Evaluating Theories of Bird Song Learning: Implications for Future Directions
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J Comp Physiol A (2002) 188: 851–866 DOI 10.1007/s00359-002-0351-5 PROXIMATE MECHANISMS OF SONG LEARNING D. Margoliash Evaluating theories of bird song learning: implications for future directions Received: 18 February 2002 / Revised: 1 July 2002 / Accepted: 5 September 2002 / Published online: 13 November 2002 Ó Springer-Verlag 2002 Abstract Studies of birdsong learning have stimulated ventrale Æ clHV lateral subdivision of the caudal region extensive hypotheses at all levels of behavioral and of hyperstriatum ventrale Æ cmHV medial subdivision physiological organization. This hypothesis building is of the caudal region of hyperstriatum ventrale Æ DLM valuable for the field and is consistent with the re- medial subdivision of the dorsal lateral nucleus of markable range of issues that can be rigorously ad- anterior thalamus Æ DM dorsomedial subdivision of dressed in this system. The traditional instructional nucleus intercollicularis Æ DMP dorsomedial nucleus of (template) theory of song learning has been challenged posterior thalamus Æ HV ventral hyperstriatum Æ HVc on multiple fronts, especially at a behavioral level by acronym used as the proper name Æ lMAN lateral evidence consistent with selectional hypotheses. In this subdivision of the magnocellular nucleus of the anterior review I highlight the caveats associated with these neostriatum Æ MLD dorsal lateral nucleus of theories to better define the limits of our knowledge and mesencephalon Æ mMAN medial subdivision of the identify important experiments for the future. The sites magnocellular nucleus of the anterior neostriatum Æ Ncm and representational forms of the various conceptual caudal medial neostriatum Æ Nd dorsal caudal neostria- entities posited by the template theory are unknown. tum Æ NIf nucleus interfacialis Æ NMDA N-methyl- The distinction between instruction and selection in D-aspartate Æ Ov nucleus ovoidalis Æ RA robust nucleus vocal learning is not well established at a mechanistic of the archistriatum Æ RAm nucleus retroambigualis Æ level. There is as yet insufficient neurophysiological data Uva nucleus uvaeformis to choose between competing mechanisms of error- driven learning and reinforcement learning. Both may obtain for vocal learning. The possible role of sleep in Introduction acoustic or procedural memory consolidation, while supported by some physiological observations, does not Perhaps the most influential theory of birdsong learning yet have support in the behavioral literature. The re- is also one of the earliest. Proposed some 40 years ago, markable expansion of knowledge in the past 20 years the template theory posits a series of conceptual objects, and the recent development of new technologies for an innate predisposition for conspecific songs, an innate physiological and behavioral experiments should permit template that guides vocal learning in the absence of direct tests of these theories in the coming decade. song models, and an acquired template formed when song models (typically, the songs of adult conspecifics) Keywords Error-driven and reinforcement learning Æ are available to the animal during the critical period Instruction and selection Æ Sleep and replay Æ Template (sensory phase) for song acquisition. The acquired theory template is conceived of as the internal sensory repre- sentation of external song models that is used to judge or Abbreviations AFP: anterior forebrain pathway Æ Am guide the young bird’s own vocal output. The form of nucleus ambiguus Æ cHV caudal region of hyperstriatum the internal representation is unspecified and is an ex- citing unresolved problem – there may be many possible forms for neural representations of sounds (e.g., see re- D. Margoliash view by Gentner and Margoliash 2002). The innate or Department of Organismal Biology and Anatomy, acquired template guides vocal learning through a pro- University of Chicago, 1027 E. 57th St., Chicago, IL 60637, USA cess of trial-and-error auditory feedback-mediated E-mail: [email protected] learning. The critical features of the sensorimotor Fax: +1-773-7020037 (feedback-mediated) learning model are the sensory 852 template and the use of error-correction. A deaf bird, geographic domains. Thus, the vocal diversity of indi- that has no access to the feedback signal, cannot correct viduals within a species may result from choosing par- errors and so his song wanders. Deafening prior to song ticular exemplars from a range of combinations of a crystallization immediately arrests vocal development relatively small set of primitives (see Marler 1997). These because it prevents access to the feedback error signals observations are consistent with a selectional model of that are compared with vocal output to guide further learning (Marler and Peters 1982a; Nelson 1992a; Nel- development (Konishi 1965, 1978, 1985; Marler 1970). son and Marler 1994). In a selectional model, the envi- The template model is an instructional model in that the ronment influences the choice of a small number of environment strongly and directly guides the song de- patterns derived from a larger set of patterns that reflect velopment, both in the sensory phase and in the senso- the natural variation in behavior that an organism rimotor phase. The template concept implies immediacy produces. of correcting vocal output during singing – feedback is Field sparrows and white-crowned sparrows may compared with a template (target) vocalization, and the develop more than one song type, then express a given errors are immediately applied to change the vocal song type based on the prevalent songs a bird encounters output. No long-term memory of the errors is posited. (Nelson 1992a, 1992b). In some species such as indigo The template theory is a succinct statement that has buntings, individuals may also maintain a private rep- stimulated a large body of behavioral research. As the ertoire of syllables (Margoliash et al. 1994a) that are leading theory it has been the natural target of multiple expressed only rarely during aggressive encounters tests. Weaknesses have been exposed in that a purely (Emlen 1972). In principle, these could be accessed to acoustic account of vocal learning does not generally achieve a rapid, ‘‘action-based’’ learning process (Marler obtain. Depending on species, birds may rely on multiple and Nelson 1993), a form of immediate copying of vo- cues as to which songs to attend to. For example, young calization. The rapid changes in song that yearling in- indigo buntings and zebra finches require social interac- digo buntings exhibit, in the extreme case completely tions to acquire songs (Payne 1981; Adret 1993). Juvenile remodeling their songs in a period of 24 h, is evidence white-crowned sparrows will learn song models prefer- for this hypothesis (Payne et al. 1988). As with the more entially from heterospecific live tutors that they can see, traditional selectional model, action-based learning ap- even if the juvenile sparrows are in acoustic contact with pears to vary from the template theory of song learning live conspecifics who sing (Baptista and Petrinovich in that the influence of the environment is more strongly 1984). Cowbirds, which are parasitic birds raised by alien constrained. This distinction may not be compelling, parents, face unusual problems as to whom to learn song however, since action-based learning is proposed for from and when. Remarkably, certain wing strokes of fe- animals that have already passed through early vocal male cowbirds in response to juvenile male songs strongly development. The role of feedback in action-based ac- shape the development of those songs (West and King quisition of new vocal material has yet to be well de- 1988). Live tutors and social interactions can perhaps scribed. There is neurobiological evidence for influence all stages of song learning. These and many re- hierarchical organization of the motor program for song lated observations do not falsify the template theory of (see below). If action-based learning is limited to song learning, but they significantly extend it with a bio- changes in patterns of expression of pre-existing vocal logical richness more consistent with the large variation in elements, then the rapidity of learning may result from behavior observed across multiple species. needing to coordinate feedback-mediated changes only A more fundamental challenge to the template theory at higher levels of the hierarchy. Such a hypothesis is of birdsong learning has questioned the extent to which neutral to the question of whether the coordination is song learning is driven by external stimuli. During vocal mediated through instructional or selectional mecha- development, an overabundance of vocal material is nisms. produced which is later whittled down when the final Selectional and instructional learning may be distinct adult song(s) crystallize. This excess material is related in at a theoretical level yet difficult to differentiate at a part to which songs birds are tutored with early in life, neural level. The potential form of a selectional process but birds can produce normal syllables to which they is highlighted by the observation that species-universals have never been exposed (e.g., Marler and Peters 1981). do not fully develop in isolate-reared or deafened birds The songs a young bird is exposed to early in life in- (Marler and Sherman 1983, 1985). Isolate song may fluence which sounds are maintained into the adult song have some species-typical structure (Konishi 1978), and and which are discarded. In song