Abstract Vocal learning in songbirds is mediated by a highly localized system of interconnected forebrain regions, including recurrent loops that traverse the cortex, basal ganglia, and thalamus. This brain-behavior system provides a powerful model for elucidating mechanisms of vocal learning, with implications for learning speech in human infants, as well as for advancing our understanding of skill learning in general. A long history of experiments in this area has tested neural responses to playback of different song stimuli in anesthetized birds at different stages of vocal development. These studies have demonstrated selectivity for different song types that provide neural signatures of learning. In contrast to the ease of obtaining responses to song playback in anesthetized birds, song-evoked responses in awake birds are greatly reduced or absent, indicating that behavioral state is an important determinant of neural responsivity. Song-evoked responses can be elicited during sleep as well as anesthesia, and the selectivity of responses to song playback in adult birds is highly similar between anesthetized and sleeping states, encouraging the idea that anesthesia and sleep are similar. In contrast to that idea, we report evidence that cortical responses to song playback in juvenile zebra finches ( Taeniopygia guttata ) differ greatly between sleep and urethane anesthesia. This finding indicates that behavioral states differ in sleep versus anesthesia and raises questions about relationships between developmental changes in sleep activity, selectivity for different song types, and the neural substrate for vocal learning.
more »
« less
Prenatal exposure to incubation calls affects song learning in the zebra finch
Songbirds are important models for understanding the mechanisms and fitness consequences of imitative vocal learning. Although the effects of early-life environmental and social conditions on song learning are well-established, the impact of early sound exposure has received surprisingly little attention. Yet recent evidence hints at auditory sensitivity in songbird embryos, including in the zebra finch (
- NSF-PAR ID:
- 10153243
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- Scientific Reports
- Volume:
- 8
- Issue:
- 1
- ISSN:
- 2045-2322
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
more » « less
Abstract Vocal learning in songbirds is mediated by cortico‐basal ganglia circuits that govern diverse functions during different stages of development. We investigated developmental changes in axonal projections to and from motor cortical regions that underlie learned vocal behavior in juvenile zebra finches (
Taeniopygia guttata ). Neurons in LMAN‐core project to RA, a motor cortical region that drives vocal output; these RA‐projecting neurons send a transient collateral projection to AId, a region adjacent to RA, during early vocal development. Both RA and AId project to a region of dorsal thalamus (DLM), which forms a feedback pathway to cortico‐basal ganglia circuitry. These projections provide pathways conveying efference copy and a means by which information about vocal motor output could be reintegrated into cortico‐basal ganglia circuitry, potentially aiding in the refinement of juvenile vocalizations during learning. We used tract‐tracing techniques to label the projections of LMAN‐core to AId and of RA to DLM in juvenile songbirds. The volume and density of terminal label in the LMAN‐core→AId projection declined substantially during early stages of sensorimotor learning. In contrast, the RA→DLM projection showed no developmental change. The retraction of LMAN‐core→AId axon collaterals indicates a loss of efference copy to AId and suggests that projections that are present only during early stages of sensorimotor learning mediate unique, temporally restricted processes of goal‐directed learning. Conversely, the persistence of the RA→DLM projection may serve to convey motor information forward to the thalamus to facilitate song production during both learning and maintenance of vocalizations. -
more » « less
Many social animals can recognize other individuals by their vocalizations. This requires a memory system capable of mapping incoming acoustic signals to one of many known individuals. Using the zebra finch, a social songbird that uses songs and distance calls to communicate individual identity (Elie and Theunissen, 2018), we tested the role of two cortical-like brain regions in a vocal recognition task. We found that the rostral region of the Cadomedial Nidopallium (NCM), a secondary auditory region of the avian pallium, was necessary for maintaining auditory memories for conspecific vocalizations in both male and female birds, whereas HVC (used as a proper name), a premotor areas that gates auditory input into the vocal motor and song learning pathways in male birds (Roberts and Mooney, 2013), was not. Both NCM and HVC have previously been implicated for processing the tutor song in the context of song learning (Sakata and Yazaki-Sugiyama, 2020). Our results suggest that NCM might not only store songs as templates for future vocal imitation but also songs and calls for perceptual discrimination of vocalizers in both male and female birds. NCM could therefore operate as a site for auditory memories for vocalizations used in various facets of communication. We also observed that new auditory memories could be acquired without intact HVC or NCM but that for these new memories NCM lesions caused deficits in either memory capacity or auditory discrimination. These results suggest that the high-capacity memory functions of the avian pallial auditory system depend on NCM.
SIGNIFICANCE STATEMENT Many aspects of vocal communication require the formation of auditory memories. Voice recognition, for example, requires a memory for vocalizers to identify acoustical features. In both birds and primates, the locus and neural correlates of these high-level memories remain poorly described. Previous work suggests that this memory formation is mediated by high-level sensory areas, not traditional memory areas such as the hippocampus. Using lesion experiments, we show that one secondary auditory brain region in songbirds that had previously been implicated in storing song memories for vocal imitation is also implicated in storing vocal memories for individual recognition. The role of the neural circuits in this region in interpreting the meaning of communication calls should be investigated in the future. -
more » « less
ABSTRACT Learned vocalizations are important for communication in some vertebrate taxa. The neural circuitry for the learning and production of vocalizations is well known in songbirds, many of which learn songs initially during a critical period early in life. Dopamine is essential for motor learning, including song learning, and dopamine‐related measures change throughout development in song‐control regions such as HVC, the lateral magnocellular nucleus of the anterior nidopallium (LMAN), Area X, and the robust nucleus of the arcopallium (RA). In mammals, the neuropeptide neurotensin strongly interacts with dopamine signaling. This study investigated a potential role for the neurotensin system in song learning by examining how neurotensin (
Nts ) and neurotensin receptor 1 (Ntsr1 ) expression change throughout development.Nts andNtsr1 mRNA expression was analyzed in song‐control regions of male zebra finches in four stages of the song learning process: pre‐subsong (25 days posthatch; dph), subsong (45 dph), plastic song (60 dph), and crystallized song (130 dph).Nts expression in LMAN during the subsong stage was lower compared to other time points.Ntsr1 expression was highest in HVC, Area X, and RA during the pre‐subsong stage. Opposite and complementary expression patterns for the two genes in song nuclei and across the whole brain suggest distinct roles for regions that produce and receiveNts . The expression changes at crucial time points for song development are similar to changes observed in dopamine studies and suggestNts may be involved in the process of vocal learning. © 2018 Wiley Periodicals, Inc. Develop Neurobiol 78: 671–686, 2018 -
more » « less
Abstract In a rapidly warming world, exposure to high temperatures may impact fitness, but the gene regulatory mechanisms that link sublethal heat to sexually selected traits are not well understood, particularly in endothermic animals. Our experiment used zebra finches (
Taeniopygia guttata ), songbirds that experience extreme temperature fluctuations in their native Australia. We exposed captive males to an acute thermal challenge (43°C) compared with thermoneutral (35°C) and lower (27°C) temperatures. We found significantly more heat dissipation behaviours at 43°C, a temperature previously shown to reduce song production and fertility, and more heat retention behaviours at 27°C. Next, we characterized transcriptomic responses in tissues important for mating effort—the posterior telencephalon, for its role in song production, and the testis, for its role in fertility and hormone production. Differential expression of hundreds of genes in the testes, but few in the brain, suggests the brain is less responsive to extreme temperatures. Nevertheless, gene network analyses revealed that expression related to dopaminergic signalling in the brain covaried with heat dissipation behaviours, providing a mechanism by which temporary thermal challenges may alter motivational circuits for song production. In both brain and testis, we observed correlations between thermally sensitive gene networks and individual differences in thermoregulatory behaviour. Although we cannot directly relate these gene regulatory changes to mating success, our results suggest that individual variation in response to thermal challenges could impact sexually selected traits in a warming world.
