Neural systems for individual song recognition in adult birds.

The songbird auditory system is an excellent model for neuroethological studies of the mechanisms that govern the perception and cognition of natural stimuli (i.e., song), and the translation of corresponding representations into natural behaviors. One common songbird behavior is the learned recognition of individual conspecific songs. This chapter summarizes the research effort to identify the brain regions and mechanisms mediating individual song recognition in European starlings, a species of songbird. The results of laboratory behavioral studies are reviewed, which show that when adult starlings learn to recognize other individual's songs, they do so by memorizing large sets of song elements, called motifs. Recent data from single neurons in the caudal medial portion of the mesopallium are then reviewed, showing that song recognition learning leads to explicit representation of acoustic features that correspond closely to specific motifs, but only to motifs in the songs that birds have learned to recognize. This suggests that the strength and tuning of high-level auditory object representations, of the sort that presumably underlie many forms of vocal communication, are shaped by each animal's unique experience.

Response biases in auditory forebrain regions of female songbirds following exposure to sexually relevant variation in male song.

In many species of songbirds, individual variation between the songs of competing males is correlated with female behavioral preferences. The neural mechanisms of song based female preference in songbirds are not known. Working with female European starlings (Sturnus vulgaris), we used immunocytochemistry for ZENK protein to localize forebrain regions that respond to sexually relevant variation in conspecific male song. The number of ZENK-ir cells in ventral caudo-medial neostriatum [NCMv] was significantly higher in females exposed to longer songs than in those exposed to shorter songs, whereas variation in the total duration of song exposure yielded no significant differences in ZENK expression. ZENK expression in caudo-medial ventral hyperstriatum [cmHV] was uniformly high in all subjects, and did not vary significantly among the three groups. These results suggest that subregions of NCM in female starlings are tuned to variation in male song length, or to song features correlated therewith. Female starlings exhibit robust behavioral preferences for longer over shorter male songs (Gentner and Hulse; Anim Behav 59:443-458, 2000). Therefore, the results of this study strongly implicate NCM in at least a portion of the perceptual processes underlying the complex natural behavior of female choice.

Perceptual classification based on the component structure of song in European starlings.

The ability to recognize individuals based on their vocalizations is common among many species of songbirds. Examining the psychological and neural basis of this functionally relevant behavior can provide insight into the perceptual processing of acoustically complex, real-world, communication signals. In one species of songbird, European starlings (Sturnus vulgaris), males sing long and acoustically complex songs composed of small stereotyped note clusters called motifs. Previous studies demonstrate that starlings are capable of individual vocal recognition, and suggest that vocal recognition results from the association of specific motifs with specific individuals. The present study tests this possibility by examining how variation among the motifs that comprise a song affect its discrimination and classification. Starlings were trained, using operant techniques, to associate multiple songs from a single male starling with one response, and songs from four other male starlings with another response. The level of stimulus control exerted by motif variation was then measured by having subjects classify three sets of novel song bouts in which motifs from the training songs were systematically recombined. The results demonstrate a significant, and approximately linear, relationship between song classification and the relative proportions of familiar motifs from different singers that compose a bout. The results also indicate that the motif proportion effects on song classification are primary to retroactive interference in the recall for specific motifs, and independent of any biases due to the syntactic organization of motifs within a bout. Together, the results of this study suggest that starlings organize the complex vocalizations of conspecifics by memorizing large numbers of unique song components (i.e., motifs) that are then associated with different classes. Because individual starlings tend to possess unique motif repertoires, it is likely that under natural conditions such classes will correspond to individual identity. Thus, it is likely that perceptual processing mechanisms similar to those described by the results of the present study form the basis for individual vocal recognition in starlings.

Individual vocal recognition and the effect of partial lesions to HVc on discrimination, learning, and categorization of conspecific song in adult songbirds.

Among songbirds, the capacity to associate particular songs with particular singers (i.e., vocal recognition) forms the cognitive basis for more complex communication behaviors such as female choice and territoriality. In the present study, we combine operant conditioning techniques and excitotoxic lesions to the forebrain nucleus HVc to examine the role of this region in the discrimination, associative learning, and categorization of conspecific song. We trained adult male and female European starlings, Sturnus vulgaris, to recognize simultaneously the songs of several conspecific males. Then, using a series of transfer procedures, we demonstrate that correct recognition does not generalize to song bouts containing novel motifs from familiar singers. This suggests that starlings do not make use of individually invariant source or filter characteristics for vocal recognition. We then lesioned a portion of HVc bilaterally with ibotenic acid, and exposed the birds to a series of manipulations testing the discrimination, associative learning, and categorization of conspecific song. The lesions attenuated song production among males, but retention of the basic recognition task (i.e., maintenance of the discrimination) was unaffected. However, when the response contingencies were reversed-as a test of associative learning independent of discrimination-the initial performance and subsequent learning rate were negatively correlated with the size of the HVc lesions. This suggests that HVc plays a role in the formation of associations between a song and some referent. The results of this study are discussed in light of earlier claims regarding the role of HVc in the perceptual processing of conspecific song.

Auditory scene analysis by European starlings (Sturnus vulgaris): perceptual segregation of tone sequences.

Like humans, animals that use acoustic stimuli to perceive their world ought to be able to parse the auditory scene into functionally significant sounds. The ability to do so ought to have significant adaptive value when, for example, an animal can identify the sounds of a predator among other natural noises. In earlier work it was shown that a species of songbird, the European starling, can identify excerpts of both its own song and songs from other avian species when the songs are mixed concurrently with other natural signals. In this experiment it is demonstrated that starlings can segregate two synthetic pure-tone sequences when the sequences differ in frequency. Taken together, the experiments show that at least one nonhuman species is capable of auditory scene analysis both for natural and for non-natural acoustic stimuli. This suggests in turn that auditory scene analysis may be a general perceptual process that occurs in many species that make use of acoustic information.

Effects of social interaction on the development of starling song and the perception of these effects by conspecifics.

To examine the effects of contact with a conspecific in the absence of species-typical song models, the authors raised starlings in male-male pairs in acoustic isolation. The songs of these birds differed significantly from those of either individual isolates or wild adults and resembled in some respects the songs of starlings tutored by live conspecifics. Operant conditioning techniques were used to demonstrate that these differences among songs were perceptually salient to conspecifics. The results indicated that (a) wild-caught adult starlings are capable of forming open-ended categories for isolate and wild song, (b) starlings perceive the songs of isolated pairs as more "isolatelike" than "wildlike," and (c) starlings can distinguish the songs of isolated pairs from those of individual isolates. Both experiments point to the importance of social factors in avian song development.