Rapid encoding of an internal model for imitative learning

As in human infant speech development, vocal imitation in songbirds involves sensory acquisition and memorization of adult-produced vocal signals, followed by a protracted phase of vocal motor practice. The internal model of adult tutor song in the juvenile male brain, termed ‘the template’, is central to the vocal imitation process. However, even the most fundamental aspects of the template, such as when, where and how it is encoded in the brain, remain poorly understood. A major impediment to progress is that current studies of songbird vocal learning use protracted tutoring over days, weeks or months, complicating dissection of the template encoding process. Here, we take the key step of tightly constraining the timing of template acquisition. We show that, in the zebra finch, template encoding can be time locked to, on average, a 2 h period of juvenile life and based on just 75 s of cumulative tutor song exposure. Crucially, we find that vocal changes occurring on the day of training correlate with eventual imitative success. This paradigm will lead to insights on how the template is instantiated in the songbird brain, with general implications for deciphering how internal models are formed to guide learning of complex social behaviours.     

Basal metabolic rate: heritability and genetic correlations with morphological traits in the zebra finch

Studies of genetic variation in metabolic traits have so far not focused on birds. In our study population of captive zebra finches we found evidence for a significant heritable genetic component in basal metabolic rate (BMR). Heritability of all morphological traits investigated (body mass, head length, tars length and wing length) was significantly larger than zero. All traits were positively phenotypically correlated. Eight of 10 genetic correlations presented in this study differed significantly from zero, all being positive, suggesting the possibility of correlated responses to any selection acting on the traits. When conditioned on the genetic variance in body mass, the heritability of BMR was reduced from 25% to 4%. Hence, our results indicate that genetic changes in BMR through directional selection are possible, but the potential for adaptation independent of body mass may be limited.     

Distribution and developmental change in [3H]MK-801 binding within zebra finch song nuclei

In many songbirds, vocal learning depends upon appropriate auditory experience during a sensitive period that coincides with the formation and reorganization of song-related neural pathways. Because some effects of early sensory experience on neural organization and early learning have been linked to activation of N-methyl-d-aspartate (NMDA) receptors, we measured binding to this receptor within the neural system controlling song behavior in zebra finches. Quantitative autoradiography was used to measure binding of the noncompetitive antagonist [³H]MK-801 (dizocilpine) in the brains of both adult and juvenile male zebra finches, focusing on four telencephalic regions implicated in song learning and production. Overall, the pattern of MK-801 binding in zebra finches was similar to the pattern found in rats (Monaghan and Cotman, 1985, J. Neurosci. 5:2909–2919; Sakurai, Cha, Penney, and Young, 1991, Neuroscience 40:533–543). That is, binding was highest in the telencephalon, intermediate in thalamic regions, and virtually absent from the brain stem and cerebellum. The telencephalic song areas exhibited intermediate levels of binding, and binding in the juveniles was not significantly different from adult levels in most song nuclei. However, in the lateral magnocellular nucleus of the anterior neostriatum (IMAN), binding at 30 days of age was significantly higher than binding in adults. Given the established role of NMDA receptors in other developing neural systems, both their presence in song control nuclei and their developmental regulation within a region implicated in song learning suggest that NMDA receptors play a role in mediating effects of auditory experience on the development of song behavior.     

He hears,she hears: Are there sex differences in auditory processing?

Songbirds learn individually unique songs through vocal imitation and use them in courtship and territorial displays. Previous work has identified a forebrain auditory area, the caudomedial nidopallium (NCM), that appears specialized for discriminating and remembering conspecific vocalizations. In zebra finches (ZFs), only males produce learned vocalizations, but both sexes process these and other signals. This study assessed sex differences in auditory processing by recording extracellular multiunit activity at multiple sites within NCM. Juvenile female ZFs (n = 46) were reared in individual isolation and artificially tutored with song. In adulthood, songs were played back to assess auditory responses, stimulus‐specific adaptation, neural bias for conspecific song, and memory for the tutor's song, as well as recently heard songs. In a subset of females (n = 36), estradiol (E2) levels were manipulated to test the contribution of E2, known to be synthesized in the brain, to auditory responses. Untreated females (n = 10) showed significant differences in response magnitude and stimulus‐specific adaptation compared to males reared in the same paradigm (n = 9). In hormone‐manipulated females, E2 augmentation facilitated the memory for recently heard songs in adulthood, but neither E2 augmentation (n = 15) nor E2 synthesis blockade (n = 9) affected tutor song memory or the neural bias for conspecific song. The results demonstrate subtle sex differences in processing communication signals, and show that E2 levels in female songbirds can affect the memory for songs of potential suitors, thus contributing to the process of mate selection. The results also have potential relevance to clinical interventions that manipulate E2 in human patients. © 2014 Wiley Periodicals, Inc. Develop Neurobiol 75: 302–314, 2015     

Early isolation from conspecific song does not affect the normal developmental decline of N-methyl-D-aspartate receptor binding in an avian song nucleus

Early effects of experience on synaptic reorganization and behavior often involve activation of N-methyl-D -aspartate (NMDA) receptors. We have begun to explore the role of this glutamate-receptor subtype in the development of learned birdsong. Song learning in zebra finches occurs during a restricted period that coincides with extensive synaptic reorganization within neural regions controlling song behavior. In one brain region necessary for song learning, the lateral magnocellular nucleus of the anterior neostriatum (lMAN), NMDA receptor binding is twice as high at the onset of song learning as in adulthood. In the present study, we used quantitative autoradiography with the noncompetitive NMDA antagonist [³H]MK-801 to examine more closely the developmental decline in NMDA receptor binding within lMAN and found that it occurred gradually over the period of song learning and was not associated with a particular stage of the learning process. In addition, early isolation from conspecific song did not affect [³H]MK-801 binding in lMAN at 30, 60, or 80 days. Since behavioral studies confirmed that our isolate rearing conditions extended the sensitive period for song learning, we conclude that the normal developmental decline in overall NMDA receptor binding within lMAN does not terminate the capacity for song learning. Finally, early deafening, which prevents both stages of song learning, also did not affect [³H]MK-801 binding in lMAN at 80 days, indicating that the decline in NMDA receptor binding occurs in the absence of auditory experiences associated with song development. © 1995 John Wiley & Sons, Inc.     

Temporal patterning of song production: Participation of nucleus uvaeformis of the thalamus

Birdsong is a learned vocal behavior used in intraspecific communication. The motor pathway serving learned vocalizations includes the forebrain nuclei NIf, HVC, and RA; RA projects to midbrain and brain stem areas that control the temporal and acoustic features of song. Nucleus Uvaeformis of the thalamus (Uva) sends input to two of these forebrain nuclei (NIf and HVC) but has not been thought to be important for song production. We used three experimental approaches to reexamine Uva's function in adult male zebra finches. (1) Electrical stimulation applied to Uva activated HVC and the vocal motor pathway, including tracheosyringeal motor neurons that innervate the bird's vocal organ. (2) Bilateral lesions of Uva including the dorso-medial portion of the nucleus affected the normal temporal organization of song. (3) Chronic multiunit recordings from Uva during normal song and calls show bursts of premotor activity that lead the onset of some song components, and also larger bursts that mark the end of complete song motifs. These results implicate Uva in the production of learned vocalizations, and further suggest that Uva contributes more to the temporal structure than to the acoustic characteristics of song. © 1993 John Wiley & Sons, Inc.