (Dooling, 1989; Sinnott, 1989). However, model also has to take account of the all-perva- involvement of the template system in song memo- siveness of developmental plasticity, the impact of rization is not obligatory, as when a nonmimic auditory experience, and the effects of deafening. learns the song of another species. With the exception of a small but interesting minor- Template systems could be involved directly or ity (see Marler and Nelson, 1992), most song uni- indirectly in memorization. They could serve to ¯ag versals fail to develop normally in isolation. Even song components and other associated stimuli espe- fewer develop in birds deafened early in life as cially worthy of attention and memorization by the illustrated by the swamp sparrow (Marler and Sher- general auditory system. Consistent with this idea man, 1983, 1985). Any theory of song development is the success Soha (1996) achieved in persuading must somehow deal with the highly degraded songs birds to learn songs they would otherwise spurn by of early deafened birds and the more structured embedding within them rudiments of the birds' own songs of birds raised in isolation with their hearing species song. It remains for neurobiologists to deter- intact. The memorization by selection model attri- mine where in the oscine brain these different func- butes the song structure present in hearing isolates tions are served and the degree to which the tem- to preactive auditory templates that become active plate system, if it exists, achieves its functional ends in development whether or not conspeci®c song has by intrinsic mechanisms, or more indirectly, by been experienced. Latent auditory templates cannot priming other parts of the brain that serve more exert an in¯uence on motor development before ac- general functions of sound memorization, to pay tivation by auditory stimuli that match their acoustic special attention to conspeci®c song. speci®cations. Stimulation of templates is also pre- sumed to aid in memorization of song stimuli. Dur- ing memorization, stimulus-triggered events in dif- MODEL 3: MEMORIZATION BY ferent parts of the template system will become sim- INSTRUCTION FOLLOWED BY ilarly coordinated in time in memory, thus matching SELECTION IN PRODUCTION the pattern of the stimulus song. Also, sound stimuli that engage templates will be committed to memory A model of song learning incorporating both memo- more rapidly and precisely than others that do not, rization by instruction and selection during produc- such as songs of other species. It is presumed that tion originated with a shift of focus from the memo- material memorized after interaction with the tem- rization phase of song development to the produc- plate system will be dedicated speci®cally to the tion phase. A new form of vocal plasticity termed processing of song stimuli and to guidance of the ``action-based learning'' was revealed (Marler, bird's own song production. 1991; Marler and Nelson, 1993; Nelson and Marler, 1994). Once songs have been memorized by a Qualifications of the Model young sparrow, it begins after some interval to pro- duce imitations, often supplemented in plastic song Any song-speci®c template mechanisms that exist by inventions and improvisations. With practice, the must operate in parallel with brain mechanisms that motor patterns stabilize and the adult song repertoire support generalized auditory learning, presumed to crystallizes. After closure of the sensitive period for

/ 8p2d$$1890 09-15-97 17:38:50 nbioa W: Neurobio1890 510 Marler memorization of new songs, and prior to crystalliza- combination of instructive and selective processes. tion, it seems to be common for songbirds to pro- The sensorimotor model for song memorization as- duce more songs than they will need. The overpro- sumes that the young bird memorizes new songs by duced repertoire is winnowed as crystallization ap- instruction, committing to memory more than will proaches, and social factors exert an in¯uence on be needed for a normal adult repertoire. These mem- which songs are kept and which are discarded. This orized songs, together with invented and improvised is the context for action-based learning. material, emerge at a later stage when memorization Nelson demonstrated that a process of selection by instruction is no longer possible, as the overpro- lies at the heart of action-based learning (1992a,b; duced repertoire of plastic songs. A process of selec- Nelson and Marler, 1994). Overproduction was ®rst tion now intrudes, mediated by patterns of social demonstrated in the swamp sparrow, Melospiza interaction in which the young male engages as the georgiana (Marler and Peters, 1982). In plastic overproduced repertoire is winnowed. In intermale song, beginning at about 6±9 months of age, imita- countersinging, responding with a song type that tions of previously memorized tutor songs ®rst ap- matches the competing rival is especially effective pear. Young males produce more plastic song types in territorial establishment, even if the matching is than needed for a mature repertoire. The overpro- only approximate. This interactive potency may duced repertoire of 12 or so song types suffers grad- contribute to the process of selective retention. ual attrition until it has shrunk to about three song The process of selection appears to proceed inde- types, the typical adult male repertoire. Crystalliza- pendently from memorization by instruction. The tion then occurs. Similarly, wild young male ®eld two kinds of process proceed on different timetables sparrows, Spizella pusilla, and white-crowned spar- and must engage different neural mechanisms de- rows, Zonotrichia leucophrys, often sing several spite the fact that the behavioral consequences are song types when ®rst establishing territories. They somewhat similar: Both result in a degree of experi- then select one, usually choosing to retain that entially dependent matching of songs produced with which best matches one of a neighboring rival's songs heard. Further evidence that instruction and songs, at the site where the young male is establish- selection are independent processes is provided by ing his ®rst territory, often somewhat remote from the parallel case of the brown-headed cowbird, Mo- the birthplace (Nelson, 1992). This takes place after lothrus ater, in which the male's choice of which closure of the sensitive period for memorization of overproduced song types to retain is guided not by new songs in these species (e.g., Nelson and Marler, male±male interactions, but by interactions with fe- 1994). The retention of a matched song has some- males. Males retain those song types that elicit a times given the mistaken impression that young distinctive ``wing stroke'' display from females males were imitating new neighbor songs at this (West and King, 1988). In this case, visual signals stage. In fact, a process of selection from within a rather than auditory exchanges are responsible for pre-established repertoire is responsible. the development of male vocal behavior. As studies In experimental veri®cation of this process, proceed, it is likely that action-based learning as hand-reared male white-crowned sparrows were tu- a form of selection-based developmental plasticity tored with a number of song types early in life. occuring during motor development, will prove to When they began to produce imitations in plastic be widespread and that depending on the species, a song the following spring, other songs were played range of interactive processes can control which to them that matched one item in their overproduced items in an overproduced repertoire are retained and plastic song repertoire, simulating the matched which are set aside. countersinging between rivals that occurs in nature when yearlings ®rst establish their territories. In ad- dition, birds heard a novel song type never encoun- DISCUSSION tered or produced before. Although these birds were incapable of acquiring new songs at this stage, they Of the three models of vocal learning reviewed, the retained and crystallized the song type that most one based on concepts of memorization by selection closely matched the tutor and discarded nonmatch- is most radical. The lines of behavioral evidence ing types. This process of selective retention and with the strongest bearing on the tenability of this attrition was imposed on a repertoire acquired at 5± model are: (a) the existence of learning preferences 6 weeks, more than 200 days previously (Nelson in naive birds, leading them in the very ®rst step of and Marler, 1994). the learning process in which songs are memorized, This sequence of events can be modeled as a to favor conspeci®c songs over those of other spe-

/ 8p2d$$1890 09-15-97 17:38:50 nbioa W: Neurobio1890 Three Models of Song Learning 511 cies. In some cases, innate knowledge of a wide enduring repertoire (review in Nelson, 1992b; array of species-speci®c song attributes has been Marler and Nelson, 1993). The timing of this stage demonstrated prior to any song production of a wide of highly unstable motor activity will vary widely array of species-speci®c song attributes. (b) An- from species to species. In some, such as the male other line of evidence is the failure of much of this swamp sparrow, it is brief and occurs once as the innate knowledge to be realized in the songs of young male approaches sexual maturity. In others, birds raised in social isolation. Certain aspects of such as the ®eld sparrow and the indigo bunting, it the normal song of the species do develop in social is more extensive, encompassing a signi®cant part isolates, however, provided that their hearing is in- of a male's ®rst breeding season. The developmental tact. In birds deafened prior to singing, even these window for action-based learning may recur period- few normal features of isolate songs fail to develop ically on a seasonal basis in some species. The ca- other than a few basic attributes such as song dura- nary may prove to be such a case (Nottebohm et tion and some elements of phrase structure, perhaps al., 1986, 1987). There is also likely to be variation controlled by respiratory motor programs (Marler between species in the social mechanism that con- and Sherman, 1983). As Konishi (1965) demon- trols the winnowing process. Two versions have strated in his classic studies, auditory feedback is already been described involving male-to-male ter- critical for normal song development. (c) Harder to ritorial countersinging in sparrows and a form of interpret, but perhaps ultimately a more valuable sexual reinforcement by females in the brown- source of new insights, is the discovery that varia- headed cowbird (West and King, 1988). Thus, ac- tion in the patterning of natural bird songs is often tion-based learning is well established as a compo- highly constrained and that learned often songs dis- nent in the development of learned bird songs and play species-speci®c universals in many aspects of may have parallels in other contexts, such as the their structure. Those aspects that do vary can be transition from play to adult behavior. Less clear is permuted in many different combinations, providing the source of the overproduced repertoire upon ample acoustic vehicles for local dialects and indi- which action-based learning operates. If in the face vidual differences. Other aspects of song structure, of further research instructive models of song mem- many more than previously realized, are shared by orization prevail, then a mixed model will be vindi- all species members, each individual employing cated. On the other hand, if a selection-based model some fraction of the universal lexicon. of song memorization proves to be closer to the None of these lines of evidence is compatible truth, then a fourth model must be contemplated in with a simple instructive model of song learning, which instruction in the pure sense plays little role the essence of which is taken to be that the process (Fig. 1, Model 4). It would be premature to try to is basically open and unconstrained. In fact, the forecast which of these alternatives is valid or version of the sensorimotor model presented here whether some mechanism will emerge, as yet unan- (Fig. 1, Model 1) is probably something of a carica- ticipated, that provides the basis for song memoriza- ture, although it serves a purpose by heightening tion as a ®rst step in the learning process. the contrast with other models in which constraints Where might song template processing occur in on the learning process are more evident and perva- the oscine brain? As a direct consequence of the sive. All three lines of evidence sit more comfort- discovery of the song system in the oscine brain ably with a model based on selection, but a neuro- (Nottebohm et al., 1976; Kelley and Nottebohm, selective model of song learning is hardly likely 1979), we have a more complete picture of the to be taken seriously until direct neurobiological underlying circuitry for song learning than for any support is forthcoming. Thus, both of the ®rst two other learned behavior. Many functional questions models set forth, one brie¯y, the other in more de- remain, however. One of the most challenging is tail, remain speculative. the role of the so-called ``recursive'' or ``anterior The third model, combining elements of instruc- forebrain circuit,'' consisting of the chain of nuclei tion and selection (Fig. 1, Model 3), has greater HVc±Area X±DLM±lMAN±RA, in the process substance. The role of social processes in selecting of song development. Lesioning seems to have no songs for crystallization from overproduced plastic immediate effect on adult singing behavior, but song repertoires is well established and likely to be greatly disrupts song ontogeny (Bottjer et al., 1984; widespread. The basic underlying process is Sohrabji et al., 1990). If the naive songbirds' brain straightforward. At a certain stage of development, is in fact innately equipped with an array of auditory a wide array of motor patterns is produced and sub- templates for song, the recursive song circuit is a sequently winnowed down to a smaller and more likely place for them to be found. This circuit is in

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Figure 1 Diagrams of the three models described in detail in the text (Models 1±3) plus a fourth that combines elements of Models 2 and 3. place and functional early in life, prior to establish- Doupe, 1997). Only recently has exploration begun ment of the motor circuit; and the functional timeta- of the possibility that there is species-speci®c song ble of at least one of its components, lMAN, agrees responsiveness in the song system at early stages well with the timing of song acquisition, both in of development (Whaling et al., 1995). If the selec- canaries and in zebra ®nches. Auditory neurons can tion-based model of song memorization has any va- be found in HVc and throughout the recursive cir- lidity, then song-selective circuitry must exist some- cuit, and some have the remarkable property discov- where in the naive songbird brain. The selective ered by Margoliash (1983, 1986) and Margoliash model of learning predicts that activation of this and Konishi (1985) that in adults, they are maxi- circuitry will play a critical role in the process of mally responsive to the male's own song. Highly song memorization, with an in¯uence on the pro- selective song responsiveness in adulthood is espe- cessing not only of the bird's own species songs cially characteristic of lMAN, an obvious place to (see Mooney, 1992), but perhaps for those of other look early in life for sensitivity to the species-spe- species as well. The search may embrace other path- ci®c universals to which we know songbirds are ways than the song system sensu stricto including behaviorally responsive. Responsiveness to a male's subareas of the forebrain auditory projection area own song develops only late as song performance Field L, where neurons that selectively respond to matures (Volman, 1993). Prior to that, song respon- complex sounds, including songs and calls, have siveness is less speci®c (Doupe and Konishi, 1992; been identi®ed (Leppelsack, 1983; Scheich et al.,

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1979). Other sound-processing areas may also be Nelson, Carol Whaling, and Jill Soha, who made invalu- involved, and are only now being identi®ed (Clay- able contributions to the research and ideas expressed in ton, 1997), as in recent efforts to establish directly this article; and Jeni Trevitt for help in preparing it for the role of gene activation in the process of song publication. Constructive criticisms by Eliot Brenowitz learning. and Kathy Nordeen were most helpful. Much of the re- search was supported by PHS Grant MH14651. Mello et al. (1992) broke new ground with their demonstration of the activation of an immediate early gene, zenk in adult canary and zebra ®nch brains in response to song stimulation after being REFERENCES deprived of song access. Heterospeci®c song had a weaker effect, and tone bursts none at all. The in- BAKER, M. C., and BOYLAN, J. T. (1995). A catalog of creases occurred in several unexpected areas, and song syllables of indigo and lazuli buntings. 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