Learning to Like Your Voice: Developing Selectivity to Birdsong

A basic principle of functional brain organization is that stimuli in the environment are coded by selective neuronal responsiveness. Classic examples of such neuronal selectivity range from cells in the visual cortex that fire only in response to simple visual stimuli to the more complex cells in the inferotemporal cortex of primates that are selective only for conspecific faces. Although the existence of such neuronal selectivity is axiomatic in cognitive neuroscience, the way in which such striking selectivity develops remains an important topic of research. The classic work of Hubel and Wiesel on the development of neuronal selectivity in the visual system demonstrated that this selectivity is not entirely prespecified or necessarily intrinsic to a neuronal cell type. In fact, severe developmental perturbations can extinguish or profoundly modify the occurrence of cortical neurons that fire selectively to simple visual stimuli. But what types of normal experiences can induce such selectivity? Is learning involved? How enduring are such experiential effects?Insight into these processes is provided by a paper in this issue of Neuron by Solis and Doupe 2000xSolis, M.M. and Doupe, A.J. Neuron. 2000; 25: 109–121Abstract | Full Text | Full Text PDF | PubMedSee all ReferencesSolis and Doupe 2000 on the development of selective firing to a bird's own song by neurons in the zebra finch brain. These so-called “song-specific” neurons were discovered by Margoliash and Konishi 1985xMargoliash, D. and Konishi, M. Proc. Natl. Acad. Sci. USA. 1985; 82: 5997–6000CrossRef | PubMedSee all ReferencesMargoliash and Konishi 1985 when investigating the auditory responsiveness of neurons in the avian song system. The song system consists of a network of interconnected nuclei in the telencephalon, diencephalon, and brainstem of songbirds that regulates the motor production of song (Nottebohm 1996xNottebohm, F. J. Comp. Physiol. [A]. 1996; 179: 149–156CrossRef | PubMedSee all ReferencesNottebohm 1996; see figure). It was therefore of great interest when a key nucleus in this circuit, HVc, was found to exhibit selective auditory responses. In particular, in some neurons the responses were selective not only to features of conspecific song in general but to specific combinations of features unique to the song produced by the male bird himself (Margoliash and Fortune 1992xMargoliash, D. and Fortune, E.S. J. Neurosci. 1992; 12: 4309–4326PubMedSee all ReferencesMargoliash and Fortune 1992). Because birdsong is a learned behavior (Marler 1997xMarler, P.R. J. Neurobiol. 1997; 33: 501–516CrossRef | PubMed | Scopus (178)See all ReferencesMarler 1997), this immediately suggested that specific types of experience were required for the development of such selectivity. Indeed, it was demonstrated by Volman 1993xVolman, S.F. J. Neurosci. 1993; 13: 4737–4747PubMedSee all ReferencesVolman 1993 that such auditory selectivity in white-crowned sparrows only emerges when the sparrows have learned to produce the highly stereotyped song typical of adult birds.Solis and Doupe 2000xSolis, M.M. and Doupe, A.J. Neuron. 2000; 25: 109–121Abstract | Full Text | Full Text PDF | PubMedSee all ReferencesSolis and Doupe 2000 have now demonstrated that selective neuronal firing to the bird's own song is not the result of only a maturational process but rather is also shaped by the learning of song itself. The authors take advantage of the fact that there are two distinct ways in which auditory experience influences song learning in zebra finches and other songbird species (Marler 1997xMarler, P.R. J. Neurobiol. 1997; 33: 501–516CrossRef | PubMed | Scopus (178)See all ReferencesMarler 1997). Early in ontogeny, young birds must hear conspecific song from a tutor and form an auditory memory of this song that is sometimes referred to as a “template.” Subsequently, they gradually match their own vocal output to this memory or template until they produce the stereotyped or “crystallized” song typical of adult birds. Solis and Doupe selectively altered learning during the second phase by denervating the vocal production organ, the syrinx, prior to the period when the finches would start matching their song to the tutor's song they had heard previously. When the transection heals, the birds have less vocal control, produce some unusual songs, and end up with variable reinnervation of the syrinx. As a result, some adult finches are unable to match the tutor's song at all, although they produce a stereotyped adult-like song, while other individuals learn to produce a reasonable match. This variability allowed the authors to address an interesting question. In the birds that are unable to match their tutor's song, will the selectivity of the neurons in the song system resemble more the tutor's song, which shaped their template, or the song they actually produce?Solis and Doupe focused on the auditory responses of neurons in nuclei such as Area X and LMAN that are in the anterior forebrain pathway of the song control system (see figure). This pathway is needed for song learning (Bottjer and Johnson 1997xBottjer, S.W. and Johnson, F. J. Neurobiol. 1997; 33: 602–618CrossRef | PubMed | Scopus (178)See all ReferencesBottjer and Johnson 1997), and neurons in this pathway were shown previously to exhibit selectivity to the bird's own song in close association with the learning of adult-typical song (Solis and Doupe 1997xSolis, M.M. and Doupe, A.J. J. Neurosci. 1997; 17: 6447–6462PubMedSee all ReferencesSolis and Doupe 1997). In this study, in anesthetized birds that had nerve cuts and whose songs were different from the tutor's song, many neurons in Area X responded equally well to the bird's own song and to the tutor's song. Furthermore, the degree of selectivity to these two stimuli over conspecific and reversed song was considerably less than in normal adults. Also, auditory responses in these birds were exceedingly rare in another song nucleus in the anterior forebrain pathway, LMAN. This is in contrast to the findings for the birds that managed to mimic their tutor in a reasonable manner. Neurons in Area X in these birds developed a normal selectivity to the bird's own song relative to other stimuli, and the neurons in LMAN were also normally selective.These data tell us something important about how this remarkable neuronal selectivity develops. Clearly, both the tutor's song and the song produced by the bird are important for the development of song-selective neurons. Also, a chronic mismatch between the song the bird produces and the template based on the tutor's song results in a significant alteration in the responsiveness of the neurons in the anterior forebrain pathway of the song system. The dual selectivity of a single neuron that was observed in the adult birds with song incongruent from the tutor's song was observed previously only in young birds that were not yet able to produce adult stereotyped song (Solis and Doupe 1999xSolis, M.M. and Doupe, A.J. J. Neurosci. 1999; 19: 4559–4584PubMedSee all ReferencesSolis and Doupe 1999). Solis and Doupe speculate that such dual selectivity may be a general feature of the adult song system that was not recognized in the past because the bird's own song is normally close to the tutor's song. Alternatively, such dual selectivity may be a juvenile feature that was maintained in these adults because of their chronic inability to match their song with the tutor's song. Thus, whether the dual selectivity is only needed for the transition to adult song or whether it plays a role in adult song maintenance and/or perception is still unclear.Overall, this study tells us that deprivation of a very specific type of experience, namely, the matching of vocal output with an auditory memory of the tutor's song, is enough to perturb the development of neuronal selectivity. Further studies on the song system should help clarify the possible adult function of these highly selective neurons. For example, are dual-selective neurons part of the mechanism by which altered song is produced in response to perturbation in auditory feedback (Leonardo and Konishi 1999xLeonardo, A. and Konishi, M. Nature. 1999; 399: 466–470CrossRef | PubMed | Scopus (205)See all ReferencesLeonardo and Konishi 1999)? Is the development of the highly selective neurons in the anterior forebrain pathway essential for the comparison between the bird's own song and the tutor's song that occurs during song learning? In any case, such precision in the development of neuronal selectivity may be a general feature of the vertebrate nervous system. Other examples of complex neuronal selectivity may require highly specific types of sensory feedback during development.Figure 1Simplified Diagram of the Song System of Songbirds in the Sagittal PlaneTwo pathways can be distinguished, the posterior motor pathway (dark stippling with solid lines connecting the nuclei) and the anterior forebrain pathway (light stippling with dotted lines connecting the nuclei). All recordings were made in the anterior forebrain pathway, a specialized forebrain–basal ganglia circuit. HVc, high vocal center; RA, robust nucleus of the archistriatum; DLM, dorsolateral thalamic nucleus; lMAN, lateral part of the magnocellular nucleus of the anterior neostriatum; RAm, nucleus retroambigualis.View Large Image | View Hi-Res Image | Download PowerPoint Slide